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March 22, 2022; 98 (12) Research Article

Postganglionic Sudomotor Assessment in Early Stage of Multiple System Atrophy and Parkinson Disease

A Morpho-functional Study

View ORCID ProfileVincenzo Provitera, Valeria Iodice, Fiore Manganelli, Stefania Mozzillo, View ORCID ProfileGiuseppe Caporaso, Annamaria Stancanelli, Ilaria Borreca, Marcello Esposito, Raffaele Dubbioso, Rosa Iodice, Floriana Vitale, View ORCID ProfileShiwen Koay, Ekawat Vichayanrat, Fernanda Valerio, Lucio Santoro, Maria Nolano
First published January 11, 2022, DOI: https://doi.org/10.1212/WNL.0000000000013300
Vincenzo Provitera
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Valeria Iodice
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Fiore Manganelli
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Stefania Mozzillo
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Giuseppe Caporaso
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Annamaria Stancanelli
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Ilaria Borreca
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Marcello Esposito
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Raffaele Dubbioso
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Rosa Iodice
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Floriana Vitale
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Shiwen Koay
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Ekawat Vichayanrat
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Fernanda Valerio
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Lucio Santoro
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Maria Nolano
From the Neurology Department (V.P., S.M., G.C., A.S., I.B., M.N.), Skin Biopsy Laboratory, Istituti Clinici Scientifici Maugeri IRCCS, Telese Terme, Italy; Department of Brain, Repair and Rehabilitation (V.I., S.K.), University College London Queen Square Institute of Neurology; Autonomic Unit (V.I., S.K., E.V., F. Valerio), National Hospital for Neurology and Neurosurgery, London, UK; Department of Neurosciences, Reproductive Sciences and Odontostomatology (F.M., R.D., R.I., F. Vitale, L.S., M.N.), University Federico II of Naples; and Clinical Neurophysiology Unit (M.E.), Cardarelli Hospital, Naples, Italy.
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Postganglionic Sudomotor Assessment in Early Stage of Multiple System Atrophy and Parkinson Disease
A Morpho-functional Study
Vincenzo Provitera, Valeria Iodice, Fiore Manganelli, Stefania Mozzillo, Giuseppe Caporaso, Annamaria Stancanelli, Ilaria Borreca, Marcello Esposito, Raffaele Dubbioso, Rosa Iodice, Floriana Vitale, Shiwen Koay, Ekawat Vichayanrat, Fernanda Valerio, Lucio Santoro, Maria Nolano
Neurology Mar 2022, 98 (12) e1282-e1291; DOI: 10.1212/WNL.0000000000013300

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Abstract

Background and Objectives Sudomotor impairment has been recognized as a key feature in differentiating Parkinson disease (PD) and multiple system atrophy–parkinsonian type (MSA-P), with the latter characterized by diffuse anhidrosis in prospective study, including patients in late stage of disease. We aimed to evaluate morphologic and functional postganglionic sudomotor involvement in patients with newly diagnosed MSA-P and PD to identify possible biomarkers that might be of help in differentiating the 2 conditions in the early stage.

Methods One hundred patients with parkinsonism within 2 years from onset of motor symptoms were included in the study. At the time of recruitment, questionnaires to assess nonmotor, autonomic, and small fiber symptoms were administered, and patients underwent postganglionic sudomotor function assessment by the dynamic sweat test and punch skin biopsy from the distal leg. Skin samples were processed for indirect immunofluorescence with a panel of antibodies, including noradrenergic and cholinergic markers. The density of intraepidermal, sudomotor, and pilomotor nerve fibers was measured on confocal images with dedicated software. A follow-up visit 12 months after recruitment was performed to confirm the diagnosis.

Results We recruited 57 patients with PD (M/F 36/21, age 63.5 ± 9.4 years) and 43 patients with MSA-P (M/F 27/16, age 62.3 ± 9.0 years). Clinical scales and questionnaires showed a more severe clinical picture in patients with MSA-P compared to those with PD. Sweating output and intraepidermal, pilomotor, and sudomotor nerve densities, compared to controls, were lower in both groups but with a greater impairment in patients with MSA-P. Pilomotor and sudomotor nerve density correlated with sweating function and with nonmotor clinical symptoms. A composite sudomotor parameter defined as the arithmetic product of sweat production multiplied by the density of sudomotor fibers efficiently separated the 2 populations; the receiver operating characteristics curve showed an area under the curve of 0.83.

Discussion Dynamic sweat test and the quantification of cutaneous autonomic nerves proved to be a sensitive morpho-functional approach to assess the postganglionic component of the sudomotor pathway, revealing a more severe involvement in MSA-P than in PD early in the disease course. This approach can be applied to differentiate the 2 conditions early.

Classification of Evidence This study provides Class II evidence that postganglionic sudomotor morpho-functional assessment accurately distinguish patients with PD from patients with MSA-P.

Glossary

COMPASS-31=
Composite Autonomic Symptom Score;
CSP=
composite sudomotor parameter;
DST=
dynamic sweat test;
H&Y=
Hoehn and Yahr;
IENF=
intraepidermal nerve fiber;
MDS-UPDRS=
Movement Disorders Society Unified Parkinson’s Disease Rating Scale;
MSA=
multiple system atrophy;
MSA-P=
MSA-parkinsonian type;
NMSS=
Nonmotor Symptoms Scale;
PD=
Parkinson disease;
PD-OH=
PD with orthostatic hypotension;
QSART=
quantitative sudomotor axon reflex test;
SFN-SIQ=
Small Fiber Neuropathy Symptoms Inventory Questionnaire;
SSR=
sympathetic skin response

Footnotes

  • Go to Neurology.org/N for full disclosures. Funding information and disclosures deemed relevant by the authors, if any, are provided at the end of the article.

  • Class of Evidence: NPub.org/coe

  • Received June 22, 2021.
  • Accepted in final form December 27, 2021.
  • © 2022 American Academy of Neurology
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