Vol.:(0123456789)1 3

Journal of Neurology (2020) 267:3121–3127 https://doi.org/10.1007/s00415-020-09986-y

LETTER TO THE EDITORS

Mixed central and peripheral nervous system disorders in severe SARS‑CoV‑2 infection

H. Chaumont1,2,3  · A. San‑Galli1 · F. Martino2,4 · C. Couratier1 · G. Joguet5 · M. Carles2,4 · E. Roze3,6 · A. Lannuzel1,2,3,7

Received: 3 June 2020 / Revised: 5 June 2020 / Accepted: 8 June 2020 / Published online: 12 June 2020 © Springer-Verlag GmbH Germany, part of Springer Nature 2020

Dear Sirs,

We report four cases of severe COVID-19 in male patients aged 50–70 with the combination of central and peripheral nervous system disorders occurring unexpectedly late after the first symptoms. Patients had comorbidities and were admitted for acute respiratory distress syndrome due to a proven SARS-CoV-2 infection. All required mechanical ven-tilation, among whom one needed an extracorporeal mem-brane oxygenation support.

Several acute neurological syndromes have been associ-ated with SARS-CoV-2 infection, including anosmia and ageusia [1, 2], meningoencephalitis [3, 4], acute hemor-rhagic necrotizing encephalopathy [5], axonal or demyeli-nating polyradiculoneuropathy [6–8], polyneuritis cranialis

[8]. Like in most of the viral infections that involve nervous system, these manifestations occurred within the first ten days after infectious symptoms. Further away from the onset of the disease, when sedation and neuromuscular blocker were withheld, 67% of the patients with severe COVID-19 develop encephalopathy including prominent agitation, con-fusion and corticospinal tract signs [9].

In our cases neurological manifestations were detected after mechanical ventilation weaning and extubation (Fig. 1). They consisted of miscellaneous symptoms such as confusion, cognitive dysfunction (memory deficit, frontal syndrome), psychiatric disorders (paranoid delusion, hal-lucinations), weakness, pyramidal signs, dysautonomia, swallowing dysfunction, vertical supranuclear eye palsy, upper limbs myoclonus, fasciculation and focal muscle atrophy (Table 1). To note, before admission to intensive care unit, patients had no neurological symptom, except for anosmia or ageusia in two of them. One patient had a small acute sub-cortical ischemic stroke on brain MRI. Cerebro-spinal fluid (CSF) analysis showed a normal cell count and a moderate increase of protein level in the up to 80 mg/L in two cases. RT-PCR and IgM for SARS-CoV-2 in the CSF were negative in all patients. On EEG, non-rhythmic frontal slow waves were observed in two patients. Three patients had electrophysiological features of acute motor demyeli-nating polyradiculoneuropathy with delayed distal latencies and F-waves, slowed conduction velocities and conduction blocks (Supplementary Table). The remaining patient had lower motor neuron features in both the upper and lower limbs. Two patients had an additional decrease of senso-rimotor potential amplitude compatible with a critical ill-ness neuropathy. Swallowing and eye movement improved within the first week. Given the persistent muscle weakness and electromyographic features suggesting a post-infectious mechanism, an immunoglobulin therapy was introduced for 5 days. Psychiatric symptoms, cognitive impairment and dysautonomia improved thereafter, but myoclonus and motor weakness of the upper limbs persisted 3 weeks after

Electronic supplementary material The online version of this article (https ://doi.org/10.1007/s0041 5-020-09986 -y) contains supplementary material, which is available to authorized users.

* H. Chaumont hugo.chaumont@chu-guadeloupe.fr

1 Centre Hospitalier Universitaire de la Guadeloupe, Service de Neurologie, 97139 Pointe-à-Pitre/Abymes, France

2 Faculté de Médecine, Université Des Antilles, Pointe-à-Pitre, France

3 Institut National de La Santé Et de La Recherche Médicale, CNRS, Unité Mixte de Recherche (UMR) 7225, Institut du Cerveau Et de La Moelle épinière, ICM, Faculté de Médecine de Sorbonne Université, U 1127, Paris, France

4 Centre Hospitalier Universitaire de La Guadeloupe, Service de Réanimation, Pointe-à-Pitre/Abymes, France

5 Laboratoire de Biologie de La Reproduction, Centre Hospitalier Universitaire de La Guadeloupe, Pointe-à-Pitre/Abymes, France

6 AP-HP, Hôpital de La Pitié-Salpêtrière, Département de Neurologie, Paris, France

7 Centre D’investigation Clinique Antilles Guyane, Inserm CIC 1424, Pointe-à-Pitre, France

3122 Journal of Neurology (2020) 267:3121–3127

1 3

discharge. Three patients required prolonged rehabilitation in a specialized center.

We describe here delayed mixed central and periph-eral disorders as a complication of severe COVID-19. It combines acute encephalopathy and motor demyelinat-ing polyradiculoneuropathy or diffuse lower motor neuron involvement. Persistent cognitive and motor deficit might result from a critical illness, but neurological features differ from critical illness-related encephalopathy and neuropathy.

Critical illness-related neuropathy is characterized by a bilateral, symmetric, axonal sensorimotor polyneuropathy resulting in an areflexic tetraplegia, without dysautonomia or cranial nerves palsy. In our patients, clinical and neuro-physiological features of peripheral nervous system involve-ment could partly reflect critical illness neuropathy but most of them are not expected in this context and are thus more likely linked to COVID-19. Abnormal eye movement, swal-lowing dysfunction and action myoclonus are unusual in

Fig. 1 Timelines showing general and neurological symptoms onset, timing of hospital admission and discharge, timing of ICU admis-sion and discharge, and paraclinical examinations and treatments. EEG, electroencephalogram; EMG electromyogram; ICU intensive care unit; IVIg intravenous immunoglobulin; MRI magnetic reso-

nance imagery. P1: Patient 1 (M, 62 y.o), P2: Patient 2 (M, 72 y.o), P3: Patient 3 (M, 50 y.o), P4: Patient 4 (M, 66 y.o). For P2, cerebral and spinal MRI were performed at two different dates (days 49 and 62, respectively)

3123Journal of Neurology (2020) 267:3121–3127

1 3

Tabl

e 1

Cha

ract

erist

ics a

nd m

anag

emen

t of s

ever

e CO

VID

-19

patie

nts p

rese

ntin

g w

ith m

ixed

cen

tral a

nd p

erip

hera

l neu

rolo

gica

l man

ifest

atio

ns

ID a

ge se

xC

omor

bidi

ties

Del

ay b

etw

een

inau

gura

l sy

mpt

oms a

nd

adm

issi

on to

:

Inau

gura

l sy

mpt

oms

Neu

rolo

gic

feat

ures

at

eval

uatio

na

MR

IEE

GEM

G (m

ain

feat

ures

)SA

RS-

CoV

-2 R

T-PC

R S

erol

ogya

CSF

b WC

C/

Prot

ein

mg/

L SA

RS-

CoV

-2

tests

Seve

rity

of

AR

DSc a

nd

med

ical

car

e

1, 6

2, M

Hyp

erte

nsio

n,

diab

etes

mel

-lit

us

Hos

pita

l: 10

 day

s, IC

U: 1

2 da

ys

Feve

r, co

ugh,

ag

eusi

a,

dysp

nea

Con

fusi

on,

dyse

xecu

tive

synd

rom

e,

mem

ory

defic

it,

swal

low

ing

diso

rder

s, le

ft fa

cial

pal

sy,

right

UL

wea

k-ne

ss (2

/5) w

ith

bila

tera

l atro

phy

of th

e fir

st pa

l-m

ar in

tero

sse-

ous,

left

UL

and

LL st

reng

th 4

/5,

atax

ia, p

ostu

ral

and

actio

n m

yo-

clon

us, l

ower

lim

b ar

eflex

ia,

uppe

r lim

b hy

perr

eflex

ia,

dysa

uton

omia

d , G

SC 1

5, m

RS

5 (a da

y 21

)

Rece

nt

isch

emic

str

oke

in

right

mid

dle

cere

bral

ar

tery

terr

i-to

ry (B

rain

M

RI)

Nor

-m

al sp

inal

co

rd M

RI

Glo

bal s

low

-in

g (5

–6 H

z)

Bila

tera

l an

d fro

ntal

, di

spha

sic,

no

n-pe

riodi

c sl

ow a

ctiv

ity

(2 H

z)

Dem

yelin

atin

g as

ymm

et-

ric m

otor

po

lyra

dicu

lo

neur

opat

hy

and

mod

er-

ate

axon

al

sens

orim

otor

ne

urop

athy

of

the

four

lim

bs

Posi

tive

RT-P

CR

in

naso

phar

ynge

al

swab

, + Ig

M, +

IgG

in

pla

sma

(a day

13)

0 / 4

5 ne

gativ

e RT

-PC

R,-

IgM

, + Ig

G,

No

intra

the-

cal s

ynth

esis

Mild

AR

DSe

Hyd

roxy

-ch

loro

quin

e su

lfate

600

 mg

Azi

thro

myc

in

250 

mg,

ICU

, V,

no

PP,

IVIg

0.4

 g/

kg, R

ehab

ilita

-tio

n ce

nter

af

ter 3

6 da

ys,

mR

S 2

3124 Journal of Neurology (2020) 267:3121–3127

1 3

Tabl

e 1

(con

tinue

d)

ID a

ge se

xC

omor

bidi

ties

Del

ay b

etw

een

inau

gura

l sy

mpt

oms a

nd

adm

issi

on to

:

Inau

gura

l sy

mpt

oms

Neu

rolo

gic

feat

ures

at

eval

uatio

na

MR

IEE

GEM

G (m

ain

feat

ures

)SA

RS-

CoV

-2 R

T-PC

R S

erol

ogya

CSF

b WC

C/

Prot

ein

mg/

L SA

RS-

CoV

-2

tests

Seve

rity

of

AR

DSc a

nd

med

ical

car

e

2, 7

2, M

Hyp

erte

nsio

n,

Dia

bete

s mel

-lit

us, O

besi

ty,

(BM

I = 31

.5),

Uro

thel

ial

carc

inom

a in

re

mis

sion

Hos

pi-

tal:1

5 da

ys,

ICU

: 17 

days

Feve

r, co

ugh,

dy

spne

aC

onfu

sion

, par

a-no

id d

elus

ion,

vi

sual

and

aud

i-to

ry h

allu

cina

-tio

ns, f

ront

al

synd

rom

e,

mem

ory

defic

it,

swal

low

ing

diso

rder

s, te

trapa

resi

s (U

L an

d LL

stre

ngth

2/

5), a

taxi

a, U

L re

st, p

ostu

ral

and

actio

n m

yocl

onus

, sl

owin

g of

ey

e m

ovem

ent

sacc

ades

, fou

r lim

bs h

yper

re-

flexi

a an

d ne

u-ro

geni

c pa

in,

dysa

uton

omia

d , G

SC 1

4, m

RS

5 (a da

y 44

)

Nor

mal

bra

in

and

spin

al

cord

MR

I

Glo

bal s

low

-in

g (5

–6 H

z)D

emye

linat

ing

mot

or p

oly-

radi

culo

neu-

ropa

thy

and

mod

erat

e to

se

vere

axo

nal

sens

orim

otor

ne

urop

athy

of

the

four

lim

bs

Posi

tive

RT-P

CR

in

naso

phar

ynge

al

swab

, + Ig

M,—

IgG

in

pla

sma,

(a day

18)

0 / 7

4,

nega

tive

RT-P

CR

,—Ig

M, +

IgG

, N

o in

trath

e-ca

l syn

thes

is

Mild

to m

oder

-at

e A

RD

Se H

ydro

xych

lo-

roqu

ine

sulfa

te

600 

mg,

A

zith

rom

ycin

25

0 m

gQ

T pr

olon

ga-

tion,

Pre

ga-

balin

300

 mg

per d

ay, I

CU

, V,

no

PP IV

Ig

0.4 

g/kg

, Re

habi

lita-

tion

cent

er

afte

r 50 

days

, m

RS

4

3125Journal of Neurology (2020) 267:3121–3127

1 3

Tabl

e 1

(con

tinue

d)

ID a

ge se

xC

omor

bidi

ties

Del

ay b

etw

een

inau

gura

l sy

mpt

oms a

nd

adm

issi

on to

:

Inau

gura

l sy

mpt

oms

Neu

rolo

gic

feat

ures

at

eval

uatio

na

MR

IEE

GEM

G (m

ain

feat

ures

)SA

RS-

CoV

-2 R

T-PC

R S

erol

ogya

CSF

b WC

C/

Prot

ein

mg/

L SA

RS-

CoV

-2

tests

Seve

rity

of

AR

DSc a

nd

med

ical

car

e

3, 5

0, M

Dia

bete

s mel

-lit

usH

ospi

tal:

18 d

ays,

ICU

:20 

days

Cou

gh, d

ysp-

nea

Con

fusi

on,

para

noid

del

u-si

on, f

ront

al

synd

rom

e,

mem

ory

defic

it,

swal

low

ing

diso

rder

s, te

tra-

pare

sis,

(UL

stren

gth

2/5

and

LL st

reng

th

3/5)

, bila

tera

l at

roph

y of

the

first

palm

ar

inte

ross

eous

, at

axia

, UL

rest,

pos

tura

l an

d ac

tion

myo

clon

us,

slow

ing

of

eye

mov

emen

t sa

ccad

es, f

our

limbs

hyp

erre

-fle

xia,

bila

tera

l an

kle

clon

us,

dysa

uton

omia

d , G

SC 1

4, m

RS

5 (a da

y 54

)

Nor

mal

bra

in

and

spin

al

cord

MR

I

Poste

rior a

nd

met

ric g

loba

l sl

owin

g (6

 Hz)

bila

t-er

al fr

onta

l pa

roxy

smal

sl

ow, d

elta

w

aves

Low

er m

otor

ne

uron

in

volv

emen

t w

ith d

ener

-va

tion

of th

e fo

ur li

mbs

, no

rmal

m

otor

evo

ked

pote

ntia

l am

plitu

de

Posi

tive

RT-P

CR

in

naso

phar

ynge

al

swab

+ Ig

M, +

IgG

in

pla

sma

(a day

19)

5 / 8

1 ne

gativ

e RT

-PC

R—

IgM

, + Ig

G,

No

intra

the-

cal s

ynth

esis

Mod

erat

e to

se

vere

AR

DSe,

H

ydro

xych

lo-

roqu

ine

sulfa

te

600 

mg,

A

zith

rom

ycin

25

0 m

gM

ethy

lpre

dni-

solo

ne 1

 g,

ICU

, EC

MO

, V,

PP

(× 1)

, IV

Ig 0

.4 g

/kg

, Reh

abili

ta-

tion

cent

er

afte

r 76 

days

, m

RS

4

3126 Journal of Neurology (2020) 267:3121–3127

1 3

Tabl

e 1

(con

tinue

d)

ID a

ge se

xC

omor

bidi

ties

Del

ay b

etw

een

inau

gura

l sy

mpt

oms a

nd

adm

issi

on to

:

Inau

gura

l sy

mpt

oms

Neu

rolo

gic

feat

ures

at

eval

uatio

na

MR

IEE

GEM

G (m

ain

feat

ures

)SA

RS-

CoV

-2 R

T-PC

R S

erol

ogya

CSF

b WC

C/

Prot

ein

mg/

L SA

RS-

CoV

-2

tests

Seve

rity

of

AR

DSc a

nd

med

ical

car

e

4, 6

6, M

Obs

truct

ive

slee

p ap

nea

synd

rom

e

Hos

pita

l: 10

 day

s, IC

U: 1

2 da

ys

Cou

gh,

Dys

pnea

, A

nosm

ia,

Dia

rrhe

a

Con

fusi

on, p

ara-

noid

del

usio

n,

visu

al h

allu

ci-

natio

ns, f

ront

al

synd

rom

e,

mem

ory

defic

it,

tetra

pare

sis (

UL

and

LL st

reng

th

3/5)

, ata

xia,

U

L po

stura

l an

d ac

tion

myo

clon

us, U

L hy

perr

eflex

ia,

LL a

refle

xia,

dy

saut

onom

iad ,

GSC

15,

mR

S 4

(a day

42)

Nor

mal

bra

in

and

spin

al

cord

MR

I

Nor

mal

Dem

yelin

at-

ing

mot

or

poly

radi

culo

ne

urop

athy

of

the

four

lim

bs

Posi

tive

RT-P

CR

in

naso

phar

ynge

al

swab

,—Ig

M, +

IgG

in

pla

sma

(a day

10)

1 / 2

2,

nega

tive

RT-P

CR

,- Ig

M, +

IgG

, N

o in

trath

e-ca

l syn

thes

is

Mild

to se

vere

A

RD

Se,

Hyd

roxy

chlo

-ro

quin

e su

lfate

60

0 m

g,

Azi

thro

myc

in

250 

mg

(day

11

–18)

Met

h-yl

pred

niso

lone

1 

g (d

ay 2

0 to

26)

ICU

, V,

PP

(× 6)

IV

Ig 0

.4 g

/kg,

D

isch

arge

d at

hom

e af

ter

40 d

ays

mR

S 2

BMI b

ody

mas

s ind

ex; C

SF c

ereb

rosp

inal

flui

d; E

CM

O e

xtra

corp

orea

l mem

bran

e ox

ygen

atio

n; E

EG e

lect

roen

ceph

alog

ram

; EM

G e

lect

rom

yogr

am; G

SC G

lasg

ow sc

ale;

ICU

inte

nsiv

e ca

re u

nit;

IgM

imm

unog

lobu

lin M

; IgG

imm

unog

lobu

lin G

; IVI

g in

trave

nous

imm

unog

lobu

lin; L

L lo

wer

lim

b; U

L up

per l

imb;

MRI

mag

netic

reso

nanc

e im

agin

g; m

RS,

mod

ified

Ran

kin

Scal

e; N

A no

t ap

plic

able

; PP

pron

e po

sitio

n; R

T-PC

R re

al-ti

me

poly

mer

ase

chai

n re

actio

n; V

mec

hani

cal v

entil

atio

n; W

CC

whi

te c

ell c

ount

(µL)

a Tim

e af

ter i

naug

ural

sym

ptom

sb C

ereb

rosp

inal

flui

d an

alys

is w

as p

erfo

rmed

at t

he ti

me

of n

euro

logi

cal e

xam

inat

ion

c Seve

re A

cute

Res

pira

tory

Dist

ress

Syn

drom

e (A

RD

S): P

aO2/

FiO

2 < 10

0; m

oder

ate

ARD

S: P

aO2/

FiO

2 < 20

0; m

ild, A

RDS:

PaO

2/Fi

O2 <

300;

PaO

2/Fi

O2

ratio

was

cal

cula

ted

usin

g th

e ar

teria

l Pr

essu

re o

f oxy

gen

(PaO

2) a

nd th

e fr

actio

n of

insp

ired

oxyg

en (F

iO2)

in m

echa

nica

l ven

tilat

ed p

atie

nts

d Dys

auto

nom

ia: o

rthos

tatic

hyp

oten

sion

, con

stipa

tion

e Patie

nt 1

(PaO

2/Fi

O2)

: day

1: 2

08, d

ay 2

: 280

, day

3: 2

40, d

ay 7

: 218

; Pat

ient

2 (P

aO2/

FiO

2): d

ay 1

: 224

, day

2: 2

20, d

ay 3

: 204

, day

7: 1

74; P

atie

nt 3

(PaO

2/Fi

O2)

: day

1: 1

40, d

ay 2

: 203

, day

3:

78,

day

7: 4

4; P

atie

nt 4

(PaO

2/Fi

O2)

: day

1: 7

5, d

ay 2

: 234

, day

3: 1

62, d

ay 7

: 69

mR

S w

as d

efine

d as

: 0: N

o sy

mpt

oms

at a

ll; 1

:No

sign

ifica

nt d

isab

ility

des

pite

sym

ptom

s; a

ble

to c

arry

out

all

usua

l dut

ies

and

activ

ities

; 2:S

light

dis

abili

ty; u

nabl

e to

car

ry o

ut a

ll pr

evio

us

activ

ities

, but

abl

e to

look

afte

r ow

n aff

airs

with

out a

ssist

ance

; 3:M

oder

ate

disa

bilit

y; re

quiri

ng s

ome

help

, but

abl

e to

wal

k w

ithou

t ass

istan

ce; 4

:Mod

erat

ely

seve

re d

isab

ility

; una

ble

to w

alk

with

out a

ssist

ance

and

una

ble

to a

ttend

to o

wn

bodi

ly n

eeds

with

out a

ssist

ance

; 5:S

ever

e di

sabi

lity;

bed

ridde

n, in

cont

inen

t and

requ

iring

con

stan

t nur

sing

car

e an

d at

tent

ion

3127Journal of Neurology (2020) 267:3121–3127

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critical illness-related encephalopathy and might rather result from COVID19-related brainstem dysfunction in our patients.

Our study suggests a wider spectrum than previously reported of neurological manifestations associated with COVID-19 and further suggests that patients with severe forms of COVID-19 should be systematically screened for neurological complications.

Acknowledgments The authors thank Yves Chaudière for his language expertise.

Author contributions HC: acquisition, analysis, and interpretation of data and drafting the manuscript; AS-G: acquisition of data and drafting the manuscript; FM: acquisition of data; CC: acquisition of data; GJ: revising the manuscript, analysis, and interpretation of data; MC: acquisition, analysis and interpretation of data and revising the manuscript; ER: drafting and revising the manuscript, analysis, and interpretation of data; AL: acquisition, analysis and interpretation of data, drafting and revising the manuscript.

Funding No funding.

Compliance with ethical standards

Availability of data and material Not applicable.

Code availability Not applicable.

Consent for publication Patient’s consent has been obtained.

Conflicts of interest Dr. Chaumont reports having received travel grant from PEPS development, Roche and Pfizer. Dr. Roze reports served on scientific advisory boards for Orkyn, Aguettant, Merz-Pharma; re-ceived honoraria for speeches from Orkyn, Aguettant, Merz-Pharma, Medday-Pharma, Everpharma, International Parkinson and Move-ment disorders Society; received research support from Merz-Pharma, Orkyn, Aguettant, Elivie, Ipsen, Everpharma, Fondation Desmarest, AMADYS, Fonds de Dotation Brou de Laurière, Agence Nationale de la Recherche; received travel grant from Vitalair, PEPS development, Aguettant, Merz-Pharma, Ipsen, Merck, Orkyn, Elivie, Adelia Medi-cal, Dystonia Medical Research Foundation, International Parkinson and Movement disorders Society, European Academy of Neurology, International Association of Parkinsonism and Related Disorders. Dr. Couratier reports having received travel grant from Allergan, Novartis,

Esai, UCB, Medtronic, Merck Serono, Biogen, LFB, Teva, Icomed, GSK, Genzyme, Aguettant, Cyberonics and Merz-Pharma. Dr. Lan-nuzel reports having received research support from France Parkinson, PSP France, Agence Nationale de la Recherche, Fonds Européen de DEveloppement Regional, French Ministry of Health, University Hos-pital of Guadeloupe, received honoraria for a speech from Associa-tion des Neurologues du Québec; received travel grant from Vitalair, PEPS development, Merz-Pharma, International Parkinson and Move-ment disorders Society. Dr. San-Galli, Dr. Martino, Dr. Carles, and Dr. Joguet report no disclosures.

Ethics approval Not applicable.

Informed consent Not applicable.

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