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 [email protected]
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
1 3
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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