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BRIEF
COMMUNICATION
S aphylococcus
lugdunensis
Skin
In ec ion:
Repo
o
16
Cases夽
A.J.
Ga cía-Malinis,a,∗A.
Milag o,bL.
To es
Sopena,cY.
Gilabe ed
aUnidad
de
De ma ología,
Hospi al
San
Jo ge,
Huesca,
Spain
bSe icio
de
Mic obiología,
Hospi al
Uni e si a io
Miguel
Se e ,
Za agoza,
Spain
cSe icio
de
Mic obiología,
Hospi al
San
Jo ge,
Huesca,
Spain
dSe icio
de
De ma ología,
Hospi al
Uni e si a io
Miguel
Se e ,
Za agoza,
Spain
KEYWORDS
S aphylococcus
lugdunensis;
Coagulase-nega i e
s aphylococci;
Skin
in ec ion
Abs ac
In oduc ion
and
objec i e:
S aphylococcus
lugdunensis
belongs
o
he
g oup
o
coagulase-
nega i e
s aphylococci.
The
aim
o
his
epo
was
o
e iew
he
clinical
and
mic obiologic
ea u es
o
cases
o
S.
lugdunensis
skin
in ec ions.
Ma e ial
and
me hods:
Obse a ional
s udy
o
all
cases
o
skin
in ec ions
in
which
S.
lugdunen-
sis
was
isola ed
by
he
mic obiology
depa men
o
Hospi al
Gene al
San
Jo ge
in
Huesca,
Spain,
be ween
2009
and
2016.
Resul s:
We
s udied
he
cases
o
16
pa ien s.
The
mos
equen
si e
o
in ec ion
was
he
inguinal-pe ineal
egion
(n
=
6,
37.5%),
and
pus ules
we e
he
mos
common
p esen a ion
(n
=
5,
31.3%).
Response
o
ea men
was
good
in
87.6%
o
he
pa ien s
(n
=
14).
Howe e ,
in ec ion
ecu ed
in
3
pa ien s,
2
o
whom
we e
on
an i-TNF
he apy.
Conclusions:
S.
lugdunensis
should
be
conside ed
a
possible
cause
o
in ec ion
when
i
is
isola ed
in
bo h
skin
and
subcu aneous
issues,
especially
in
pa ien s
on
biologic
he apies.
©
2020
AEDV.
Published
by
Else ie
Espa˜
na,
S.L.U.
This
is
an
open
access
a icle
unde
he
CC
BY-NC-ND
license
(h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/).
PALABRAS
CLAVE
S aphylococcus
lugdunensis;
Es afilococo
coagulasa
nega i e;
In ección
cu ánea
In ección
cu ánea
po
S aphylococcus
lugdunensis:
p esen ación
de
16
casos
Resumen
In oducción
y
obje i o:
S aphylococcus
lugdunensis
pe enece
al
g upo
de
los
es afilococos
coagulasa
nega i os.
El
obje i o
del
es udio
es
e isa
las
ca ac e ís icas
clínicas
y
mic obiológ-
icas
de
los
pacien es
diagnos icados
de
una
in ección
cu ánea
po
S.
lugdunensis.
Ma e ial
y
mé odos:
Es udio
obse acional
e ospec i o
de
odos
los
casos
de
in ecciones
cu áneas
en
las
que
se
aisló
S.
lugdunensis
diagnos icados
en e
2009
y
2016
en
el
Se icio
de
Mic obiología
del
Hospi al
San
Jo ge
de
Huesca.
夽Please
ci e
his
a icle
as:
Ga cía-Malinis
AJ,
Milag o
A,
To es
Sopena
L,
Gilabe e
Y.
In ección
cu ánea
po
S aphylococcus
lugdunensis:
p esen ación
de
16
casos.
Ac as
De mosifiliog .
2020.
h ps://doi.o g/10.1016/j.ad.2019.05.017
∗Co esponding
au ho .
E-mail
add ess:
[email p o ec ed]
(A.J.
Ga cía-Malinis).
1578-2190/©
2020
AEDV.
Published
by
Else ie
Espa˜
na,
S.L.U.
This
is
an
open
access
a icle
unde
he
CC
BY-NC-ND
license
(h p://
c ea i ecommons.o g/licenses/by-nc-nd/4.0/).
ADENGL-2497;
No.
o
Pages
5
ARTICLE IN PRESS
+Model
A.J.
Ga cía-Malinis,
A.
Milag o,
L.
To es
Sopena
e
al.
Resul ados:
Se
incluye on
16
pacien es.
La
localización
más
ecuen e
ue
la
zona
inguinope -
ineal
(n
=
6,
37,5%)
y
la
o ma
de
p esen ación
más
habi ual
ue on
las
pús ulas
(n
=
5,
31,3%).
El
87,6%
de
los
pacien es
(n
=
14)
mos a on
buena
espues a
al
a amien o;
sin
emba go,
3
pacien es
ecu ie on.
De
ellos,
2
es aban
en
a amien o
con
un
an i-TNF.
Conclusión:
S.
lugdunensis
debe ía
conside a se
el
posible
agen e
causal
de
la
in ección
cuando
se
aísla
an o
en
piel
como
en
ejido
celula
subcu áneo,
especialmen e
en
pacien es
que
es án
ecibiendo
a amien o
biológico.
©
2020
AEDV.
Publicado
po
Else ie
Espa˜
na,
S.L.U.
Es e
es
un
a ´
ıculo
Open
Access
bajo
la
licencia
CC
BY-NC-ND
(h p://c ea i ecommons.o g/licenses/by-nc-nd/4.0/).
In oduc ion
S aphylococcus
lugdunensis
belongs
o
he
g oup
o
coagulase-nega i e
s aphylococci
(CoNS).
Fi s
desc ibed
in
1988
by
F eney
in
Lyon,
F ance,1 his
eme ging
pa hogen
is
mo e
i ulen
han
o he
CoNS
and
can
cause
in ec ions
wi h
high
mo ali y.2
S
lugdunensis
is
a
commensal
CoNS
in
a eas
wi h
apoc ine
glands,3and
causes
in ec ions
o
he
skin
and
subcu a-
neous
cell
issue,
gene ally
esul ing
in
abscess
o ma ion.4
Pa ien s
wi h
p edisposing
condi ions
such
as
diabe es
o
umo s
a e
a
g ea e
isk
o
acqui ing
S
lugdunensis
in ec-
ion,
al hough
deep
and
supe ficial
in ec ions
ha e
also
been
desc ibed
in
heal hy
indi iduals,5in
which
he
skin
is
he
main
poin
o
en y.
In
his
s udy
we
sough
o
e iew
he
clinical
and
mic o-
biological
cha ac e is ics
o
pa ien s
in
ou
cen e
who
we e
diagnosed
wi h
skin
in ec ions
om
which
S
lugdunensis
was
isola ed,
as
well
as
he
ea men s
applied
and
he
cou se
o
he
in ec ion.
Ma e ial
and
Me hods
We
pe o med
a
e ospec i e
obse a ional
s udy
o
all
cases
o
skin
in ec ions
o
which
mic obiological
cul u e
e ealed
he
p esence
o
S
lugdunensis
a
he
Mic obiology
Se ice
o
Hospi al
San
Jo ge
de
Huesca
be ween
2009
and
2016.
The
ollowing
a iables
we e
eco ded:
age;
sex;
asso-
cia ed
sys emic
diseases
and
hei
ea men ;
loca ion
and
ype
o
skin
lesion;
ea men
and
e olu ion;
and
o he
mic oo ganisms
concomi an ly
isola ed
om
he
same
lesion.
Mic obiological
diagnosis
was
based
on
cul u e
o
he
samples
in
s anda d
media.
Mic oo ganism
iden ifica ion
and
an ibio ic
sensi i i y
es s
we e
pe o med
using
Mic oScan®
(Beckman
Coul e ),
applying
he
c i e ia
o
he
Clinical
and
Labo a o y
S anda ds
Ins i u e
(CLSI).
Iden ifica ion
was
confi med
using
he
o ni hine
deca boxylase
(ODC)
es
and
he
py olidonyl-a ylamidase
(PYR)
es
(Rosco
Diagnos ica
A/S,
Denma k).
Resul s
Table
1
summa izes
he
cha ac e is ics
o
he
sample
pop-
ula ion,
which
consis ed
o
16
pa ien s
(9
women,
7
men)
wi h
a
mean
age
o
52.19
yea s
( ange,
19---83
y).
Six
pa ien s
(37.5%)
had
unde lying
sys emic
diseases.
The
mos
commonly
a ec ed
loca ion
was
he
inguinal/pe ineal
a ea
(n
=
6,
37.5%),
ollowed
by
he
lowe
ex emi ies
(n
=
3,
18.8%).
The
mos
common
clinical
p esen a ions
we e
pus ules
(n
=
5,
31.3%),
in e igo- ype
lesions
(n
=
5,
31.3%),
and
abscessed
cys s
(n
=
3,
18.8%)
(Fig.
1A).
The
p esence
o
an
abscess
was
epo ed
in
only
1
pa ien .
S
lugdunensis
was
he
only
pa hogen
isola ed
in
cul u es
om
11
(68.8%)
o
he
16
pa ien s.
The
mic oo ganism
mos
equen ly
isola ed
concomi an ly
wi h
S
lugdunensis
was
Esche ichia
coli
(n
=
2,
12.5%).
A
cu ious
ea u e
o
he
S
lug-
dunensis
samples
isola ed
on
blood
aga
was
a
cha ac e is ic
smell
o
cu ed
po k.
An
an ibiog am
pe o med
o
all
samples
e ealed
an ibio ic
sensi i i y
o
all
S
lugdunensis
isola es,
excep
o
one
ha
showed
esis ance
o
clindamycin,
e y h omycin,
os omycin,
and
e acycline.
Fungal
cul u e
was
pe o med
in
6
pa ien s,
5
o
whom
had
suspec ed
in e igo.
O al
ea men ,
he
mos
common
o
which
was
o al
penicillin,
was
ecei ed
by
75%
o
pa ien s
(n
=
12).
Top-
ical
ea men
was
ecei ed
by
56.3%
(n
=
9)
o
pa ien s,
o
whom
5
ecei ed
associa ed
o al
an ibio ic
ea men .
Mupi ocin
(n
=
3,
18.8%)
and
e y h omycin
(n
=
2,
12.5%)
we e
he
mos
equen ly
p esc ibed
opical
an ibio ics
among
pa ien s
who
ecei ed
opical
ea men .
O
he
5
pa ien s
wi h
in e igo-like
lesions,
only
one
p esen ed
coin ec ion
(wi h
Candida
albicans
and
T ichophy on
ub um),
which
esponded
adequa ely
o
o al
e binafine.
In
cases
in ol ing
abscesses
o
abscessed
cys s,
he
lesions
we e
d ained.
A
good
ea men
esponse
was
obse ed
in
87.6%
o
pa ien s
(n
=
14).
Two
pa ien s,
bo h
o
whom
had
E
coli
coin-
ec ions,
did
no
espond
o
ea men .
Th ee
pa ien s
who
showed
a
good
ini ial
esponse
expe ienced
ecu ence
(2
episodes
each).
O
hese
3
pa ien s,
2
we e
being
ea ed
wi h
an i- umo
nec osis
ac o
(TNF)
agen s.
Discussion
Despi e
o ming
pa
o
he
skin
mic obio a,
S
lugdunensis
is
o
g ea
pa hogenic
impo ance
and,
like
S aphylococcus
au eus,
can
cause
in asi e,
highly
i ulen
communi y
and
nosocomial
in ec ions.6
In
ou
se ies,
skin
in ec ions
caused
by
S
lugdunen-
sis
we e
mos ly
mild
and
p edominan ly
a ec ed
he
inguinal/pe ineal
a ea.
The
mos
equen
clinical
p esen-
2
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Table
1
Clinical
Cha ac e is ics,
Coin ec ion
S a us,
T ea men ,
and
In ec ion
Cou se
Case
Age,
y
Sex
Lesion
Loca ion
Lesion
Type
Associa ed
Diseases
Biological
T ea men
Concomi an
In ec ions
O al
T ea men
Topical
T ea men
T ea men
Response
1
83
Female
Lowe
limbs
Pus ules
Diges i e
mas ocy o-
sis
No
Co ynebac e ium
s ia-
um/amycola um
Cloxacillin
No
Good
esponse
2
45
Male
Abdomen
Su gical
wound
No
No
No
Amoxicillin
Mupi ocin
Good
esponse
3
38
Female
Lowe
limbs
In e igo
No
No
Candida
albicans
and
T ichophy on
ub um
Te binafine
No
Good
esponse
4
79
Male
Inguinal/pe ineal
and
glu eal
egions
P essu e
ulce
No
No
E
coli
Amoxicillin
Mupi ocin
No
esponse
5
68
Female
Inguinal/pe ineal
and
glu eal
egions
Abscess
Pso iasis
Yes
No
Doxycycline
Fusidic
acid
and
be ame hasone
Good
ini ial
esponse,
subsequen
ecu ence
6
40
Female
Lumba
egion
Abscessed
cys
No
No
No
Cloxacillin
No
Good
esponse
7
45
Female
Inguinal/pe ineal
and
glu eal
egions
Pus ules
Hid adeni is
No
No
Clindamycin
No
Good
ini ial
esponse,
subsequen
ecu ence
8
19
Male
Inguinal/pe ineal
and
glu eal
egions
Pus ules
Hid adeni is
No
No
Clindamycin
and
i ampicin
No
Good
esponse
9
40
Female
Abdomen
Pus ules
Rheuma oid
a h i is
Yes
No
Amoxicillin-
cla ulanic
acid
No
Good
ini ial
esponse,
subsequen
ecu ence
10
53
Male
Lumba
egion
Abscessed
cys
No
No
No
Cloxacillin
No
Good
esponse
11
41
Male
Inguinal/pe ineal
and
glu eal
egions
In e igo
Hepa i is
A
i us
No
S ep ococcus
agalac iae
(g oup
B)
No
E y h omycin
Good
esponse
12
61
Male
Lowe
limbs
Pus ules
No
No
No
Cloxacillin
Mupi ocin
Good
esponse
13
67
Female
Inguinal/pe ineal
and
glu eal
egions
In e igo
No
No
No
No
E y h omycin
Good
esponse
14
65
Female
Submamma y
egion
In e igo
No
No
No
No
Fusidic
acid
Good
esponse
15
35
Female
Ches
Abscessed
cys
No
No
No
Amoxicillin-
cla ulanic
acid
Fusidic
acid
and
be ame hasone
Good
esponse
16
56
Male
Axillae
In e igo
No
No
E
coli
No
Hyd oco isone
and
miconazole
No
esponse
3
ARTICLE IN PRESS
+Model
A.J.
Ga cía-Malinis,
A.
Milag o,
L.
To es
Sopena
e
al.
Figu e
1
A,
Abscess
caused
by
S
lugdunensis
in
he
inguinal
egion
o
a
pa ien
ecei ing
adalimumab
ea men .
B,
S
lugdunensis
colony
g owing
on
blood
aga .
a ions
we e
in e igo-like
and
pus ula
lesions.
Recu ence
was
obse ed
only
in
pa ien s
ea ed
wi h
an i-TNF
agen s.
The
majo i y
o
S
lugdunensis
in ec ions
epo ed
in
he
li e a u e
p esen
as
in ec ions
o
he
skin
o
subcu aneous
issue
ha
esul
in
abscess
o ma ion.7,8 Among
29
cases
ecen ly
desc ibed
by
Zaa ou a
e
al,9 he
mos
equen
p esen a ion
was
pus ulosis/ olliculi is
(16
pa ien s).
In
line
wi h
hose
findings,
pus ules
and
in e igo
we e
he
mos
common
p esen a ions
(5
cases
o
each)
in
ou
se ies.
The
mos
equen ly
a ec ed
loca ions
in
ou
s udy
popula ion
coincided
wi h
hose
epo ed
in
p e ious
s ud-
ies.
These
include
he
inguinal/pe ineal
a ea,7,10 abdomen,
lowe
ex emi ies,11 and
mamma y
egion,5all
o
which
a e
a eas
in
which
S
lugdunensis
is
a
commensal
mic oo ganism.
Skin
in ec ions
due
o
S
lugdunensis
usually
espond
o
an ibio ic
ea men .11 Unlike
o he
CoNS,
S
lugdunensis
is
gene ally
sensi i e
o
penicillins
owing
o
i s
low
le els
o
be a-lac amase
p oduc ion,
and
less
han
5%
o
isola es
a e
esis an
o
oxacillin.5In
cases
o
simple
skin
abscesses,
he apeu ic
guidelines
ecommend
incision
and
d ainage
o
he
lesion;
fi s -line
an ibio ic
ea men
is
no
indica ed.
In
complica ed
cases,
d ainage
and
o al
ea men
wi h
na ow-spec um
an ibio ics
such
as
ce ad oxil,
cephalexin,
o
cloxacillin
is
ecommended.
In
cases
o
olliculi is,
he
d ugs
o
choice
a e
mupi ocin
and
usidic
acid,
combined
wi h
hygiene
measu es.
In
pa ien s
wi h
ex ensi e
olliculi-
is,
addi ion
o
an
o al
an ibio ic
(ce ad oxil,
cephalexin,
o
cloxacillin)
is
ecommended.12 The
mos
common
ea -
men
epo ed
in
he
li e a u e
is
opical
an ibio ic
he apy,
combined
wi h
o al
an ibio ics
in
mo e
complica ed
cases.13
Because
S
lugdunensis
colonizes
he
skin,
i
is
impo -
an
o
de e mine
when
his
mic oo ganism
becomes
a
pa hogen.
One
o
he
cases
in
ou
se ies
was
a
pa ien
wi h
T
ub um
and
C
albicans
coin ec ion
who
esponded
a o -
ably
o
e binafine.
This
is
a
clea
example
o
S
lugdunensis
me ely
ac ing
as
a
colonizing
agen .
Co-in ec ion
wi h
E
coli
was
de ec ed
in
he
2
pa ien s
in
which
no
ea men
esponse
was
obse ed,
sugges ing
ha
E
coli,
and
no
S
lug-
dunensis,
was
he
pa hogen
esponsible
o
he
in ec ion.
The
pa hogenic
capaci y
o
S
lugdunensis
in
os eoa icula
in ec ions
has
been
co obo a ed
p ospec i ely.14 Howe e ,
cau ion
is
ad ised
when
in e p e ing
single
posi i e
samples
om
skin
o
subcu aneous
issue
o
om
known
niches
o
his
CoNS.15
S
lugdunensis
in ec ion
ha
esponded
well
o
an ibio ic
ea men
has
been
desc ibed
in
a
pa ien
wi h
pso iasis
and
pso ia ic
a h i is
who
was
being
ea ed
wi h
adali-
mumab
and
me ho exa e.16 In
ou
se ies,
2
o
he
pa ien s
who
expe ienced
lesion
ecu ence
we e
being
ea ed
wi h
an
an i-TNF
agen ,
specifically
adalimumab.
One
o
he
pa ien s
swi ched
o
adalimumab
a e
showing
a
poo
esponse
o
an ibio ic
ea men .
Skin
in ec ion
is
one
o
he
mos
equen ly
epo ed
side
e ec s
o
an i-TNF
d ugs.17
This
is
because
TNF-␣
is
a
p o-inflamma o y
cy osine
ha
plays
an
impo an
ole
in
inna e
immuni y,
and
he e o e
i s
inhibi ion
can
inc ease
he
isk
o
in ec ions,
especially
hose
o
bac e ial
o igin.18
S
lugdunensis
can
be
easily
iden ified
in
he
labo a o y,
p o ided
ha
i s
possible
p esence
is
aken
in o
conside a-
ion.
Incuba ion
on
blood
aga
o
18
o
24
hou s
gi es
ise
o
colonies
wi h
weak
␤-hemolysis,
which
inc eases
a e
48
hou s
(Fig.
1B).
Two
es s
a e
equi ed
o
iden i y
his
bac e ium:
he
ODC
and
PYR
es s.
Bo h
a e
posi i e
in
he
case
o
S
lugdunensis,
unlike
o he
CoNS.
Ma ix-assis ed
lase
deso p ion
ioniza ion--- ime
o
fligh
mass
spec ome y
(MALDI-TOF
MS)
p o ides
a
apid
and
cos -e ec i e
means
o
iden i ying
S
lugdunensis.19 I
has
a
sensi i i y
and
specifici y
close
o
100%
o
he
iden ifica ion
o
CoNS,
especially
S
lugdunensis.20 The
p esen
se ies
was
pe o med
be o e
he
ecen
acquisi ion
o
a
MALDI-TOF
sys em
by
ou
hospi al.
The
des uc i e
na u e
o
S
lugdunensis,
i s
g ea
i u-
lence,
and
i s
abili y
o
cause
suppu a i e
in ec ions
mo e
han
jus i y
ac i e
su eillance
o
his
mic oo ganism.
In
he
pas
S
lugdunensis
was
occasionally
iden ified
as
a
causal
agen
o
human
pa hology,
bu
is
now
de ec ed
wi h
inc eas-
ing
equency.
This
may
be
due
o
be e
unde s anding
o
i s
mic obiological
cha ac e is ics,
a
highe
index
o
clini-
cal
suspicion,
and
he
use
o
MALDI-TOF,
which
has
enabled
cha ac e iza ion
o
nume ous
CoNS
species
ha
we e
p e i-
ously
iden ified
simply
as
coagulase-nega i e
s aphylococci
o
S aphylococcus
species.5
S
lugdunensis
can
be
conside ed
a
pa hogenic
mic oo -
ganism
o
skin
in
ce ain
ci cums ances,
depending
on
he
clinical
pic u e
and
a ec ed
loca ion,
and
in
pa ien s
wi h
sys emic
o
local
isk
ac o s,
such
as
hose
in
ou
se ies
who
we e
ea ed
wi h
an i-TNF
agen s.
Funding
This
s udy
did
no
ecei e
specific
unding
om
any
public
sec o ,
p i a e
sec o ,
o
nonp ofi
en i ies.
4
ARTICLE IN PRESS
+Model
ACTAS
De mo-Sifiliog áficas
xxx
(xxxx)
xxx---xxx
Conflic s
o
In e es
The
au ho s
decla e
ha
hey
ha e
no
conflic s
o
in e es .
Re e ences
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J,
B un
Y,
Bes
M,
Meugnie
H,
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F,
G imon
PAD,
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sp.
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and
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sp.
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J-J.
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Skin
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so
issue
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lugdunensis:
epo
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o
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o
ma ix-assis ed
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des-
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ioniza ion- ime
o
fligh
mass
spec ome y
in
ou ine
clinical
labo a o ies
imp o es
iden ifica ion
o
coagulase-
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5