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ABSTRACT
In oduc ion: Celluli is and e ysipelas ep esen he mos equen cause o hospi aliza ion in he de ma ology depa men o San a
Ma ia Hospi al in Lisbon, Po ugal. The aim o his s udy was o in es iga e whe he pa ien demog aphics, como bidi ies, p e ious
episodes o celluli is/e ysipelas, he p esence o complica ions, labo a o y ma ke s a admission, mic obial isola ion o p e ious use o
an ibio ics, a e associa ed wi h p olonged s ays.
Ma e ial and Me hods: Re ospec i e analysis, including pa ien s admi ed wi h celluli is/e ysipelas in he inpa ien de ma ology de-
pa men o San a Ma ia Hospi al be ween July 1s 2012 and June 30 h 2017.
Resul s: The e we e 372 admissions, co esponding o 348 pa ien s. The median leng h o s ay was 11 days. Inc eased age
(p = 0.002, OR 1.03, 95% CI 1.01 – 1.04), p e ious episode o celluli is/e ysipelas equi ing hospi aliza ion (p = 0.005, OR 4.81,
95% CI 1.63 – 14.23), he p esence o celluli is/e ysipelas-associa ed complica ions (p = 0.001, OR 3.28, 95% CI 1.63 – 6.59), leukocy-
osis (p = 0.049, OR 1.81, 95% CI 1.00 – 3.30), high le els o C- eac i e p o ein (p = 0.035, OR 1.03, 95% CI 1.00 – 1.06) and a posi i e
cul u e esul (p = 0.002, OR 2.59, 95% CI 1.41 – 4.79) we e associa ed wi h p olonged hospi aliza ion.
Discussion: P olonged hospi aliza ion o celluli is/e ysipelas is associa ed wi h highe cos s, addi ional clinical in es iga ion, in asi e
ea men s, p olonged cou ses o an ibio ic he apy, isk o nosocomial in ec ions, and delayed e u n o ac i i ies o daily li ing. Thus,
he in es iga ion o clinical-labo a o y ac o s associa ed wi h p olonged hospi aliza ion o celluli is / e ysipelas is essen ial and may be
use ul o he cons uc ion o a se e i y sco e.
Conclusion: The knowledge o he cha ac e is ics ha a e associa ed wi h p olonged s ay among pa ien s wi h celluli is/e ysipelas may
be ele an o imp o e heal h ca e, by educing he leng h o hospi al s ay and associa ed isks and cos s.
Keywo ds: C-Reac i e P o ein; Celluli is; E ysipelas; Hospi aliza ion; Leukocy osis
Clinical and Labo a o y Fac o s Associa ed wi h P olonged
Hospi al S ay among Pa ien s wi h Celluli is/E ysipelas
Fa o es Clínico-Labo a o iais Associados ao In e namen o
P olongado em Doen es com Celuli e/E isipela
Ângela RODA1, Ana Ma cos PINTO1, Ana Ri a FILIPE2, Ana Ri a TRAVASSOS1, João Ped o FREITAS1,
Paulo FILIPE1,3,4
Ac a Med Po 2019 Jun;32(6):448–452 ▪ h ps://doi.o g/10.20344/amp.10735
1. Se iço de De ma ologia. Hospi al de San a Ma ia. Cen o Hospi ala Uni e si á io Lisboa No e. Lisboa. Po ugal.
2. Unidade de Saúde Pública de Oei as. Ag upamen o de Cen os de Saúde de Lisboa Ociden al e Oei as. Oei as. Po ugal.
3. Clínica Uni e si á ia de De ma ologia. Faculdade de Medicina. Uni e sidade de Lisboa. Lisboa. Po ugal.
4. Ins i u o de Medicina Molecula . Faculdade de Medicina. Uni e sidade de Lisboa. Lisboa. Po ugal.
 Au o co esponden e: Ângela Roda. [email p o ec ed]
Recebido: 28 de ab il de 2018 – Acei e: 02 de ou ub o de 2018 | Copy igh © O dem dos Médicos 2019
RESUMO
In odução: A celuli e e a e isipela cons i uem a causa mais equen e de in e namen o no Se iço de De ma ologia do Hospi al San a
Ma ia. Es e es udo e e como obje i o in es iga se as ca ac e ís icas demog á icas, as como bilidades, a exis ência de episódios
p é ios de celuli e/e isipela, a p esença de complicações associadas, os pa âme os labo a o iais na admissão, o isolamen o de
mic o ganismo em cul u a ou o uso p é io de an ibió icos es ão associados a in e namen os p olongados.
Ma e ial e Mé odos: Es udo e ospe i o, incluindo os doen es in e nados no Se iço de De ma ologia do Hospi al San a Ma ia com
o diagnós ico de celuli e/e isipela, en e 1 de julho de 2012 e 30 de junho de 2017.
Resul ados: Exis i am 372 in e namen os, co espondendo a 348 doen es. A mediana do empo de in e namen o oi de 11 dias.
A idade (p = 0,002, OR 1,03, 95% IC 1,01 – 1,04), a exis ência de in e namen o p é io po celuli e/e isipela (p = 0,005, OR 4,81,
95% IC 1,63 – 14,23), a p esença de complicações associadas à celuli e/e isipela (p = 0,001, OR 3,28, 95% IC 1,63 – 6,59), a leuco-
ci ose (p = 0,049, OR 1,81, 95% IC 1,00 – 3,30), alo es ele ados de p o eína C ea i a (p = 0,035, OR 1,03, 95% IC 1,00 - 1,06) e o
isolamen o de mic o ganismo em cul u a (p = 0,002, OR 2,59, 95% IC 1,41 – 4,79) es i e am associados a in e namen os p olongados.
Discussão: A pa dos maio es cus os associados, o in e namen o p olongado po celuli e/e isipela es á equen emen e associado à
necessidade de in es igação clínica adicional, a a amen os in asi os, a cu sos p olongados de an ibio e apia, ao isco de in eções
nosocomiais e ao a aso no e o no às a i idades da ida diá ia. Assim, o es udo dos a o es clínico-labo a o iais associados ao in e -
namen o p olongado po celuli e/e isipela é undamen al e pode á se ú il pa a a cons ução de um sco e de g a idade.
Conclusão: O conhecimen o de ca ac e ís icas clínicas e labo a o iais associadas ao in e namen o p olongado pode á se ele an e
pa a melho a os cuidados de saúde, a a és da edução dos empos de in e namen o e dos seus iscos e cus os associados.
Pala as-cha e: Celuli e; E isipela; Hospi alização; Leucoci ose; P o eína C-Reac i a
INTRODUCTION
A Celluli is and e ysipelas a e he leading causes o
admission o he Depa men o De ma ology o he Hos-
pi al San a Ma ia, co esponding o a ound 18% o annual
admissions.
E en hough celluli is can be di e en ia ed om e ysip-
elas, his is mainly based on unclea clinical c i e ia and is
i ele an ega ding he app oach o ea men and man-
agemen . The e o e, bo h e ms a e in e changeably used
in clinical p ac ice.1
Up o da e, li le is known on he ac o s wi h an in luence
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Roda A, e al. Fac o s associa ed wi h p olonged hospi al s ay among pa ien s wi h celluli is/e ysipelas, Ac a Med Po 2019 Jun;32(6):448–452
on hospi al leng h o s ay (LOS) o pa ien s wi h celluli is/e -
ysipelas. This s udy was aimed a de ining he associa ion
be ween p olonged LOS and pa ien ’s demog aphic cha ac-
e is ics, como bidi ies, he p esence o p e ious episodes
o celluli is/e ysipelas o p e ious complica ions associa ed
wi h bo h condi ions, labo a o y pa ame e s on admission,
posi i e cul u es o p e ious an ibio ic ea men .
MATERIAL AND METHOD
This was a e ospec i e s udy in ol ing pa ien s aged
18 o olde admi ed o he Depa men o De ma ology o
he Hospi al de San a Ma ia be ween 1 Jul 2012 and 30 Jun
2017 and diagnosed wi h celluli is / e ysipelas, ega dless
o he loca ion o he a ec ed a ea.
The ollowing explana o y a iables we e assessed: de-
mog aphic cha ac e is ics, including pa ien ’s age and gen-
de , he p esence o como bidi ies, namely diabe es melli-
us, pe iphe al ascula disease (a ec ing eins, a e ies
and lympha ic essels), immune impai men (associa ed
wi h in ec ious, haema ological and pha macological dis-
ease); his o y o celluli is/e ysipelas, namely he p esence
o a leas one p e ious episode o celluli is/e ysipelas, a
leas one p e ious admission due o celluli is/e ysipelas
and compliance wi h an ibio ic p ophylaxis; he p esence
o complica ions associa ed wi h celluli is/e ysipelas (in-
cluding abscess, lymphangi is, nec osis, skin ulce s, blis-
e s, os eoa icula in ol emen ); he p esence o a po al
o en y [all he condi ions in ol ing skin ba ie dis up ion,
including ungal in ec ions o he skin, hai and nails, i al
(he pe ic in ec ions), bac e ial ( olliculi is, boils), auma ic
wounds, su gical wounds, insec bi es and s ings]; labo-
a o y pa ame e s on admission, namely whi e blood cell
coun , neu ophil coun , C- eac i e p o ein (CRP) le el;
posi i e cul u e (ulce o abscess exuda e and/o blood cul-
u e); an ibio ic ea men o he cu en episode o celluli is/
e ysipelas on he week p e ious o admission.
The selec ion o a iables was based on he pa hophys-
iology o he disease and i s hypo he ical ela ionship wi h
he leng h o s ay in hospi al.
S a is ical analysis
Ca ego ical a iables we e p esen ed in he desc ip i e
analysis as equencies and a es and con inuous a iables
as means and s anda d de ia ions, o medians and in e -
qua ile ange, depending on he ype o da a (no mally o
non-no mal dis ibu ed, espec i ely). The Shapi o-Wilk es
o no mali y was used and cu -o based [-1; 1] skewness
and ku osis alues we e analysed.
Hospi al admissions we e di ided in o wo di e en
g oups, depending on he leng h o s ay (g ea e han 14
days o 14 days and less); his dicho omisa ion was based
on he median LOS o ou g oup o pa ien s and was sub-
sequen ly de ined. A leng h o hospi al s ay g ea e han 14
days was conside ed as a p olonged LOS.
Chi-squa e o Fishe ’s exac es we e used in bi a i-
a e analysis in o de o check o an associa ion be ween
ca ego ical a iables and S uden ’s - es was used o he
assessmen o con inuous a iables.
Finally, an imp o ed logis ic eg ession model was de-
eloped, wi h a s epwise da a en y me hod, including s a-
is ically signi ican a iables in bi a ia e analysis, aimed a
de ining which a iables we e associa ed wi h p olonged
LOS.
Only wo- ailed p- alues we e epo ed, wi h a 0.05 sig-
ni icance le el (α). Da a analysis was made by use o he
SPSS, e sion 23 so wa e.
Table 1 – Uni a ia e analysis o he cha ac e is ics o pa ien s admi ed wi h celluli is/e ysipelas
Gene al
(n = 372)
Sho s ay
(n = 247)
P olonged s ay
(n = 125) p- alue
Age – mean (SD) (yea s) 61.2 (18.4) 59.5 (18.7) 64.5 (17.4) 0.01
Female gende – n (%) 191 (51%) 122 (49%) 69 (55%) 0.29
Diabe es melli us – n (%) 86 (23%) 50 (20%) 36 (29%) 0.06
Pe iphe al ascula disease – n (%) 96 (26%) 55 (22%) 41 (33%) 0.03
Immune impai men – n (%) 47 (13%) 29 (12%) 18 (14%) 0.47
P e ious local su ge y – n (%) 83 (22%) 51 (21%) 32 (26%) 0.28
P e ious episode(s) o celluli is/e ysipelas – n (%) 79 (21%) 50 (20%) 29 (23%) 0.51
P e ious hospi al admission due o celluli is/e ysipelas – n (%) 24 (6%) 8 (3%) 16 (13%) < 0.001
An ibio ic p ophylaxis 15 (4%) 9 (4%) 6 (5%) 0.59
Complica ions – n (%) 66 (18%) 32 (13%) 34 (27%) 0.001
De ined po al o en y – n (%) 193 (52%) 129 (52%) 64 (51%) 0.85
Leukocy osis – n (%) 188 (51%) 109 (44%) 79 (63%) 0.001
Neu ophilia – n (%) 221 (59%) 135 (55%) 86 (69%) 0.009
CRP – mean (SD) (mg/dL) 12.4 (9.9) 11.2 (8.9) 14.8 (11.5) 0.002
Posi i e cul u e* – n (%) 82 (22%) 37 (15%) 45 (36%) < 0.001
An ibio ic ea men on he week p e ious o admission – n (%) 111 (30%) 67 (27%) 44 (35%) 0.11
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Roda A, e al. Fac o s associa ed wi h p olonged hospi al s ay among pa ien s wi h celluli is/e ysipelas, Ac a Med Po 2019 Jun;32(6):448–452
RESULTS
A o al o 372 hospi al admissions we e eco ded du ing
he s udy pe iod, co esponding o 348 pa ien s, wi h an 11-
day median leng h o s ay, mos ly a ec ing he lowe limb
(n = 284, 76%), ollowed by he ace (n = 42, 11%) and he
uppe limb (n = 36, 10%). Fo y ou pe cen o he hospi al
admissions we e conside ed as p olonged LOS (n = 125).
Pa ien ’s cha ac e is ics a e shown in Table 1. A signi i-
can ly highe mean age was ound in he g oup o pa ien s
wi h p olonged LOS [64.5 (17.4) s. 59.5 (18.7); p = 0.01]
while no signi ican di e ences we e ound as ega ds pa-
ien ’s gende (p = 0.29), e en hough mos ly emale pa-
ien s wi h p olonged LOS we e ound. Ra es o 29% s.
20%, 33% s. 22%, 14% s. 12% and 26% s. 21% we e
ound as ega ds p olonged s. sho s ay, espec i ely, in
pa ien s wi h diabe es melli us, pe iphe al ascula disease,
immune impai men and p e ious local su ge y. A p e ious
his o y o celluli is/e ysipelas was ound in 21% o hospi al
admissions and a leas one p e ious hospi al admission
due o he same eason was ound in 6% o he cases. As
ega ds he episode o celluli is/e ysipelas unde lying he
hospi al admission, he p esence o complica ions was
signi ican ly mo e equen in pa ien s wi h p olonged LOS
(27% s. 13%; p = 0.001). The complica ions associa ed
wi h celluli is/e ysipelas a e shown in Table 2. The iden i ica-
ion o a po al o en y was simila in bo h g oups (52% s.
51%). Cul u es we e ca ied ou in 262 admissions, which
we e posi i e in 31% (n = 82) o he cases (72 cases wi h a
posi i e exuda e cul u e, se en wi h a posi i e blood cul u e
and h ee wi h bo h posi i e exuda e and blood cul u es).
The mic oo ganisms ha we e g own a e shown in Fig. 1.
Finally, no signi ican di e ences we e ound as ega ds
an an ibio ic ea men on he week p e ious o admission,
e en hough his was mo e equen ly ound in he g oup
wi h a p olonged LOS (35% s. 27%) (p = 0.11).
The adjus men o he model o logis ic eg ession has
allowed o he iden i ica ion o pa ien ’s age (p = 0.002),
p e ious admission wi h celluli is/e ysipelas (p = 0.005),
p esence o complica ions (p = 0.001), leukocy osis (p =
0.049), CRP alue (p = 0.035) and posi i e cul u e (p =
0.002) as ac o s associa ed wi h p olonged LOS (Ta-
ble 3). The p esence o p e ious admission wi h celluli is/
Table 2 – Complica ions associa ed wi h celluli is/e ysipelas
Gene al
(n = 66)
Sho s ay
(n = 32)
P olonged s ay
(n = 34)
Abscess – n (%) 33 (50%) 11 (35%) 22 (64%)
Lymphangi is – n (%) 22 (33%) 18 (56%) 4 (12%)
Skin ulce – n (%) 4 (6%) 1 (3%) 3 (9%)
Nec osis – n (%) 1 (2%) 0 (0%) 1 (3%)
Skin blis e – n (%) 2 (3%) 1 (3%) 1 (3%)
Os eoa icula in ol emen – n (%) 4 (6%) 1 (3%) 3 (9%)
Figu e 1 – Mic oo ganisms g own in cul u e.
MSSA: me hicillin-sensi i e S aphylococcus au eus; MRSA: me hicillin- esis an S aphylococcus au eus; P. ae uginosa: Pseudomona
ae uginosa; spp.: species. O he s, including: Se a ia ma cescens (n = 3), E. coli (n = 1), Klebsiella pneumoniae (n = 1), Pan oea agglo-
me ans (n = 1)
P olonged s ay Sho s ay
MSSA
+ P. aue ginosa
O he
P. ae uginosa
S ep ococcus spp.
MRSA
MSSA
2
4
3
1
8
3
7
9
4
16
20
5
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451
e ysipelas and he p esence o complica ions we e he mos
signi ican a iables.
The au ho s decla e ha ing ollowed he ongoing p o-
ocols a he heal hca e ins i u ion as ega ds he publica-
ion o any pe sonal da a. An anonymised da ase has been
used and none o he au ho s had any access o any iden i-
ica ion elemen s o he pa ien s. The s udy was ca ied ou
acco ding o he Helsinki Decla a ion o he Wo ld Medical
Associa ion.
DISCUSSION
This is he i s Po uguese s udy on he clinical and lab-
o a o ial ac o s associa ed wi h p olonged LOS o pa ien s
admi ed wi h celluli is/e ysipelas. The e o e, i was ound
ha pa ien ’s age, he p esence o a leas one p e ious
hospi al admission wi h celluli is/e ysipelas, he p esence o
complica ions, leukocy osis, CRP alue on admission and
a posi i e cul u e we e associa ed wi h a long hospi al s ay.
In addi ion o highe associa ed cos s, p olonged LOS
due o celluli is/e ysipelas is equen ly associa ed wi h he
need o addi ional clinical e alua ion wi h diagnos ic es s
(including imaging), wi h in asi e p ocedu es, including
su gical d ainage o deb idemen , long- e m an ibio ic ea -
men , wi h he isk o nosocomial in ec ions and delayed e-
co e y o he ac i i ies o daily li ing, wi h an impac on he
pa ien ’s quali y o li e.
Despi e no ideal an ibio ic egimen has e e been es-
ablished, a he apeu ic p o ocol based on he p esence o
como bidi ies and p e ious an ibio ic ea men is ollowed
in ou depa men . E en hough clinical guidelines ha e al-
eady been ecommended o he app oach and ea men
o pa ien s wi h celluli is/e ysipelas, he e a e s ill ew da a
allowing o he iden i ica ion o pa ien s a isk o p olonged
LOS and, in addi ion, ha could bene i om a mo e agg es-
si e ea men .2,3
In line wi h ou s udy, o he s udies ha e looked o he
cha ac e is ics o pa ien s wi h celluli is/e ysipelas associ-
a ed wi h p olonged LOS. Acco ding o he No h-Ame ican
mul i-cen ic s udy by Gang e al. on 4,224 hospi al admis-
sions due o lowe limb celluli is/e ysipelas, a iables such
as pa ien ’s age, emale gende , diabe es melli us, achy-
ca dia, hypo ension, leukocy osis, neu ophilia and ele a -
ed se um c ea inine we e associa ed wi h p olonged LOS.4
In a s udy om New Zealand, in ol ing 51 pa ien s admi -
ed wi h lowe limb celluli is, i has been ound ha an ele-
a ed neu ophil coun , he sco e o oedema and he use
o diu e ics we e independen ly associa ed wi h p olonged
LOS.5 In 2003, Ca a alà e al. ha e examined 332 pa ien s
admi ed wi h celluli is, ega dless o i s loca ion and ha e
eached he conclusion ha pa ien s wi h mul iple como -
bidi ies, hypoalbuminaemia, kidney ailu e o skin nec osis
on admission emained longe in he hospi al.6 In addi ion,
an Aus alian s udy in ol ed 395 episodes o celluli is/e -
ysipelas a ec ing di e en ana omical loca ions has ound
ha o e 60 yea s o age, symp oms las ing mo e han 4
days, he p esence o hypoalbuminaemia, he p esence
o bac e aemia and me hicillin- esis an S aphylococcus
au eus (MRSA) we e associa ed wi h p olonged LOS. On
he o he hand, neu ophilia and ele a ed se um c ea inine
we e no associa ed wi h p olonged LOS in his analysis.7
Finally, a Canadian s udy based on he na ional da abase o
65,454 pa ien s admi ed wi h celluli is has shown ha o e
65 yea s o age, emale gende and conges i e hea ailu e
we e ac o s associa ed wi h p olonged LOS.8
He e ogeneous esul s s ill exis and could be in lu-
enced by he absence o clea ly de ined c i e ia o he di-
agnosis and app oach o pa ien s wi h celluli is/e ysipelas,
leading o di e en app oaches in he di e en cen es, as
well as ega ding he a e age LOS.9–11 Howe e , Gang e
al. a gued ha he esul s o hese s udies could ep esen
an impo an ool o he cons uc ion o a se e i y sco e,4
in line wi h he sco es applied o pneumonia ha led o he
educ ion o he a es o hospi al admission, as well as LOS
and associa ed complica ions.12–15
The p esence o po en ial con ounding ac o s o p o-
longed LOS is one o he majo limi a ions o his obse -
a ional s udy, including un a ou able social backg ound
o o he complica ions no di ec ly ela ed o he episode
o celluli is/e ysipelas. Howe e , he applica ion o an im-
p o ed logis ic eg ession model, wi h a s epwise da a en-
y me hod, was aimed a educing he s a is ical impac o
con ounding ac o s.
CONCLUSION
In conclusion, he knowledge o he p edic i e clinical
and labo a o ial cha ac e is ics could be ele an o im-
p o ed heal hca e deli e y, aimed a educing he leng h o
s ay and associa ed isks and cos s.
HUMAN AND ANIMAL PROTECTION
The au ho s decla e ha he ollowed p ocedu es we e
acco ding o egula ions es ablished by he E hics and
Table 3 – Imp o ed logis ic eg ession, including 70% o da a (262/372), due o missing alues
p- alue Adjus ed odds a io 95% con idence in e al
Age 0.002 1.03 1.01 – 1.04
P e ious hospi al admission due o celluli is/
e ysipelas 0.005 4.81 1.63 –14.23
Pe iphe al ascula disease 0.42 1.30 0.69 – 2.46
Complica ions 0.001 3.28 2.63 – 6.59
Leukocy osis 0.049 1.81 1.00 – 3.30
CRP 0.035 1.03 1.00 – 1.06
Posi i e cul u e* 0.002 2.59 1.41 – 4.79
Roda A, e al. Fac o s associa ed wi h p olonged hospi al s ay among pa ien s wi h celluli is/e ysipelas, Ac a Med Po 2019 Jun;32(6):448–452
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Clinical Resea ch Commi ee and acco ding o he Helsinki
Decla a ion o he Wo ld Medical Associa ion.
DATA CONFIDENTIALITY
The au ho s decla e ha hey ha e ollowed he p o o-
cols o hei wo k cen e on he publica ion o pa ien da a.
In o med consen s we e ob ained.
CONFLICTS OF INTEREST
The au ho s decla e ha he e we e no con lic s o in e -
es in w i ing his manusc ip .
FINANCIAL SUPPORT
The au ho s decla e ha he e was no public o p i a e
inancial suppo in w i ing his manusc ip .
Roda A, e al. Fac o s associa ed wi h p olonged hospi al s ay among pa ien s wi h celluli is/e ysipelas, Ac a Med Po 2019 Jun;32(6):448–452
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