Academic Edi o : Albe o
En ico Ma aolo
Recei ed: 22 No embe 2024
Re ised: 30 Decembe 2024
Accep ed: 8 Janua y 2025
Published: 9 Janua y 2025
Ci a ion: Szabó, S.; Feie , B.;
Mă ginean, A.; Dumi ana, A.-E.;
Cos in, S.L.; C is ea, C.; Bolboacă, S.D.
E alua ion o he Bac e ial In ec ions
and An ibio ic P esc ibing P ac ices in
he In ensi e Ca e Uni o a Clinical
Hospi al in Romania. An ibio ics 2025,
14, 64. h ps://doi.o g/10.3390/
an ibio ics14010064
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Licensee MDPI, Basel, Swi ze land.
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A icle
E alua ion o he Bac e ial In ec ions and An ibio ic P esc ibing
P ac ices in he In ensi e Ca e Uni o a Clinical Hospi al
in Romania
Sándo Szabó 1,†, Bogdan Feie 1,†, Alina Mă ginean 2, And a-Elena Dumi ana 2, Simona Ligia Cos in 2,
Cecilia C is ea 1,* and So ana D. Bolboacă3
1Depa men o Analy ical Chemis y, Facul y o Pha macy, “Iuliu Ha
,ieganu” Uni e si y o Medicine and
Pha macy, 4 Pas eu S ee , 400349 Cluj-Napoca, Romania; [email p o ec ed] (S.S.);
eie .geo [email p o ec ed] (B.F.)
2“D . Cons an in Papilian” Mili a y Eme gency Hospi al, 400132 Cluj-Napoca, Romania;
[email p o ec ed] (A.M.); [email p o ec ed] (A.-E.D.); [email p o ec ed] (S.L.C.)
3Depa men o Medical In o ma ics and Bios a is ics, Facul y o Medicine, “Iuliu Ha
,ieganu” Uni e si y o
Medicine and Pha macy Cluj-Napoca, 400349 Cluj-Napoca, Romania; [email p o ec ed]
*Co espondence: [email p o ec ed]o
†These au ho s con ibu ed equally o his wo k.
Abs ac : In oduc ion: Heal hca e-associa ed in ec ions (HAIs) a e associa ed wi h in-
c eased mo ali y, an imic obial esis ance, and high an ibio ic use. Me hods: The cha ac-
e is ics o bac e ial esis ance and an ibio ic consump ion in he in ensi e ca e uni (ICU)
o a clinical hospi al in Romania we e e alua ed. Demog aphic da a o pa ien s, iden i ied
bac e ia, an ibio ics adminis e ed, and hei sensi i i y p o iles we e collec ed and analyzed.
Resul s: One hund ed and wen y- i e pa ien s, wi h a median age o 68 yea s, mos ly male
(60%), we e included in he s udy. Mo e han one- hi d o he pa ien s died. The deceased
pa ien s we e olde (median age o 74 yea s), had longe hospi aliza ion (median o 9 days)
and bac e ia de ec ed (55.3%), and had highe an ibio ic consump ion han he discha ged
pa ien s. The mos equen bac e ia iden i ied in ou coho we e Acine obac e baumannii,
Klebsiella pneumoniae, and Pseudomonas ae uginosa in deceased pa ien s and Klebsiella pneu-
moniae,Esche ichia coli,S aphylococcus hemoly icus, and En e ococcus aecalis in he su i ed
g oup. The op h ee an ibio ics used we e ce iaxone, me onidazole, and me openem.
Resis ance o an ibio ics was obse ed in 44.3% o he deceased g oup and 37.5% o pa ien s
who we e discha ged (χ2= 5.5, p= 0.0628). Discussion: A posi i e mono onic associa ion
was obse ed be ween he numbe o hospi aliza ion days and he numbe o an ibio ic
doses, wi h a highe co ela ion coe icien o deceased pa ien s (0.6327, p< 0.0001) han in
su i ed g oup (0.4749, p< 0.0001). Conclusions and Fu u e T ends: This s udy p o ides
a eal pic u e o HAIs, he cha ac e is ics o bac e ia, and he consump ion o an ibio ics in
an ICU o a clinical hospi al in Romania. The da a ob ained a e simila o hose om o he
in e na ional s udies, bu u he s udies a e needed o e lec he eal si ua ion in Romania.
Keywo ds: heal hca e-associa ed in ec ions (HAIs); bac e ia; an ibio ic (AB); in ensi e ca e
uni (ICU); an ibio ic esis ance
1. In oduc ion
Heal hca e-associa ed in ec ions (HAIs) a e se ious in ec ions and a majo public
heal h p oblem [
1
,
2
] associa ed wi h a signi ican isk o mo bidi y, mo ali y, and p olonged
hospi al s ay [
3
–
5
]. In Eu ope, app oxima ely ou million pa ien s a e in ec ed annually
An ibio ics 2025,14, 64 h ps://doi.o g/10.3390/an ibio ics14010064
An ibio ics 2025,14, 64 2 o 18
in heal hca e acili ies [
3
,
6
]. Heal hca e-associa ed in ec ions a e associa ed wi h a 4- old
highe mo ali y a e and a 3- old longe hospi aliza ion [7].
Admission o hospi als in eme ging coun ies such as Romania is associa ed wi h
a 15% isk o de eloping HAI [
1
,
3
], bu HAIs emain unde - epo ed [
8
]. The isk o
occu ence o HAIs in de eloped coun ies is, on a e age, 5% (up o 16%); howe e , in
he In ensi e Ca e Uni (ICU), his isk can be highe and can inc ease o 30% compa ed
o o he hospi al wa ds [
3
]. In ensi e-ca e in ec ions cons i u e app oxima ely hal o all
HAIs [
7
]. The mos common HAIs in he ICU a e en ila o -associa ed pneumonia (VAP),
u ina y ac in ec ions (UTIs), and bloods eam in ec ions (BSIs) [
1
,
4
]. The p esence o
HAIs in pa ien s hospi alized in he ICU p olongs hospi aliza ion by i e days [
9
]. HAIs a e
esponsible o a di ec cos o €7 billion annually [
1
]. HAIs inc ease he use o an ibio ics,
he eme gence o mul i- esis an bac e ia, mo bidi y, mo ali y a es, and he cos o medical
ca e [
3
,
4
,
7
]. The p esence o HAIs is associa ed wi h highe an ibio ic consump ion as i
equi es he use o b oad-spec um an ibio ics o a long pe iod, he eby inc easing he
isk o an ibio ic esis ance [
10
]. Fo op imal an ibio ic managemen , he implemen a ion
o an ibio ic s ewa dship p og ams is needed. El-Sokka y e al. analyzed he da a om
57 ICUs in 24 coun ies ega ding in ec ion p e en ion and con ol p og ams, and an ibio ic
s ewa dship ac i i ies and showed ha mos cen e s ha e a su eillance p og am [
11
]. Such
p og ams may educe he eme gence o d ug- esis an bac e ia. In Romania, an ibio ic-
esis an in ec ions accoun o o e 60% o all HAI cases, compa ed o app oxima ely 5%
in Finland; howe e , he e alua ed samples we e small in some cases [
1
,
12
]. The mos
common mul i-d ug esis an (MDR) bac e ia a e de ined using he ac onym ESKAPE:
En e ococcus aecium,S aphylococcus au eus,Klebsiella pneumoniae,Acine obac e baumannii,
Pseudomonas ae uginosa, and En e obac e spp. [
13
]. App oxima ely 70% o pa ien s in he
ICUs ecei e an ibio ic ea men [
14
]. The use o an imic obials in Eu opean ICUs depends
mainly on he a ailabili y o an ibio ics; he e o e, he e a e di e ences be ween coun ies
in e ms o an ibio ic molecules used.
Romania has implemen ed measu es o p e en and limi HAIs and o dec ease
an imic obial esis ance [
15
]; howe e , da a on he bac e ia and consump ion o an ibio ics
in ICUs a e limi ed. In his s udy, we aimed o in es iga e he e iology o bac e ial in ec ions
in he ICU o a clinical hospi al in Romania and o desc ibe he bac e ial pa e n in collec ed
biological samples and an ibio ic consump ion in deceased and su i ing pa ien s.
2. Resul s
2.1. The E alua ed Coho
Fou hund ed and se en y-se en pa ien s we e hospi alized du ing he s udy pe iod,
o whom 125 me he inclusion c i e ia and we e e alua ed. Mo e han one- hi d o he pa-
ien s we e included in he deceased g oup, and hese pa ien s had a longe hospi aliza ion
s ay, and used a highe numbe o di e en an ibio ics and an ibio ic doses han hose who
su i ed (Table 1).
Table 1. Cha ac e is ics o he e alua ed coho .
Cha ac e is ic All (n= 125) Deceased (n= 38) Su i ed (n= 87) p-Value
Age a
0.1794
Median [Q1 o Q3] 68 [62 o 79] 74 [63.3 o 81.8] 68 [61 o 77.5]
{min o max} {39 o 94} {48 o 93} {39 o 94}
Sex b
0.3825
Women 50 (40) 13 (34.2) 37 (42.5)
Men 75 (60) 25 (65.8) 50 (57.5)
An ibio ics 2025,14, 64 3 o 18
Table 1. Con .
Cha ac e is ic All (n= 125) Deceased (n= 38) Su i ed (n= 87) p-Value
Days o hospi al s ay a
0.0031
Median [Q1 o Q3] 6 [4 o 10] 9 [5.3 o 13.8] 6 [4 o 8]
{min o max} {3 o 48} {3 o 35} {3 o 48}
No. o biological samples b
0.1036
0 43 (34.4) 8 (21.1) 35 (40.2)
1 40 (32) 17 (44.7) 23 (26.4)
2 19 (15.2) 7 (18.4) 12 (13.8)
>2 23 (18.4) 6 (15.8) 17 (19.5)
No. o bac e ia b,*
0.0342
0 71 (56.8) 17 (44.7) 54 (62.1)
1 24 (19.2) 6 (15.8) 18 (20.7)
2 21 (16.8) 12 (31.6) 9 (10.3)
>2 9 (7.2) 3 (7.9) 6 (6.9)
No. o an ibio ics b
0.0261
1 47 (37.9) 13 (34.2) 34 (39.5)
2 44 (35.5) 9 (23.7) 35 (40.7)
>2 33 (26.6) 16 (42.1) 17 (19.8)
No. o pa ien s wi h a leas
one c
R 46 (36.8) 18 (47.4) 28 (32.2) 0.1054
I 17 (13.6) 8 (21.1) 9 (10.3) 0.1082
S 53 (42.4) 2330 (52.6) 33 (37.9) 0.1261
To al no. o an ibio ic doses a
0.0040
Median [Q1 o Q3] 15 [9 o 31] 18 [14.3 o 45] 13 [7.5 o 26.5]
{min o max} {0 o 172} {4 o 137} {0 o 172}
a
median [Q1 o Q3], {min o max}, whe e Q1 is he i s qua ile, Q3 is he hi d qua ile, min is hen minimum,
max is he maximum; compa ison be ween g oups wi h Mann–Whi ney es .
b
no (%), compa ison wi h Chi-
squa ed es o * Fishe ’s exac es .
c
Numbe o cases wi h a leas one case o R = esis ance; I = in e media y;
S = sensible.
The op h ee biological samples collec ed we e u ine, b onchial sec e ions, and pu-
ulen / luid sec e ions (Figu e 1a), and he mos equen bac e ium was A. baumannii
(Figu e 1b).
An ibio ics 2025, 14, x FOR PEER REVIEW 3 o 18
Table 1. Cha ac e is ics o he e alua ed coho .
Cha ac e is ic All (n = 125) Deceased (n = 38) Su i ed (n = 87) p-Value
Age a
0.1794
Median [Q1 o Q3] 68 [62 o 79] 74 [63.3 o 81.8] 68 [61 o 77.5]
{min o max} {39 o 94} {48 o 93} {39 o 94}
Sex b
0.3825
Women 50 (40) 13 (34.2) 37 (42.5)
Men 75 (60) 25 (65.8) 50 (57.5)
Days o hospi al s ay a
0.0031
Median [Q1 o Q3] 6 [4 o 10] 9 [5.3 o 13.8] 6 [4 o 8]
{min o max} {3 o 48} {3 o 35} {3 o 48}
No. o biological samples b
0.1036
0 43 (34.4) 8 (21.1) 35 (40.2)
1 40 (32) 17 (44.7) 23 (26.4)
2 19 (15.2) 7 (18.4) 12 (13.8)
>2 23 (18.4) 6 (15.8) 17 (19.5)
No. o bac e ia b,*
0.0342
0 71 (56.8) 17 (44.7) 54 (62.1)
1 24 (19.2) 6 (15.8) 18 (20.7)
2 21 (16.8) 12 (31.6) 9 (10.3)
>2 9 (7.2) 3 (7.9) 6 (6.9)
No. o an ibio ics b
0.0261
1 47 (37.9) 13 (34.2) 34 (39.5)
2 44 (35.5) 9 (23.7) 35 (40.7)
>2 33 (26.6) 16 (42.1) 17 (19.8)
No. o pa ien s wi h a leas one c
R 46 (36.8) 18 (47.4) 28 (32.2) 0.1054
I 17 (13.6) 8 (21.1) 9 (10.3) 0.1082
S 53 (42.4) 2330 (52.6) 33 (37.9) 0.1261
To al no. o an ibio ic doses a
0.0040 Median [Q1 o Q3] 15 [9 o 31] 18 [14.3 o 45] 13 [7.5 o 26.5]
{min o max} {0 o 172} {4 o 137} {0 o 172}
a median [Q1 o Q3], {min o max}, whe e Q1 is he i s qua ile, Q3 is he hi d qua ile, min is hen
minimum, max is he maximum; compa ison be ween g oups wi h Mann–Whi ney es . b no (%),
compa ison wi h Chi-squa ed es o * Fishe s exac es . c Numbe o cases wi h a leas
one case o R = esis ance; I = in e media y; S = sensible.
(a) (b)
9%
3%
15%
34%
21%
43%
3%
0%
37%
21%
18%
53%
0% 10% 20% 30% 40% 50% 60%
Canulla
Ce eb ospinal luid
B onchial sec e ion
Pu ulen / luid sec e ion
Blood
U ine
Biological sample
dead ali e
3%
11%
7%
6%
1%
13%
2%
2%
0%
5%
5%
2%
7%
0%
0%
1%
26%
8%
11%
5%
3%
13%
5%
0%
3%
13%
8%
3%
3%
3%
3%
0%
0% 5% 10% 15% 20% 25% 30%
Acine obac e baumannii
Esche ichia coli
En e ococcus aecalis
En e ococcus aecium
En e obac e cloacae
Klebsiella pneumoniae
P o eus mi abilis
P o eus penne i
P o idencia s ua ii
Pseudomonas ae uginosa
S aphylococcus au eus
S aphylococcus epide midis
S aphylococcus hemoly icus
S aphylococcus simulans
S aphylococcus hominis
S aphylococcus wa ne i dead ali e
Figu e 1. (a) Dis ibu ion o collec ed biological samples (38 deceased pa ien s and 87 who su i ed);
(b) dis ibu ion o bac e ia pe g oup exp essed as he numbe o posi i e cases pe numbe o eligible
cases, conside ing ha he same pa ien can ha e mo e han one bac e ium).
An ibio ics 2025,14, 64 4 o 18
2.2. Types o Bac e ia and Dis ibu ion in Collec ed Biological Samples
The mos equen ly iden i ied bac e ia we e A. baumannii,K. pneumoniae, and P. ae uginosa
in he deceased g oup and K. pneumoniae,Esche ichia coli,S. hemoly icus, and E. aecalis in
he su i ing g oup (Figu e 1b).
K. pneumoniae was he only bac e ia iden i ied in he cannula samples ( wo cases). One
ce eb al luid cul u e e ealed he p esence o K. pneumoniae.
Conside ing he possibili y o mul iple biological samples being collec ed om pa-
ien s, 41 posi i e cul u es we e iden i ied in he deceased g oup and 51 we e iden i ied
in he su i ing g oup. Two bac e ia wi h a p e alence highe han 10% we e obse ed
exclusi ely in he deceased g oup: A. baumannii and K. pneumoniae. The numbe o cases
wi h posi i e cul u es in biological samples by g oup a e p esen ed in Table 2.
Table 2. Dis ibu ion o bac e ia in biological samples by g oup.
Bac e ium Biological Sample No. Pa ien s (Pe cen age, %)
All, n= 125 Deceased, n= 38 Su i ed, n= 87
Acine obac e baumannii B onchial sec e ion 9 (7.2) 7 (18.4) 2 (2.3)
Pu ulen / luid sec e ion 4 (3.2) 3 (7.9) 1 (1.1)
En e obac e cloacae B onchial sec e ion 2 (1.6) 1 (2.6) 1 (1.1)
En e ococcus aecalis
Blood 2 (1.6) 1 (2.6) 1 (1.1)
U ine 2 (1.6) 1 (2.6) 1 (1.1)
Pu ulen / luid sec e ion 5 (4) 2 (5.3) 3 (3.4)
En e ococcus aecium
Blood 1 (0.8) 1 (2.6)
U ine 3 (2.4) 1 (2.6) 2 (2.3)
Pu ulen / luid sec e ion 4 (3.2) 1 (2.6) 3 (3.4)
Esche ichia coli
Blood 1 (0.8) 1 (1.1)
U ine 4 (3.2) 4 (4.6)
B onchial sec e ion 1 (0.8) 1 (1.1)
Pu ulen / luid sec e ion 7 (5.6) 3 (7.9) 4 (4.6)
Klebsiella pneumoniae
Cannula 2 (1.6) 2 (2.3)
Ce eb ospinal luid 1 (0.8) 1 (2.6)
Blood 1 (0.8) 1 (1.1)
U ine 2 (1.6) 2 (2.3)
B onchial sec e ion 9 (7.2) 5 (13.2) 4 (4.6)
Pu ulen / luid sec e ion 3 (2.4) 3 (3.4)
P o eus mi abilis
U ine 2 (1.6) 2 (2.3)
B onchial sec e ion 1 (0.8) 1 (2.6)
Pu ulen / luid sec e ion 1 (0.8) 1 (2.6)
P o eus penne i Pu ulen / luid sec e ion 2 (1.6) 2 (2.3)
P o idencia s ua i Blood 1 (0.8) 1 (2.6)
Pseudomonas ae uginosa U ine 3 (2.4) 3 (7.9)
B onchial sec e ion 2 (1.6) 2 (5.3)
S aphylococcus au eus
B onchial sec e ion 2 (1.6) 1 (2.6) 2 (2.3)
Pu ulen / luid sec e ion 5 (4) 2 (5.3) 1 (1.1)
U ine 1 (0.8) 1 (1.1)
S aphylococcus epide midis
U ine 1 (0.8) 1 (2.6)
B onchial sec e ion 2 (1.6) 2 (2.3)
Blood 1 (0.8) 1 (1.1)
An ibio ics 2025,14, 64 5 o 18
Table 2. Con .
Bac e ium Biological Sample No. Pa ien s (Pe cen age, %)
All, n= 125 Deceased, n= 38 Su i ed, n= 87
S aphylococcus hemoly icus
Blood 4 (3.2) 1 (2.6) 3 (3.4)
U ine 1 (0.8) 1 (1.1)
Pu ulen / luid sec e ion 2 (1.6) 2 (2.3)
S aphylococcus hominis Blood 1 (0.8) 1 (2.6)
S aphylococcus simulans Blood 1 (0.8) 1 (2.6)
S aphylococcus wa ne i Pu ulen / luid sec e ion 1 (0.8) 1 (1.1)
Da a a e exp essed as numbe and co esponding pe cen age (%).
2.3. Adminis e ed An ibio ics
Pa ien s wi h no bac e ia iden i ied in hei biological samples ecei ed up o h ee
an ibio ics (deceased s. su i ed: 88:89% up o wo an ibio ics and 12:11% h ee an-
ibio ics). Di e en an ibio ics we e adminis e ed, including an ibio ics wi h he same o
di e en pha maceu ical o ms. The dis ibu ion o an ibio ics adminis e ed o pa ien s
wi h mul iple o no bac e ial in ec ions is p esen ed in Table 3.
Table 3. The numbe o an ibio ics adminis e ed pe numbe o iden i ied bac e ia s a i ied by g oup.
No. o An ibio ics o No. Pa ien s (Pe cen age, %)
All, n= 125 Deceased, n= 38 Su i ed, n= 87
no bac e ia 71 (56.8) 17 (44.7) 54 (62.1)
1 AB 32 (45.1) 8 (47.1) 24 (44.4)
2 ABs 31 (43.7) 7 (41.2) 24 (44.4)
3 ABs 8 (11.3) 2 (11.8) 6 (11.1)
1 bac e ium 24 (19.2) 6 (15.8) 18 (20.7)
1 AB 10 (41.7) 2 (33.3) 8 (44.4)
2 ABs 8 (33.3) 1 (16.7) 7 (38.9)
3 ABs 6 (25) 3 (50) 3 (16.7)
2 bac e ia 21 (16.8) 12 (31.6) 9 (10.3)
1 AB 5 (23.8) 3 (25) 2 (22.2)
2 ABs 3 (14.3) 1 (8.3) 2 (22.2)
3 ABs 8 (38.1) 6 (50) 2 (22.2)
>3 ABs 5 (23.8) 2 (16.7) 3 (33.3)
3 bac e ia 5 (4) 2 (5.3) 3 (3.4)
no AB 1 (20) 0 (0) 1 (33.3)
2 ABs 1 (20) 0 (0) 1 (33.3)
3 ABs 1 (20) 1 (50) 0 (0)
>3 ABs 2 (40) 1 (50) 1 (33.3)
4 bac e ia 4 (3.2) 1 (2.6) 3 (3.4)
2 ABs 1 (25) 0 (0) 1 (33.3)
3 ABs 1 (25) 0 (0) 1 (33.3)
>3 ABs 2 (50) 1 (100) 1 (33.3)
Da a a e epo ed as no (%). AB = an ibio ic.
Table 4summa izes he an ibio ics used in deceased and su i ing pa ien s. The op i e
an ibio ics used we e ce iaxone (34.2% deceased s. 28.7% su i ed, p= 0.5405), me on-
idazole (15.8% deceased s. 32.2% su i ed, p= 0.0581), me openem (36.8% deceased s.
20.7% su i ed, p= 0.0570), ancomycin (23.7% deceased s. 11.5% su i ed, p= 0.0808), and
amoxicillin/cla ulanic acid (26.3% deceased s. 8.0% su i ed, p= 0.0061).
An ibio ics 2025,14, 64 6 o 18
Table 4. The use o an ibio ics by g oup.
An ibio ic No. Pa ien s (Pe cen age, %)
All, n= 125 Deceased, n= 38 Su i ed, n= 87
Amikacin 500 mg 3 (2.4) 1 (2.6) 2 (2)
Amoxicillin/Cla ulanic acid
1000/200 mg 17 (13.6) 10 (26.3) 7 (7.1)
Ampicillin 1 g 3 (2.4) 1 (2.6) 2 (2)
Azi h omycin 500 mg 2 (1.6) 1 (2.6) 1 (1)
Ce azolin 1 g 1 (0.8) 0 (0) 1 (1)
Ce ope azon/Sulbac am
1000/1000 mg 20 (16) 2 (5.3) 18 (18.4)
Ce azidime 1 g 3 (2.4) 2 (5.3) 1 (1)
Ce iaxone 1 g 38 (30.4) 13 (34.2) 25 (25.5)
Ce u oxime 1.5 g 15 (12) 0 (0) 15 (15.3)
Clindamycin 300 mg/2 mL 4 (3.2) 1 (2.6) 3 (3.1)
Colis in 1MUI 13 (10.4) 6 (15.8) 7 (7.1)
Doxycycline 100 mg 4 (3.2) 2 (5.3) 2 (2)
E y h omycin 200 mg 4 (3.2) 1 (2.6) 3 (3.1)
E apenem 1 g 7 (5.6) 1 (2.6) 6 (6.1)
Fos omycin 3 g p.o. 1 (0.8) 0 (0) 1 (1)
Gen amicin 80 mg 2 (1.6) 0 (0) 2 (2)
Linezolid 2 mg/mL 2 (1.6) 1 (2.6) 1 (1)
Me openem 1000 mg 32 (25.6) 14 (36.8) 18 (18.4)
Me onidazole 250 mg 10 (8) 2 (5.3) 8 (8.2)
Me onidazole 5 g/200 mL 34 (27.2) 6 (15.8) 28 (28.6)
Moxi loxacin 400 mg/250 mL 2 (1.6) 1 (2.6) 1 (1)
Oxacillin 1000 mg 2 (1.6) 2 (5.3) 0 (0)
Penicillin G Po assium1 MUI 1 (0.8) 0 (0) 1 (1)
Pipe acillin/Tazobac am 2 g/0.25 g 6 (4.8) 4 (10.5) 2 (2)
Ri ampin 300 mg caps. 1 (0.8) 1 (2.6) 0 (0)
Tigecycline 50 mg 2 (1.6) 0 (0) 2 (2)
Teicoplanin 400 mg 1 (0.8) 1 (2.6) 0 (0)
T ime hop im/Sul ame hoxazole
400/80 mg 4 (3.2) 3 (7.9) 1 (1)
Vancomycin 1 g 19 (15.2) 9 (23.7) 10 (10.2)
Da a epo ed as a numbe (%).
The dis ibu ion o an ibio ics by bac e ia and g oup, conside ing ha a pa ien could ha e
mo e han one bac e ium iden i ied, and mo e han one an ibio ic used, is p esen ed in Table 5.
Table 5. Dis ibu ion o adminis e ed an ibio ics by bac e ia and g oup.
Bac e ium Adminis e ed An ibio ic
Deceased, n= 38 Su i ed, n= 87
Acine obac e baumannii
Amikacin 500 mg (n= 1)
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 1)
Ampicillin 1 g (n= 1)
Ce azidime 1 g (n= 2)
Ce iaxone 1 g (n= 3)
Colis in 1 MUI (n= 6)
E apenem 1 g (n= 1)
Me openem 1000 mg (n= 6)
Me onidazole 5 g/200 mL (n= 3)
Pipe acillin/Tazobac am 2 g/0.25 g
(n= 2)
Ri ampin 300 mg caps. (n= 1)
T ime hop im/Sul ame hoxazole
400/80 mg (n= 2)
Vancomicyn 1 g (n= 3)
Ce iaxone 1 g (n= 1)
Colis in 1 MUI (n= 3)
E y h omicin 200 mg (n= 1)
Me openem 1000 mg (n= 3)
Me onidazole 5 g/200 mL (n= 1)
Pipe acillin/Tazobac am 2 g/0.25 g
(n= 1)
Vancomycin 1 g (n= 2)
An ibio ics 2025,14, 64 7 o 18
Table 5. Con .
Bac e ium Adminis e ed An ibio ic
Deceased, n= 38 Su i ed, n= 87
Esche ichia coli
Colis in 1 MUI (n= 1)
E apenem 1 g (n= 1)
Me openem 1000 mg (n= 3)
Me onidazole 250 mg (n= 1)
Me onidazole 5 g/200 mL (n= 1)
Ri ampin 300 mg caps. (n= 1)
Vancomycin 1 g (n= 1)
Ampicillin 1 g (n= 2)
Ce azolin 1 g (n= 1)
Ce ope azone/Sulbac am
1000/1000 mg (n= 1)
Ce iaxone 1 g (n= 3)
Colis in 1 MUI (n= 2)
E apenem 1 g (n= 3)
Me openem 1000 mg (n= 3)
Me onidazole 250 mg (n= 1)
Me onidazole 5 g/200 mL (n= 5)
Vancomycin 1 g (n= 1)
En e ococcus aecalis
Amikacin 500 mg (n= 1)
Colis in 1 MUI (n= 2)
Me openem 1000 mg (n= 4)
Me onidazole 5 g/200 mL (n= 1)
Teicoplanin 400 mg (n= 1)
T ime hop im/Sul ame hoxazole
400/80 mg (n= 2)
Vancomycin 1 g (n= 1)
Ce azolin 1 g (n= 1)
Ce iaxone 1 g (n= 4)
Doxycycline 100 mg (n= 1)
Linezolid 2 mg/mL (n= 1)
Me openem 1000 mg (n= a)
Me onidazole 5 g/200 mL (n= 2)
En e ococcus aecium
Ce iaxone 1 g (n= 2)
Colis in 1 MUI (n= 1)
Me openem 1000 mg (n= 1)
Vancomycin 1 g (n= 1)
Ampicillin 1 g (n= 2)
Ce iaxone 1 g (n= 3)
Colis in 1 MUI (n= 2)
E y h omycin 200 mg (n= 1)
E apenem 1 g (n= 1)
Me openem 1000 mg (n= 2)
Me onidazole 5 g/200 mL (n= 2)
Vancomycin 1 g (n= 1)
Klebsiella pneumoniae
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 2)
Ampicillin 1 g (n= 1)
Ce azidime 1 g (n= 2)
Ce iaxone 1 g (n= 1)
Colis in 1 MUI (n= 2)
Me openem 1000 mg (n= 1)
Me onidazole 5 g/200 mL (n= 1)
Pipe acillin/Tazobac am 2 g/0.25 g
(n= 2)
Vancomycin 1 g (n= 1)
Amikacin 500 mg (n= 1)
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 1)
Ampicillin 1 g (n= 2)
Ce ope azone/Sulbac am
1000/1000 mg (n= 1)
Ce iaxone 1 g (n= 3)
Clindamycin 300 mg/2 mL (n= 1)
Colis in 1 MUI (n= 4)
E apenem 1 g (n= 2)
Fos omycina 3 g p.o. (n= 1)
Me openem 1000 mg (n= 8)
Me onidazole 250 mg (n= 2)
Me onidazole 5 g/200 mL (n= 2)
Tigecycline 50 mg (n= 2)
Vancomycin 1 g (n= 2)
P o eus mi abilis
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 1)
Me openem 1000 mg (n= 1)
Oxacillin 1000 mg (n= 1)
T ime hop im/Sul ame hoxazole
400/80 mg (n= 1)
Ce ope azone/Sulbac am
1000/1000 mg (n= 1)
Ce iaxone 1 g (n= 1)
Ce u oxime 1.5 g (n= 1)
Me openem 1000 mg (n= 1)
An ibio ics 2025,14, 64 8 o 18
Table 5. Con .
Bac e ium Adminis e ed An ibio ic
Deceased, n= 38 Su i ed, n= 87
Pseudomonas ae uginosa
Ce azidime 1 g (n= 2)
Ce iaxone 1 g (n= 1)
Colis in 1 MUI (n= 1)
Linezolid 2 mg/mL (n= 1)
Me openem 1000 mg (n= 3)
Pipe acillin/Tazobac am 2 g/0.25 g
(n= 2)
Vancomycin 1 g (n= 2)
Amikacin 500 mg (n= 1)
Ce azolin 1 g (n= 1)
Ce iaxone 1 g (n= 2)
Clindamycin 300 mg/2 mL (n= 1)
Colis in 1 MUI (n= 2)
Fos omycin 3 g p.o. (n= 1)
Me openem 1000 mg (n= 3)
Me onidazole 250 mg (n= 2)
Me onidazole 5 g/200 mL (n= 2)
Tigecycline 50 mg (n= 2)
Vancomycin 1 g (n= 1)
S aphylococcus au eus
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 2)
Ce iaxone 1 g (n= 2)
Clindamycin 300 mg/2 mL (n= 1)
Oxacillin 1000 mg (n= 2)
Pipe acillin/Tazobac am 2 g/0.25 g
(n= 1)
T ime hop im/Sul ame hoxazole
400/80 mg (n= 1)
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 1)
Ce iaxone 1 g (n= 2)
Clindamycin 300 mg/2 mL (n= 1)
Colis in 1 MUI (n= 1)
E y h omycin 200 mg (n= 1)
Me openem 1000 mg (n= 1)
Me onidazole 5 g/200 mL (n= 1)
Penicillin G po assium 1 MUI (n= 1)
Vancomycin 1 g (n= 2)
S aphylococcus epide midis
Amoxicillin/Cla ulanic acid
1000/200 mg (n= 1)
Me openem 1000 mg (n= 1)
Vancomycin 1 g (n= 1)
Ce iaxone 1 g (n= 2)
Ce u oxim 1.5 g (n= 1)
Me openem 1000 mg (n= 1)
Vancomycin 1 g (n= 1)
S aphylococcus hemoly icus
Me openem 1000 mg (n= 1)
Me onidazole 5 g/200 mL (n= 1)
Teicoplanin 400 mg (n= 1)
T ime hop im/Sul ame hoxazole
400/80 mg (n= 1)
Vancomycin 1 g (n= 1)
Ce iaxone 1 g (n= 4)
Colis in 1 MUI (n= 1)
Linezolid 2 mg/mL (n= 1)
Me openem 1000 mg (n= 2)
Tigecycline 50 mg (n= 1)
Vancomycin 1 g (n= 2)
Speci ic bac e ia we e iden i ied among deceased pa ien s only:
•
En e obac e cloacae and p esc ibed an ibio ics o pa ien s: amoxicillin/cla ulanic acid
1000/200 mg (n= 1), me openem 1000 mg (n= 1), and ancomycin 1 g (n= 1).
•
P o idencia s ua ii and p esc ibed an ibio ics o pa ien s: amoxicillin/cla ulanic acid
1000/200 mg (n= 1), e y h omycin 200 mg (n= 1), and ancomycin 1 g (n= 1).
•
S aphylococcus simulans and he p esc ibed an ibio ics we e as ollows: me openem
1000 mg (n= 1), me onidazole 5 g/200 mL (n= 1), eicoplanin 400 mg (n= 1),
ime hop im/sul ame hoxazole 400/80 mg (n= 1), and ancomycin 1 g (n= 1).
•
S aphylococcus hominis and p esc ibed an ibio ics o pa ien s: linezolid 2 mg/mL (n= 1),
me openem 1000 mg (n= 1), and ancomycin 1 g (n= 1).
An ibio ics 2025,14, 64 9 o 18
Speci ic bac e ia we e exclusi ely obse ed in he su i ing g oup:
•
P o eus penne i and used an ibio ics: ampicillin 1 g (n= 2), ce iaxone 1 g (n= 1),
colis in 1 MUI (n= 2), me openem 1000 mg (n= 2), me onidazole 5 g/200 mL (n= 1),
and ancomycin 1 g (n= 1).
•
S aphylococcus wa ne i and used an ibio ics: linezolid 2 mg/mL (n= 1) and me openem
1000 mg (n= 1).
A posi i e mono onic associa ion be ween hospi aliza ion leng h and numbe o
an ibio ic doses used was ound in he in es iga ed coho , wi h a highe co ela ion
coe icien in deceased pa ien s (
ρ
= 0.6327. p< 0.0001) han in he su i ing g oup
(ρ= 0.4749, p< 0.0001).
In he analyzed coho , he hospi aliza ion leng h was signi ican ly di e en among
pa ien s wi h a di e en numbe o collec ed biological samples ( om 0 o 5 samples,
wi h i e samples collec ed om wo pa ien s) (K uskal–Wallis es : p< 0.0001, Figu e 2).
The di e ence emained s a is ically signi ican o deceased pa ien s (K uskal–Wallis es :
p= 0.0124) only when pa ien s wi hou biological samples we e compa ed o hose wi h
h ee biological samples (pos hoc analysis, 0 s. 3: p= 0.0055). In he su i ing g oup,
he numbe o days o hospi aliza ion was also s a is ically signi ican (K uskal–Wallis es :
p= 0.0001), wi h he ollowing signi ican di e ences in pos hoc analysis: p= 0.0001 o 0
s. 4, p= 0.0028 o 1 s. 4, and p= 0.02621 o 2 s. 4.
An ibio ics 2025, 14, x FOR PEER REVIEW 8 o 18
S aphylococcus he-
moly icus
Me openem 1000 mg (n = 1)
Me onidazole 5 g/200 mL (n = 1)
Teicoplanin 400 mg (n = 1)
T ime hop im/Sul ame hoxazole 400/80 mg (n = 1)
Vancomycin 1 g (n = 1)
Ce iaxone 1 g (n = 4)
Colis in 1 MUI (n = 1)
Linezolid 2 mg/mL (n = 1)
Me openem 1000 mg (n = 2)
Tigecycline 50 mg (n = 1)
Vancomycin 1 g (n = 2)
Speci ic bac e ia we e iden i ied among deceased pa ien s only:
• En e obac e cloacae and p esc ibed an ibio ics o pa ien s: amoxicillin/cla ulanic acid
1000/200 mg (n = 1), me openem 1000 mg (n = 1), and ancomycin 1 g (n = 1).
• P o idencia s ua ii and p esc ibed an ibio ics o pa ien s: amoxicillin/cla ulanic acid
1000/200 mg (n = 1), e y h omycin 200 mg (n = 1), and ancomycin 1 g (n = 1).
• S aphylococcus simulans and he p esc ibed an ibio ics we e as ollows: me openem
1000 mg (n = 1), me onidazole 5 g/200 mL (n = 1), eicoplanin 400 mg (n = 1), ime-
hop im/sul ame hoxazole 400/80 mg (n = 1), and ancomycin 1 g (n = 1).
• S aphylococcus hominis and p esc ibed an ibio ics o pa ien s: linezolid 2 mg/mL (n =
1), me openem 1000 mg (n = 1), and ancomycin 1 g (n = 1).
Speci ic bac e ia we e exclusi ely obse ed in he su i ing g oup:
• P o eus penne i and used an ibio ics: ampicillin 1 g (n = 2), ce iaxone 1 g (n = 1), col-
is in 1 MUI (n = 2), me openem 1000 mg (n = 2), me onidazole 5 g/200 mL (n = 1),
and ancomycin 1 g (n = 1).
• S aphylococcus wa ne i and used an ibio ics: linezolid 2 mg/mL (n = 1) and me openem
1000 mg (n = 1).
A posi i e mono onic associa ion be ween hospi aliza ion leng h and numbe o an ibi-
o ic doses used was ound in he in es iga ed coho , wi h a highe co ela ion coe icien in
deceased pa ien s (ρ = 0.6327. p < 0.0001) han in he su i ing g oup (ρ = 0.4749, p < 0.0001).
In he analyzed coho , he hospi aliza ion leng h was signi ican ly diffe en among
pa ien s wi h a diffe en numbe o collec ed biological samples ( om 0 o 5 samples, wi h
i e samples collec ed om wo pa ien s) (K uskal–Wallis es : p < 0.0001, Figu e 2). The
diffe ence emained s a is ically signi ican o deceased pa ien s (K uskal–Wallis es : p =
0.0124) only when pa ien s wi hou biological samples we e compa ed o hose wi h h ee
biological samples (pos hoc analysis, 0 s. 3: p = 0.0055). In he su i ing g oup, he num-
be o days o hospi aliza ion was also s a is ically signi ican (K uskal–Wallis es : p =
0.0001), wi h he ollowing signi ican diffe ences in pos hoc analysis: p = 0.0001 o 0 s.
4, p = 0.0028 o 1 s. 4, and p = 0.02621 o 2 s. 4.
Figu e 2. Dis ibu ion o numbe o hospi aliza ion days by numbe o biological samples (pos hoc
analysis: 0 s. 3 p = 0.0007, 0 s. 4 p < 0.0001, 1 s. 4 p = 0.0069). Do s ep esen he aw da a, he box
Figu e 2. Dis ibu ion o numbe o hospi aliza ion days by numbe o biological samples (pos hoc
analysis: 0 s. 3 p= 0.0007, 0 s. 4 p< 0.0001, 1 s. 4 p= 0.0069). Do s ep esen he aw da a, he
box middle line is he median, he boxes a e he i s , and he hi d qua ile and he wicke s a e he
minimum and maximum (excluding he ou lie s). Colo s ep esen he dis ibu ion o he leng h o
hospi al s ay o each numbe o biological samples.
S a is ically signi ican di e ences in hospi aliza ion leng h o di e en numbe s o
bac e ia iden i ied in any biological sample we e obse ed only in he su i ed g oup
(K uskal–Wallis es : p= 0.0046, pos hoc analysis: 0 (n = 54) s. 3 (n = 3), p= 0.0401)
(Figu e 3).
S a is ically signi ican di e ences we e obse ed be ween an ibio ic doses o di e en
numbe s o bac e ia iden i ied in any biological sample only in su i ed pa ien s (K uskal–
Wallis es : p= 0.0023, pos hoc analysis: 0 (n = 54) s. 2 (n = 3), p= 0.0114) (Figu e 4b).
An ibio ics 2025,14, 64 16 o 18
o Fishe ’s exac es acco ding o he expec ed equencies o he a ibu e da a. The Mann–
Whi ney U es o K uskal–Wallis es was used o compa e quan i a i e da a be ween
wo o mo e g oups. Whene e he K uskal–Wallis es showed s a is ically signi ican
di e ences be ween g oups, a pos hoc analysis was conduc ed. The Kendall au co ela ion
coe icien was calcula ed o quan i y he associa ion be ween he numbe o iden i ied
bac e ia and biological samples.
Bac e ial cul u es we e pe o med using di e en biological samples (e.g., cannula,
ce eb ospinal luid, blood, u ine, b onchial sec e ion, and pu ulen / luid sec e ion). In
some cases, mo e han one biological sample was collec ed om he same. In addi ion, mo e
han one bac e ium was iden i ied in biological samples om he same pa ien . An ibio ic
suscep ibili y es s we e pe o med o any bac e ia iden i ied in he biological samples.
The e o e, he o al numbe o iden i ied bac e ia was highe han ha o pa ien s in he
analyzed coho .
Explo a o y s a is ical analysis was conduc ed using S a is ica so wa e ( .13.5, TIBCO
So wa e Inc., Palo Al o, CA, USA). G aphical ep esen a ions we e c ea ed using Mic oso
Excel (Mic oso O ice 365, USA) o JASP ( . 0.18.3.0). All es s we e wo- ailed a a
signi icance le el o 5%, and p- alues less han 0.05 we e conside ed s a is ically signi ican .
5. Conclusions and Fu u e T ends
In ec ion wi h K. pneumoniae was obse ed in he coho , ega dless o he g oup, and
wi h A. baumannii and P. ae uginosa among deceased pa ien s, and E. coli,S. hemoly icus,
and E. aecalis among discha ged pa ien s. The deceased g oup was olde and had a longe
hospi aliza ion s ay, highe bac e ial load, numbe o an ibio ics used, and highe o al
an ibio ic doses adminis e ed. Bac e ia wi h he highes le els o esis ance o an ibio ics
iden i ied in his coho we e K. pneumoniae,S. hemoly icus, and A. baumannii. Ou esul s
highligh ed he main challenges eco ded in one ICU o a clinical hospi al in Romania in
e ms o HAIs, iden i ied bac e ia, and he consump ion o an ibio ics. Ou esul s could be
used o de elop guidelines o heal hca e p o essionals and suppo measu es o mo e
judicious use o an ibio ics. Rapid de ec ion me hods o bac e ia, as well as ca e ul and
con inuous an ibio ic su eillance, no only in he ICU, a e needed o guide heal hca e
wo ke s o p o ide he bes pa ien ca e.
Au ho Con ibu ions: Concep ualiza ion, C.C., S.S. and B.F.; me hodology, S.S., A.M., A.-E.D.,
S.L.C. and S.D.B. alida ion, S.S., B.F. and S.D.B.; o mal analysis, S.S., A.M., A.-E.D. and S.L.C.;
in es iga ion, S.S., A.-E.D. and S.L.C.; esou ces, C.C.; da a cu a ion, S.S. and B.F.; w i ing—o iginal
d a p epa a ion, S.S., B.F., C.C. and S.D.B.; w i ing— e iew and edi ing, C.C. and S.D.B.; supe ision,
C.C. and S.D.B.; p ojec adminis a ion, C.C. unding acquisi ion, C.C. All au ho s ha e ead and
ag eed o he published e sion o he manusc ip .
Funding: This wo k was suppo ed by he Eu opean Union’s Ho izon Eu ope esea ch and inno a ion
p og am unde he g an ag eemen “Eu opean in eg a ion o new echnologies and social-economic
solu ions o inc easing consume us and engagemen in sea ood p oduc s (FishEuT us ), G an
Ag eemen : 101060712/2022.
Ins i u ional Re iew Boa d S a emen : The s udy was conduc ed in acco dance wi h he Decla a ion
o Helsinki and app o ed by he E hics Commi ee o “Cons an in Papilian” Mili a y Eme gency
Hospi al (p o ocol code A5987/04.10.2022) o s udies in ol ing humans.
In o med Consen S a emen : Pa ien consen was wai ed by he e hics commi ee due o he
e ospec i e analysis o ou inely collec ed da a.
Da a A ailabili y S a emen : Da a una ailable due o e hical es ic ions.
Con lic s o In e es : The au ho s decla e no con lic s o in e es .
An ibio ics 2025,14, 64 17 o 18
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