ORIGINAL PAPERS

Adv Clin Exp Med 2008, 17, 3, 259–268 © Copyright by Silesian Piasts
ISSN 1230−025X University of Medicine in Wrocław

BEATA KOWALSKA−KROCHMAL1, IZABELA DOLNA1, KRZYSZTOF SZUFNAROWSKI2,

EWA DWORNICZEK1, ROMAN FRANICZEK1, HANNA DASZKOWSKA3, GRAŻYNA GOŚCINIAK1,
IRENA CHOROSZY−KRÓL1

Frequency and Antibiotic Susceptibility of Enterococcal

Strains Isolated from Patients of Different Departments
of a University Teaching Hospital in Wrocław
Częstość izolacji i lekowrażliwość szczepów z rodzaju Enterococcus
pochodzących od pacjentów hospitalizowanych w klinikach
Akademickiego Szpitala Klinicznego we Wrocławiu
1
Department and Unit of Microbiology, Silesian Piasts University of Medicine in Wrocław, Poland
2
University Teaching Hospital, Hospital Infections Group, Wrocław, Poland
3
Microbiology Laboratory of the University Laboratory Diagnostic, Wrocław, Poland

Abstract
Background. Strains of Enterococcus have in recent years become one of the most frequent etiology factors in
nosocomial infections, both in children and adults. The biggest threat are the strains resistant to glycopeptide and
to high level aminoglycosides
Objectives. Estimation of frequency of isolation and drug susceptibility of enterococci obtained from differen clin−
ical samples from patients from University Teaching Hospital (UTH) in Wrocław.
Material and Methods. One thousand nine hundred thirty three (1933) strains of Enterococcus isolated from
patients from different clinic of UTH were enrolled in this study. Frequency of isolation of enteroccocci in rela−
tion to general number of strains (N = 12435) and in relation to Gram−positive bacteria (5581) collected in period
1.01.2006–28.02.2007 was determined. Susceptibility to ampicillin, doxycycline, ciprofloxacin, gentamicin, van−
comycin and teicoplanin was estimated.
Results. More than 2/3 of enterococci were isolated in pediatric wards. Highest number of strains was isolated
from children from the Department of Bone Marrow Transplantation (23.6%), from Pediatric and
Gastroenterology Hospital (20.6) and from adults from Gastroenterology Hospital (11.4%). Most frequently ente−
rococci were obtained from stool and urine. Twenty strains were isolated from blood, 5 from cerebrospinal fluid
and 11 strains from other physiological sterile fluids. Fiftheen strains were resistant to vancomicin, all of which
belonged to the species E. faecium and were obtained from nephrology department patients (1 child and 14 adults).
The percentage of HLGR strains reached 23,6% in the E. faecalis group and 40.3% in E. faecium group. E. fae−
calis strains were more susceptible to to ampicillin (97,3% i 3,4% respectively) and less susceptible to doxycycline
(28.0% i 67.6% respectively).
Conclusions. Isolation of VRE strains from Nefrological Departments suggest necessity monitoring of glycopep−
tide susceptibility among strains obtained as from urine as other clinical samples especially from stool (VRE col−
onization) (Adv Clin Exp Med 2008, 17, 3, 259–268).
Key words: Enterococcus, frequency of isolation, antibiotic susceptibility.

Streszczenie
Wprowadzenie. Szczepy z rodzaju Enterococcus w ostatnich latach stały się jednym z najczęstszych czynników
etiologicznych zakażeń szpitalnych, zarówno u dzieci, jak i dorosłych. Największym zagrożeniem stają się szcze−
py oporne na glikopeptydy oraz duże stężenia aminoglikozydów.
Cel pracy. Ocena częstości izolacji i lekowrażliwości enterokoków pochodzących z różnych próbek klinicznych
od pacjentów z klinik Akademickiego Szpitala Klinicznego (ASK) we Wrocławiu.
Materiał i metody. Analizie poddano 1933 szczepy z rodzaju Enterococcus wyizolowane od pacjentów z różnych
klinik ASK. Oceniono częstość izolacji enterokoków zarówno w odniesieniu do ogólnej puli szczepów (12435),
260 B. KOWALSKA−KROCHMAL et al.

jak i do Gram−dodatnich bakterii (5581) wyosobnionych od pacjentów w okresie od 1.01.2006 do 28.02.2007 r.

Oceniono wrażliwość na ampicylinę, doksycyklinę, ciprofloksacynę, gentamycynę, wankomycynę i teikoplaninę.
Wyniki. Ponad 2/3 enterokoków pochodziło z oddziałów pediatrycznych. Najwięcej szczepów wyizolowano z Od−
działu Przeszczepów Szpiku (23,4%) i z Kliniki Pediatrii i Gastroenterologii (20,6%) oraz od dorosłych z Kliniki
Gastroenterologii (11,4%). Enterokoki były najczęściej wyosobniane z kału i moczu. Dwadzieścia wyizolowano
z krwi, 5 z płynu mózgowo−rdzeniowego i 11 z innych fizjologicznie jałowych płynów. Piętnaście szczepów by−
ło opornych na wankomycynę, wszystkie należały do gatunku E. faecium, wyizolowanych od 14 dorosłych
i 1 dziecka z oddziałów nefrologicznych. Odsetek szczepów HLGR wynosił 23,6% wśród E. faecalis i 40,3%
wśród E. faecium. Szczepy E. faecalis były bardziej niż E. faecium wrażliwe na ampicylinę (odpowiednio 97,3
i 3,4%) i ciprofloksacynę (49,5 i 11,3%), a mniej wrażliwe na doksycyklinę (odpowiednio 28,0 i 67,6%).
Wnioski. Izolacja szczepów bakterii z rodzaju Enterococcus opornych na wankomycynę VRE z oddziałów nefro−
logii sugeruje konieczność stałego monitorowania wrażliwości na glikopeptydy zarówno enterokoków izolowa−
nych z moczu, jak i z innych materiałów, zwłaszcza z kału (kolonizacja szczepami VRE) (Adv Clin Exp Med
2008, 17, 3, 259–268).
Słowa kluczowe: Enterococcus, częstość izolacji, antybiotykowrażliwość.

Bacteria of the genus Enterococcus have in
recent years become one of the most frequent eti−
ological factors in nosocomial infections, both in
adults and children. Among the reasons for the
increased role of enterococci in infections can be
the misuse and irrational use of wide−spectrum
antibiotics, especially cephalosporins, as well as
the widespread use of invasive medical proce−
dures. The above practices lead to the selection of
multi−resistant strains, posing a serious therapeutic
problem. The largest threat are strains resistant to
glycopeptides (mainly vancomycin, i.e. VRE
strains), antibiotics which are the drugs of choice
in serious infections caused by multi−resistant
Gram−positive cocci. The increasingly frequent
occurrence of high−level aminoglycoside−resistant
(HLAR) strains among pathogenic enterococci
makes standard therapy with these antibiotics in
combination with β−lactams impossible.
Material and Methods
Evaluated were the frequency of occurrence
and drug susceptibility of enterococci isolated
between Jan. 1, 2006, and Feb. 28, 2007, from
patients of the departments of the University
Teaching Hospital (UTH) in Wrocław, including
the following pediatric hospitals: Bone Marrow
Transplantation Hospital; Pediatric Oncology and
Hematology Hospital (Hematology (Hem.) and
Transplantation (Transp.) departments); Pediatric
Nephrology (Ped. Nephr.) Hospital; Pediatric
Surgery and Urology Hospital (Ped. Surg.);
Pediatric, Gastroenterology, and Nutrition
Hospital (Ped. Gastr.); Department of Intensive
Pediatric Therapy and Anesthesiology (IPTA);
Pediatrics and Infectious Diseases Hospital (Ped.
Inf.); Pediatrics, Cardiology, and Allergology
Hospital (Ped. Allerg.); and the Neonatology
Hospital (Neonat.), and the following hospitals for
adult patients: Angiology, Arterial Hypertension,
and Diabetology (Ang); Nephrology and Trans−
plantation Medicine Hospital (Nephr.); Vascular
Surgery, General Surgery, and Transplantation
Surgery Hospital and General, Gastroentero−
logical, and Endocrinological Surgery Hospital
(Surg.); Alimentary Tract and General Surgery
Hospital (Alim. Tract Surg.); Trauma and Hand
Surgery Hospital (Trauma Surg.); Gynecology,
Reproduction, and Obstetrics Hospital (Gyn.);
Gastrology and Hepatology Hospital (Gastr.); and
the Internal and Allergic Diseases Hospital (Int.−
Allerg.). Bacteriological tests, including the isola−
tion, identification, and assessment of bacterial
susceptibility to antibiotics, were performed using
routine methods at the Microbiology Laboratory
of the University Laboratory Diagnostic Center of
Silesian Piasts University of Medicine in
Wrocław. Resistance to vancomycin was con−
firmed at the Department of Microbiology of
Silesian Piasts University of Medicine in Wrocław
using the agar dilution method (in line with CLSI
guidelines) [1].
Results
The frequencies of the enterococcal strains
isolated from different clinical material obtained
from patients treated in the hospitals and depart−
ments between Jan. 1, 2006, and Feb. 28, 2007, are
presented in Tables 1 and 2. During this time, 1993
enterococcal strains were isolated, which consti−
tuted 15.5% of the total number of bacterial strains
isolated (N = 12435) and 34.6% of the Gram−pos−
itive bacteria (N = 5581). More than 2/3 of the
fecal streptococci were isolated in pediatric wards
(71.3%, 1378 strains), representing 17.0% of the
total number of isolates (N = 8105) and 32.9% of
the Gram−positive bacteria (N = 4189) isolated
from children at the UTH. Enterococcal strains
Frequency and Antibiotic Susceptibility of Enterococcal Strains 261

Table 1. Frequency of isolation of enterococci obtained from patients from Wrocław University Teaching Hospital
Tabela 1. Częstość izolacji enterokoków pochodzących od pacjentów z Akademickiego Szpitala Klinicznego we Wrocławiu

Clinics Total Entero− Total Entero− Total E. faecalis E. faecium Other E.

(Kliniki) number coccus number coccus number % % (Inne E.)
(Ogólna % (Ogólna % (Ogólna %
liczba) liczba) liczba)
Gram (+) Gram (+) Entero−
i Gram (–) coccus (E)
Pediatrics
(Dziecięce)
Ped. Nephr. 533 16.9 196 45.9 90 90 6.7 3.3
Ped. Inf. 352 15.9 163 34.4 56 82.2 17.8 0
Hem. 612 14.9 317 28.7 91 61.5 38.5 0
Transp. 2229 23.4 1583 33 522 29.9 69.9 0.2
Neonat. 1132 8.4 565 16.8 95 75.8 24.2 0
IPTA 631 8.4 315 16.8 53 69.8 28.3 1.9
Ped. Gastr. 1814 20.6 602 62.1 374 94.9 2.1 3
Ped. Allerg. 601 13.3 354 22.6 80 95 3.8 1.2
Ped. Surg. 201 8.4 94 8.1 17 76.5 23.5 0
Total 8105 17 4189 32.9 1378 64.7 34 1.3
(Razem)
Adults
(Dorosłych)
Ang. 219 7.3 89 25.8 23 95.7 0 4.3
Surg. 513 8.8 180 35 63 76.2 22.2 1.6
Gastr. 361 11.4 89 65.2 58 87.9 12.1 0
Int.−Allerg. 440 4.7 198 14.1 28 85.8 7.1 7.1
Alim.−Tract.Surg. 111 10.8 52 30.8 16 31.2 68.8 0
Trauma. Surg. 81 8 48 20.8 10 70 20 10
Nephr. 2092 6.7 562 47.2 265 64.9 32.1 3.2
Gyn. 513 8.3 263 35 92 98.9 1.1 0
Total 4330 12.8 1392 39.9 555 75.7 22 2.3
(Razem)
Together pediatrics 12435 15.5 5581 34.6 1933 67.9 30.6 1.5
and adults clinics
(Razem dziecięce
i dorosłych)

IPTA – Department of Intensive Pediatric Therapy and Anaesthesiology.

IPTA – Oddział Intensywnej Terapii Dziecięcej i Anestezjologii.

isolated from adult patients (28.7%, n = 555) rep−
resented 12.8% of the total number of strains
(N = 4330) and 39.9% of the Gram−positive bacte−
ria (N = 1392).
The frequency of isolation of enterococci in
the individual hospitals and departments was
assessed both in relation to the general number of
strains and to the number of Gram−positive bacte−
ria isolated from patients of the individual wards.
Considering the general number of isolates, the
highest number of enterococci was isolated from
children from the Department of Transplants and
from the Pediatric and Gastroenterology Hospital,
where they represented 23.4 and 20.6%, respec−
tively, of the total number of isolated strains, and
from adult patients of the Gastroenterology
Hospital and the Alimentary Tract Surgery
Hospital, representing 11.4 and 10.8%, respective−
ly, of the total number of strains. However, when
only Gram−positive bacteria are considered, fecal
streptococci constituted more than 60% of all the
strains isolated at the Gastroenterology Hospital
and at the Pediatric and Gastroenterology
Hospital, slightly less than 50% at the Nephrology
and Pediatric Nephrology Hospital, and only 8%
at the Pediatric Surgery Hospital and 14% at the
Internal and Allergic Diseases Hospital.
E. faecalis strains (N = 1312) prevailed
(67.9%) among the fecal streptococci isolated
from UTH patients. Strains isolated from children
(N = 892) constituted 64.7% of all enterococci iso−
lated at pediatric hospitals and were isolated most
frequently from feces (n = 405, 45.4%) and urine
(n = 376, 42.2%). Fecal strains represented more
 Table 2. Frequency of isolation of enterococci from different clinical samples
Tabela 2. Częstość izolacji enterokoków z różnych próbek klinicznych

Clinics
Clinics Enterococcus faecalis Enterococcus faecium
(Kliniki)
(Kliniki)
N urine stool wound blood, CFS from RTI other** N urine stool wound blood, CFS from RTI other**
262

(mocz) (kał) pus and and other (próbki (inne) (mocz) (kał) pus and and other (próbki (inne)
swabs fluids* z dróg swabs fluids* z dróg
(ropa (krew, PMR oddech.) (ropa (krew, PMR oddech.)
i wym. i inne i wym. i inne
z ran) płyny) z ran) płyny)
n % n % n % n % n % n % n % n % n % n % n % n %
Pediatric
Pediatric
(Dziecię−
(Dziecię−
ce (1))
ce (1))
Ped. Nephr.
Ped.Nephr 81 77 95.1 2 2.5 1 1.2 0 0 1 1.2 0 0 6 5 83.3 1 16.7 0 0 0 0 0 0 0 0
Ped.Inf.
Ped.Inf. 46 3 6.5 40 87.2 0 0 0 0 2 4.3 1 2.2 10 0 0 10 100 0 0 0 0 0 0 0 0
HEM.
HEM. 56 10 17.9 31 55.5 1 1.8 4 7.2 4 7.2 6 10.1 35 0 0 28 80 0 0 1 2.9 0 0 6 17.1
Transp.
Transp. 156 22 14.1 80 51.3 1 0.6 3 1.9 16 10.3 34 21.8 365 25 6.8 231 63.3 0 0 2 0.5 33 9.1 74 20.3
Neonat.
Neonat. 72 29 40.2 30 41.7 1 1.4 5 6.9 3 4.2 4 5.6 23 2 8.7 13 56.5 0 0 3 13 4 17.5 1 4.3
IPTA
IPTA 37 4 10.8 28 75.7 0 0 1 2.7 3 8.1 1 2.7 15 0 0 8 53.3 1 6.7 2 13.3 3 20 1 6.7
Ped. Gastr.
Ped.Gastr. 355 164 46.2 183 51.5 2 0.6 0 0 0 0 6 1.7 8 5 62.5 3 37.5 0 0 0 0 0 0 0 0
Ped. Allerg.
Ped.Allerg. 76 66 86.9 9 11.8 0 0 0 0 0 0 1 1.3 3 2 66.7 1 33.3 0 0 0 0 0 0 0 0
Ped. Surg.
Ped.Surg. 13 1 7.7 2 15.4 6 46.2 3 23 0 0 1 7.7 4 1 25 0 0 0 0 2 50 0 0 1 25
TotalTotal 892 376 42.2 405 45.4 12 1.3 16 1.8 29 3.2 54 6.1 469 40 8.5 295 62.9 1 0.2 10 2.1 40 8.5 83 17.8
(Razem)
(Razem)
Adults
Adults
(Doro−
(Doro−
słychs¦ych
(2))(2))
Ang
Ang. 22 2 9.1 1 4.5 19 86.4 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0 0
Surg.
Surg. 48 2 4.2 1 2.1 17 35.4 6 12.5 0 0 22 45.8 14 2 14.2 0 0 9 64.3 1 7.1 0 0 2 14.3
Gastr
Gastr. 51 3 5.9 33 64.7 3 5.9 0 0 0 0 12 23.5 7 0 0 3 42.3 2 28.3 0 0 0 0 2 28.3
Int.−Allerg. 24
Int.−Allerg. 7 29.2 11 45.8 0 0 0 0 4 16.6 2 8.3 2 2 100 0 0 0 0 0 0 0 0 0 0
Alim.
Alim. 5 1 20 0 0 3 60 0 0 0 0 1 20 11 1 9.1 0 0 1 9.1 0 0 2 18.2 7 63.6
Tract. Surg.
Tract.Surg.
Trauma.
Trauma.
Surg.
Surg. 7 0 0 0 0 7 100 0 0 0 0 0 0 2 2 100 0 0 0 0 0 0 0 0 0 0
Nephr.
Nephr. 172 128 74.4 20 11.6 15 8.7 1 0.6 5 2.9 3 1.8 85 52 61.2 7 8.2 10 11.8 2 2.4 6 7 8 9.4
Gyn.
Gyn. 91 0 0 0 0 10 11 0 0 0 0 81 89 1 0 0 0 0 0 0 0 0 0 0 1 100
TotalTotal 420 143 34 66 15.8 74 17.6 7 1.7 9 2.1 121 28.8 122 59 48.4 10 8.2 22 18 3 2.4 8 6.6 20 16.4
(Razem)
(Razem)
Together
Together 1312 519 39.6 471 35.9 86 6.6 23 1.8 38 2.9 175 13.2 591 99 16.7 305 51.6 23 3.9 13 2.2 48 8.1 103 17.4
(Razem
(Razem
1 + 2)
1 + 2)
B. KOWALSKA−KROCHMAL et al.

* – other physiological sterille samples, ** – wymazy z pochwy i szyjki macicy; samples from vaginal wet mounts and from cervical smears.
IPTA – Department of Intensive Pediatric Therapy and Anaesthesiology. Oddział Intensywnej Terapii Dziecięcej i Anestezjologii.
N – number of E. faecalis or E. faecium isolated from particular Clinics, n – number of enterococci isolated from particular clinical samples.
Frequency and Antibiotic Susceptibility of Enterococcal Strains
than 75% of the E. faecalis isolated from children
from the Infectious Diseases Hospital (87.2%) and
the Intensive Care Unit (75.7%) and more than
50% of the strains isolated at the Hematology
(55.4%), Gastroenterology (51.5%), and
Transplantation (51.3%) wards. Urinary strains
represented 95.1% of E. faecalis isolated from
children at the Nephrology Hospital and 86.9% of
the isolates from the Allergic Diseases Hospital.
E. faecalis strains isolated from adult patients
(N = 420) constituted 75.7% of the total number of
enterococci and were most frequently isolated
from urine (n = 143, 34%) and other materials (n =
121, 28.8%). Urinary strains constituted 74.4% of
E. faecalis isolated from patients of the
Nephrology Hospital, 29.9% at the Internal
Diseases Hospital, and less than 10% at other hos−
pitals. Strains from other materials represented
89% of E. faecalis isolated from patients of the
Gynecology Hospital (mainly from vaginal wet
mounts and cervical smears). Fecal strains were
isolated mainly from patients of the
Gastroenterology Hospital and constituted 64.7%
of E. faecalis. Strains isolated from pus and wound
infections prevailed among E. faecalis isolated
from the patients of the Department of Angiology
and Surgery Departments.
E. faecium (N = 591) represented 30.6% of the
total number of strains of the genus Enterococcus
obtained from UTH patients. E. faecium strains
isolated in pediatric wards (N = 469, 34.0%) were
most frequently isolated from the feces (n = 295,
62.9%). The largest number of E. faecium were
obtained in the Transplantation Ward (365/469,
77.8%), with fecal strains representing 63.3%.
E. faecium strains isolated from adult patients
(N = 122) represented 22% of all enterococci and
were isolated most often from urine (n = 59,
48.4%) and were obtained primarily at the
Nephrology Department.
Twenty enterococci strains were isolated from
blood, including 14 E. faecalis strains and 6 E. fae−
cium strains. Twelve E. faecalis and 5 E. faecium
strains were isolated at pediatric hospitals from
young patients of the Oncology and Hematology
Department (4 E. faecalis and 1 E. faecium),
Transplantation Department (3 and 2, respective−
ly), and the Neonatology Hospital (5 and 2). As for
adult patients, only 3 strains were isolated from
blood (and all at surgical hospitals), including
2 E. faecalis strains and 1 E. faecium strain.
Five enterococci strains were isolated from the
cerebrospinal fluid, all from children, including
3 strains isolated at the Pediatric Surgery
Department (2 E. faecalis and 1 E. faecium) and
2 E. faecium strains each isolated at the ICU and at
the Neonatology Hospital. Enterococci were also
263
isolated from the fluids from body cavities, with
11 strains in total, including 4 from children, i.e.
2 from the Surgery Department (1 E. faecalis and
1 E. faecium) and 2 from the ICU (1 E. faecalis
and 1 E. faecium), and 7 from adult patients, i.e.
4 E. faecalis strains from the Vascular Surgery
Department and 3 strains from the Nephrology
Department (2 E. faecium and 1 E. faecalis).
Drug Susceptibility
Among the strains of the genus Enterococcus
isolated from patients treated at the UTH, 15 van−
comycin−resistant strains were found, all of which
belonged to the species E. faecium obtained from
nephrology department patients, including 1 obtai−
ned from a child and the remaining ones from
adults (Fig. 1). In the E. faecalis group, the per−
centage of high−level gentamycin resistant
(HLGR) strains reached 23.6%, while in the
E. faecium group it stood at 40.3%. E. faecalis
strains were more susceptible to ampicillin than
were E. faecium strains (97.3% and 3.4%, respec−
tively) and ciprofloxacin (49.5% and 11.3%) and
less susceptible to doxycycline (28.0% and 67.6%,
respectively).
Comparison of the susceptibility of enterococ−
ci isolated from children and from adults shows
that in the E. faecalis strain group (Fig. 2) no sig−
nificant susceptibility differences were found,
while in the E. faecium group (Fig. 3) a much
higher percentage of the strains isolated from
adults (19.4% and 0.5%, respectively) was resis−
tant to vancomycin; in this group of bacteria,
HLAR strains were more frequently isolated from
children (55.3% vs. 22.2%).
An analysis of the drug susceptibility of the
enterococcal strains isolated at individual hospitals
and departments was performed. Because of the
small numbers of strains from the individual hos−
pitals for which drug susceptibility analysis was
conducted, data from three hospitals were taken
for the comparative study, including the
Nephrology and Gynecology Hospital for adults
and the Department of Transplantation of the pedi−
atric hospitals. In comparison with the strains iso−
lated from patients of the nephrology and bone
marrow transplantation departments (MT), E. fae−
calis strains (Fig. 4) isolated from patients from
the gynecology departments were more suscepti−
ble both to ciprofloxacin (62.1, 42.7, and 38.7%,
respectively) and to doxycycline (45, 24%, no
analysis was performed for MT). A smaller per−
centage of HLGR strains was also found (12.5,
25.3%, and 28.6%, respectively). Of the E. faeci−
um strains (Fig. 5) isolated from the nephrology
department patients, 28.6% were vancomycin
264 B. KOWALSKA−KROCHMAL et al.

% susceptibility
E. faecalis – Paediatric Clinics
% wra¿liwoœci
kliniki dzieciêce
100 E. faecalis – Clinic of Adults
% susceptibility kliniki doros³ych
E. faecalis % wra¿liwoœci
90
E. faecium 100
80

70 80

60

50 60

40
40
30

20
20

10

0 0
ampicillin gentamicin 120 vancomycin ampicillin gentamicin 120 vancomycin
ampicylina gentamycyna 120 wankomycyna ampicylina gentamycyna 120 wankomycyna
doxycycline ciprofloxacin teikoplanin doxycycline ciprofloxacin teikoplanin
doksycyklina ciprofloksacyna teikoplanina doksycyklina ciprofloksacyna teikoplanina

Fig. 1. Comparison of drug susceptibility (%) of total
isolated strains of Enterococcus faecalis and Entero−
coccus faecium (University Teaching Hospital in Wro−
cław, 1.01.2006–28.02.2007)
Ryc. 1. Porównanie lekoowrażliwości (%) ogólnej
liczby szczepów Enterococcus (E.) faecalis i Entero−
coccus (E.) faecium (Akademicki Szpital Kliniczny,
Wrocław, 1.01.2006–28.02.2007 r.)
Fig. 2. Comparison of drug susceptibility (%) of E. fa−
ecalis isolated from children and adults hospitalized at
the University Teaching Hospital in Wrocław,
1.01.2006–28.02.2007
Ryc. 2. Porównanie lekowrażliwości (%) szczepów
Enterococcus faecalis izolowanych od dzieci i od do−
rosłych hospitalizowanych w Akademickim Szpitalu
Klinicznym we Wrocławiu (1.01.2006–28.02.2007 r.)

resistant (MIC ≥ 128 µg/ml) and only 2.2% were

HLGR strains, while no strains isolated at the bone
E. faecium – Paediatric Clinics
marrow transplantation department were resistant kliniki dzieciêce
E. faecium – Clinic of Adults
to vancomycin, but the percentage of HLGR stood % susceptibility kliniki doros³ych
% wra¿liwoœci
at a high 52.1%. 100

Discussion 80

This study of epidemiological data from hos− 60

pitals and departments of the University Teaching

Hospital in Wrocław conducted from Jan. 1, 2006, 40

to Feb. 28, 2007, showed that fecal enterococci

represented 15.5% of the total number of isolated 20
bacterial strains and 34.6% of the Gram−positive
bacteria. In a study conducted in Greece in the last 0
years of the 20th century (quoted in [2]), ampicillin
ampicylina
gentamicin 120
gentamycyna 120
vancomycin
wankomycyna
doxycycline ciprofloxacin teikoplanin
Enterococcus strains constituted 7.1% of all isolat− doksycyklina ciprofloksacyna teikoplanina

ed bacteria and 23.9% of Gram−positive bacteria.
Reports from Slovakia [3] show as much as 40.2%
of enterococcal infections among newborns in
1999–2000, while according to Czech data, ente−
rococci were responsible for 13% of infections of
diabetics in December 1998 to December 1999
[4]. The last two reports concerning the two south−
ern neighbors of Poland confirm that small chil−
dren, especially newborns and diabetics, are prone
to infections, including enterococcal infections.
Infections with fecal enterococci are also frequent
in ICUs; in a study conducted in 2000 in Great
Britain [5] they represented 14.3% of all infections
caused by Gram−positive bacteria. The analysis of
Fig. 3. Comparison of drug susceptibility (%) of E. fa−
ecium isolated from children and adults hospitalized at
the University Teaching Hospital in Wrocław,
1.01.2006–28.02.2007
Ryc. 3. Porównanie lekowrażliwości (%) szczepów
Enterococcus faecium izolowanych od dzieci i od do−
rosłych hospitalizowanych w Akademickim Szpitalu
Klinicznym we Wrocławiu (1.01.2006–28.02.2007 r.)
data gathered at the UTH shows that the entero−
cocci strains isolated from children hospitalized at
the Transplantation Department and at gastroen−
terology hospitals were isolated mainly from
Frequency and Antibiotic Susceptibility of Enterococcal Strains 265

Gynaecology
Oddzia³ Ginekologiczny feces. It is common knowledge that these microor−
Adults Nephrology
Oddzia³ Nefrologiczny
ganisms constitute the normal flora of the alimen−
% susceptibility Children Bone Marrow tary tract, but their presence in patients with
% wra¿liwoœci Dzieciêcy Oddzia³ Przeszczepu Szpiku
impaired immunity may have clinical significance,
100
especially regarding multi−resistant strains
90
(including VRE). The possibility to identify such
80 strains during long−term treatment with antibi−
70
otics, especially in immunosuppressed patients,
and the translocation of the enterococci to other
60
systems and organs facilitated by invasive medical
50 procedures indicate the need for routine monitor−
40 ing of drug susceptibility of the such fecal isolates.
30
According to reports from around the world,
E. faecalis strains prevailed among isolated fecal
20
enterococci and constituted 56–90% of all entero−
10 cocci [5–10]. E. faecium strains were isolated less
0
frequently (5.2–27.6%), and the remaining
ampicillin
ampicylina
gentamicin 120
gentamycyna 120
vancomycin
wankomycyna
Enterococcus species represented 2.9–25%. The
doxycycline
doksycyklina
ciprofloxacin
ciprofloksacyna
teikoplanin
teikoplanina
analyzed material showed that E. faecalis repre−
sented 67.9% of all fecal enterococci isolated,
Fig. 4. Comparison of drug susceptibility (%) E. faecalis E. faecium 30.6%, and the remaining species
isolated from children from the department of Bone
1.5%. The SENTRY Antimicrobial Surveillance
Marrow Transplantation and from adults in the Gyneco−
logy and Nephrology Hospitals (1.01.2006–28.02.2007) Program [9] covering the period 1997–2000
showed geographical differences in the frequency
Ryc. 4. Porównanie lekowrażliwości (%) szczepów En− of isolation of individual Enterococcus species: in
terococcus faecalis izolowanych od dzieci z Oddziału
Przeszczepów Szpiku i od dorosłych z Kliniki Gineko−
Europe, E. faecalis constituted 67%, in
logii i Kliniki Nefrologii (1.01.2006–28.02.2007 r.) Asia–Pacific 76%, in Latin America 76%, and in
North America 56%; E. faecium constituted,
respectively, 17, 15, 5, and 19%, while the remain−
Adults Nephrology ing species were 16, 9, 19, and 25%, respectively.
Oddzia³ Nefrologiczny
% susceptibility Children Bone Marrow In the present study the frequency of isolation of
% wra¿liwoœci Dzieciêcy Oddzia³ Przeszczepu Szpiku
E. faecalis was close to the above European data,
100
and deviations concerned E. faecium and the
90
remaining species. Data from some European
80 countries, such as Greece [2], Great Britain [5],
70 Turkey [7], and Croatia [6], published in
60
2000–2005 included a larger percentage share of
E. faecalis in enterococcal infections (from 72.4%
50
in Greece to 83.7–90.2% in Croatia). In similar
40 data from Cuba [10] published in 2005 the fre−
30 quency of isolation of E. faecalis reached 85%.
20
In the present study concerning isolates from
the UTH, E. faecium strains which are more resis−
10
tant to antibiotics than E. faecalis represented as
0
ampicillin gentamicin 120 vancomycin
much as 30.6% of the total number of enterococci,
ampicylina
doxycycline
gentamycyna 120
ciprofloxacin
wankomycyna
teikoplanin
while data from literature sources indicate that the
doksycyklina ciprofloksacyna teikoplanina
percentage share of this species in other countries,
Fig. 5. Comparison of drug susceptibility (%) E. fae− not only in Europe, but in the rest of the world,
cium isolated from children from the department of was lower, and only in some countries exceeded
Bone Marrow Transplantation and from adults in 20% (Greece 27.6% [2], 24.5% Great Britain [5],
the Nephrology Hospital (1.01.2006–28.02.2007) and Lebanon 22.9% [11]), while in Latin America
Ryc. 5. Porównanie lekowrażliwości (%) szczepów [8–10] and in Turkey [7] it did not exceed 10%.
Enterococcus faecium izolowanych od dzieci z Od− What is interesting is the significant percentage
działu Przeszczepów Szpiku i od dorosłych z Kliniki share of other enterococcal species observed espe−
Nefrologii (1.01.2006–28.02.2007 r.) cially in North America (25%) [9] and Latin
America (ca. 19%) [9, 10], except for Cuba (5%)
[10]. In the present study, the share of
266
Enterococcus strains reached only 1.5%, while
other Polish data from 1996 collected at four hos−
pitals [12] showed a twice higher frequency of iso−
lation of Enterococcus spp.
The pathogenic properties of fecal enterococci
are confirmed by the presence of the above
microorganisms in such materials as urine, blood,
and wound exudate. As confirmed by literature
sources, Enterococcus species are most frequently
isolated from patients with urinary tract infections.
Multicenter studies carried out in Poland and cov−
ering the period 1998–1999 [13] indicate that ente−
rococci were the dominant urinary tract pathogen
among Gram−positive cocci isolated from hospi−
talized patients. The present study showed that in
the E. faecalis group, strains isolated from urine
represented 39.6% and in the E. faecium group
16.7%, and only 8.5% of E. faecalis isolated from
children was derived from urine in comparison
with as much as 48.4% of E. faecalis isolated from
adult patients. Other authors confirm the role of
enterococcal bacteria as urinary tract pathogens. In
a study carried out in Turkey [7], enterococci iso−
lated from urine constituted 70% of the total num−
ber of enterococci, in Croatia 52.7% [6], and in
Mexico [8] and Cuba [10] more than 30%.
In total, strains isolated from blood, cere−
brospinal fluid, and other body fluids constituted
1.9% of the analyzed material (blood 1.0%, cere−
brospinal fluid 0.3%, and other fluids 0.6%).
Strains isolated from pus represented 6.0% and
from the respiratory tract 4.5%. According to other
authors, of the total number of isolated enterococ−
ci, strains isolated from blood represented 3.1% in
Croatia [6], 7.2% in Poland [12], and 11.8% in the
pediatric hospital in Mexico [8].
According to a study performed in
Washington, USA, concerning nosocomial entero−
coccal infections in children, septicemia was diag−
nosed in 62% of the patients and CNS inflamma−
tion in 1%. In the above study the authors indicat−
ed that the factors contributing to nosocomial
enterococcal infections are the presence of central
catheters, mechanical ventilation, pathological
changes, procedures within the alimentary tract, as
well as long−term antibacterial treatment, especial−
ly with such antibiotics as ampicillin, cefotaxim,
ceftazidime, clindamycin, gentamycin, or van−
comycin.
Enterococci, which have a natural resistance
to cephalosporins, low concentrations of amino−
glycosides, licosamides, and cotrimoxazole, are
characterized by variable susceptibility to
aminopenicillin antibiotics, tetracyclines, fluoro−
quinolones, glycopeptides, and high concentra−
tions of aminoglycosides. The drug susceptibility
of individual strains varies depending on the genus
B. KOWALSKA−KROCHMAL et al.
and origin of the strain (outpatients/inpatients,
patients from various hospital wards). The present
study showed that 15 (3.8%) of the studied strains
were resistant to vancomycin, while retaining their
sensitivity to teicoplanin. All VRE strains
belonged to the species E. faecium. Multicenter
studies covering Europe, Asia−Pacific, Latin
America, and North America [9] showed that in
2000 the highest percentage of glycopeptide−resis−
tant enterococci (GRE) was observed in North
America (12% VAR, 10% TPR) and the lowest in
Asia (both 1%), while in Europe, 2% of the strains
were found to be resistant to vancomycin and 1%
to teicoplanin. The present study as well as those
by other authors show that GRE strains were
found mainly in the E. faecium group; in the
United States the percentage of these strains
reached as much as 50% [9] and in some European
countries it ranged from 3.1% in France [14] to
18% in Great Britain [5], while in Cuba it was
10% [10]. The available data indicate that both in
European countries such as Great Britain [15],
Germany [16], Belgium [17], and Poland (data
from 2003–2005 in [18]) and in the United States
[9] and Argentina [19], Van A strains were domi−
nant (resistant both to vancomycin and
teicoplanin), while in the present study, van−
comycin−resistant strains were susceptible to
teicoplanin, which excludes the above resistance
phenotype. Interesting data on VRE colonization
in pediatric wards were presented by Gray and
George from Birmingham [15], who observed col−
onization by the above strains in 38.3% of children
from the hematology and oncology ward and only
2.3% of the pediatric patients from the ICU.
Reports from Belgium [17] show that GRE strains
were not characterized by high resistance to gen−
tamycin, and only 23% of them were HLSR.
Nearly 70% of the VRE strains isolated from pedi−
atric patients at the hospital in Birmingham [15]
were susceptible to tetracycline and ciprofloxacin,
although both of these antibiotics are not recom−
mended for children.
The analysis of the drug susceptibility of ente−
rococci isolated from UTH patients shows signifi−
cant differences in the susceptibilities of E. fae−
calis and E. faecium strains. Most of the E. fae−
calis strains were susceptible to ampicillin (98%
of the strains isolated from children and 96.6%
from adults). Around half of the strains were sus−
ceptible to fluoroquinolons (52.3 and 48.0%) and
much less to doxycycline (30.4 and 17.4%). The
percentage of HLGR strains was 23 and 24.1%.
Studies by other authors indicate total susceptibil−
ity [5, 10, 12, 13, 20] or slight resistance to ampi−
cillin [2, 6, 7, 11, 21] and varied susceptibility to
ciprofloxacin (14–18.5% in Croatia [6], 56% in
Frequency and Antibiotic Susceptibility of Enterococcal Strains 267

Italy [21], and 82% in the Netherlands [20]), and
to tetracycline (67% in Italy [21], 78% in the
Netherlands [20]). The percentage of HLGR
strains ranged from 11.5% in outpatients to 37% in
inpatients in Croatia [3], 15% in Italy [10], and as
much as 40% of ICU strains in Great Britain [5].
The majority of E. faecium strains isolated from
UTH patients were resistant to ampicillin (the per−
centage of sensitive strains isolated from children
was as small as 3.2% and for adults the percentage
was 3.7%) and fluoroquinolons (14.8 and 7.9%,
respectively), but a large number of them were sus−
ceptible to doxycycline (71.4 and 66.7%). The per−
centage of HLGR strains was 55.3 and 22.2%,
respectively. Studies by other authors show either
total resistance of E. faecium strains to ampicillin
[7, 12], small susceptibility (4%) in Great Britain
[5], and greater susceptibility (24%) in Greece [2].
The percentage of strains susceptible to fluoro−
quinolons presented in available literature was also
very diversified and ranged from 13.3% in Poland
in 1996 [12] and 15.5% in Italy in 1997–1999 [21]
to 70–80% in Cuba in 2001 [10], while the percent−
age of strains susceptible to tetracycline was similar
to or lower than the results of the present study and
ranged from 45 in Japan [22] to 60% in Italy [21]
and Lebanon [11], while in Cuba it was as low as
10% [10]. The share of HLGR strains among E. fae−
cium was diversified and ranged from 10–15% in
Italy [21] to 88% in Turkey [7].

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Address for correspondence:

Beata Kowalska−Krochmal
Department and Unit of Microbiology
Silesian Piasts University of Medicine
Chałubińskiego 4
50−367 Wrocław
Poland

Conflict of interest: None declared

Received: 4.02.2008
Revised: 31.03.2008
Accepted: 29.05.2008