Hospital-acquired infections due to multidrug-resistant
organisms in Hungary, 2005-2010
S Caini (email@example.com)1,2, A Hajdu1, A Kurcz1, K Böröcz1
1. National Center for Epidemiology (NCE), Budapest, Hungary
2. European Programme for Intervention Epidemiology Training (EPIET), European Centre for Disease Prevention and Control
(ECDC), Stockholm, Sweden
Citation style for this article:
Caini S, Hajdu A, Kurcz A, B öröcz K. Hospital-acquired infections due to multidrug-resistant organisms in Hung ary, 2005-2010. Eu ro Surveill. 20 13;18(2):pii=20352.
Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=20352
Article submitted on 18 March 2012 / p ublished on 10 January 2013
Healthcare-associated infections caused by multidrug-
resistant organisms are associated with prolonged
medical care, worse outcome and costly therapies.
In Hungary, hospital-acquired infections (HAIs) due
to epidemiologically important multidrug-resistant
organisms are notifiable by law since 2004. Overall,
6,845 case-patients (59.8% men; median age: 65
years) were notified in Hungary from 2005 to 2010.
One third of case-patients died in hospital. The over-
all incidence of infections increased from 5.4 in 2005
to 14.7 per 100,000 patient-days in 2010. Meticillin-
resistant Staphylococcus aureus (MRSA) was the most
frequently reported pathogen (52.2%), but while its
incidence seemed to stabilise after 2007, notifica-
tions of multidrug-resistant Gram-negative organ-
isms have significantly increased from 2005 to 2010.
Surgical wound and bloodstream were the most fre-
quently reported sites of infection. Although MRSA
incidence has seemingly reached a plateau in recent
years, actions aiming at reducing the burden of HAIs
with special focus on Gram-negative multidrug-resist-
ant organisms are needed in Hungary. Continuing pro-
motion of antimicrobial stewardship, infection control
methodologies, reinforced HAI surveillance among
healthcare and infection control practitioners, and
engagement of stakeholders, hospital managers and
public health authorities to facilitate the implementa-
tion of existing guidelines and protocols are essential.
Healthcare-associated infections are infections aris-
ing from any aspect of healthcare management, most
commonly during hospitalisation in acute care facilities
(hospital-acquired infections, HAI) where the patient
receives treatment for another medical or surgical
condition. These infections are a significant cause of
morbidity and mortality worldwide, primarily among
immunocompromised and elderly people, especially if
the causative organism has developed resistance to a
number of antimicrobial agents. Patients infected with
multidrug-resistant organisms usually have a signifi-
cantly longer hospital stay, are more likely to be in need
of intensive care, costly therapies and treatments, and
have a worse prognosis . While the burden of HAIs
due to multidrug-resistant organisms may vary widely
according to geographical region, healthcare setting,
type of pathogen and antimicrobial substance, its rel-
evance to patient safety and public health continues to
increase both nationally and internationally. Therefore
surveillance of HAIs caused by multidrug-resistant
organisms, epidemiological, microbiological or both,
has been established in most industrialised countries
[2-6], and the need for a global approach has been rec-
Data from the European Antimicrobial Resistance
Surveillance Network (EARS-Net) are worrisome. The
proportion of strains of major pathogens isolated from
blood or cerebrospinal fluid (CSF) with resistance to
important antimicrobial agents exceeds 10% or even
25% in several countries, with the highest figures seen
in southern and eastern Europe [8,9]. Recently, national
efforts in infection control in the European Union (EU)
have led in some countries to a plateau or even a
reversal of the trend of increasing resistance to anti-
microbial agents, for example for meticillin-resistant
Staphylococcus aureus (MRSA), penicillin- and/or mac-
rolide-resistant Streptococcus pneumoniae and amino-
glycoside-resistant Enterococci; however, increasing
trends are still being observed for multidrug-resistant
Escherichia coli and Klebsiella pneumoniae .
Carbapenems are currently considered as last-line
antibiotics for the treatment of many infections caused
by certain multidrug-resistant organisms. In particular,
carbapenem resistance among Gram-negative microor-
ganisms such as K. pneumoniae [9,10], Pseudomonas
aeruginosa  and Acinetobacter baumannii  has
recently increased in Europe.
In Hungary (population ca. 10 million), HAIs due to
epidemiologically important multidrug-resistant
organisms are notifiable by law through the national
surveillance system for nosocomial infections (Nemzeti
Nosocomiális Surveillance Rendszer, NNSR) which was
established in October 2004. Reporting is mandatory
for all hospitals. We aimed at describing the patient
population and infections due to multidrug-resistant
organisms reported to the relevant surveillance mod-
ule of the NNSR, and assessing the epidemiological
trends during the period from 2005 to 2010 and the
recent situation of reported HAIs caused by multidrug-
resistant organisms in Hungary.
Data source and reporting method
The NNSR, operated by the National Center for
Epidemiology in Budapest, Hungary, is a national
surveillance network and a database of nosocomial
infections. Data on incident cases are collected, using
surveillance methodology and HAI case definitions
of the United States Centers for Disease Control and
Prevention (US CDC) . As of December 2010, the
NNSR consisted of three compulsory modules (noso-
comial outbreaks, HAI caused by multidrug-resistant
organisms/Clostridium difficile, and nosocomial blood-
stream infections), four voluntary modules (surgical
site infections, intensive care unit- and perinatal inten-
sive care unit-based surveillance, device-associated
infections) and a disinfectant database . Reporting
of the compulsory elements is continuous.
The relevant surveillance module of the NNSR con-
tains records from patients with HAI caused by a given
multidrug-resistant organism at one or more anatomi-
cal sites, acquired during a given hospital stay. HAI is
defined as a localised or systemic condition resulting
from an adverse reaction to the presence of an infec-
tious agent(s) or its toxin(s), with no evidence that
the infection was present or incubating at the time of
HAIs caused by the following multidrug-resistant
organisms were included in the period studied:
meticillin-resistant S. aureus (MRSA), vancomycin-
resistant Enterococcus sp. (VRE), multidrug-resistant
Enterobacter sp., multidrug-resistant Escherichia coli,
multidrug-resistant Klebsiella sp., multidrug-resistant
A. baumannii, multidrug-resistant P. aeruginosa, co-
trimoxazole-resistant Stenotrophomonas maltophilia,
and intermediate vancomycin-resistant S. aureus
(VISA). The pathogens and key antibiotics to which
resistance was monitored were selected through
national expert consultations (Table 1). Throughout the
period studied, resistance thresholds defined by the
Clinical and Laboratory Standards Institute (CLSI) were
used in laboratories in Hungary [14-19].
Variables required included information on patients’
demographics (age, sex), lifestyle characteristics
(smoking, alcohol consumption, drug abuse), medical
history (concomitant diseases, recent surgeries), hos-
pital stay (hospital ward, diagnosis upon admission,
therapies or medical procedures applied as well as use
of catheters before the recognition of HAI), outcome at
discharge (recovered, transferred to another hospital,
deceased), and healthcare-associated infection caused
by a multidrug-resistant organism (pathogen, type of
infection, date of microbiological confirmation). Data
on admission diagnosis, concomitant diseases and life-
style characteristics were gathered from International
Classification of Diseases (ICD-10) diagnosis codes
documented in the medical records. Case-based data
were entered in the internet-based surveillance tool by
infection control (IC) nurses and, if available, approved
by IC doctors when the patient affected was discharged
from the hospital or dies. No post-discharge data are
Study design and study population
We conducted a descriptive study including all noti-
fied cases of HAI due to multidrug-resistant organisms
in Hungary until 2010. We defined a case-patient as a
patient who was infected with one or more multidrug-
resistant organisms at one or more anatomical sites
during a given hospital stay. Data from 2004 were
Pathogens included in the module for hospital-acquired
infections due to multidrug-resistant organisms of the
national surveillance system for nosocomial infections in
ESBL: extended spectrum beta-lactamase; MRSA: meticillin-
resistant Staphylococcus aureus; VISA: intermediate
vancomycin-resistant S. aureus; VRE: vancomycin-resistant
a VISA was added to the surveillance module in 2008.
Microorganism Antibiotic resistance
aureus (MRSA) Meticillin/oxacillin
Klebsiella sp. Third generation cephalosporins for ESBL-
production, imipenem and/or meropenem
baumannii Imipenem and/or meropenem
Escherichia coli Third generation cephalosporins for E SBL-
production, imipenem and/or meropenem
Sensitive to maximum two of the following
agents: piperacillin/tazobactam, cef tazidin,
cefepim, imipenem, meropenem,
ciprofloxacin, gentamicin, tobramycin,
Enterobacter sp. Third generation cephalosporins for ESBL-
production, imipenem and/or meropenem
maltophilia Cotrimaxazol (sumetrolim)
aureus (VISA)aIntermediate sensitivit y to vancomycin
discarded because the surveillance system was estab-
lished and launched in that year, and the reported
data are incomplete. Furthermore we excluded case-
patients for whom date of admission, date of discharge
or microbiological tests were not available.
Descriptive and analytical methods
We estimated the yearly coverage of the surveillance
system by means of three indicators: proportion of all
hospitals included in the system (hospitals notifying at
least one multidrug-resistant organism/all hospitals in
Hungary), proportion of hospitalisations (hospitalisa-
tion in the notifying hospitals/hospitalisations in all
hospitals in Hungary), and proportion of patient-days
(patient-days in the notifying hospitals/patient-days in
all hospitals in Hungary).
We described HAI case-patients in terms of the follow-
ing variables: sex, age at admission, lifestyle char-
acteristics, underlying medical conditions, type of
healthcare institution, hospital ward, medical proce-
dures and devices applies, outcome, type of infection
and type of multidrug-resistant organism.
We classified healthcare institutions into five catego-
ries: primary (typically city hospitals with essential
medical specialties), secondary (typically county hos-
pitals and large hospitals in the capital city with highly
differentiated clinical functions), tertiary (central refer-
ral hospitals and university clinics with highly differen-
tiated clinical functions, specialised staff and technical
equipment), specialised hospitals (single clinical spe-
cialty, possibly with sub-specialties) as well as chronic
Distributions of categorical variables between patient
groups (e.g. case-patients with versus those without
prior operation) were compared using the chi-square
test. A p-value of 0.05 was considered to be statisti-
cally significant. For continuous variables, interquar-
tile ranges (IQR) were calculated.
Annual incidence densities of reported HAIs were cal-
culated as: (number of HAIs notified to NNSR during
a given year) / (patient-days from all hospitals noti-
fying at least one HAI that year) x 100,000. Incidence
densities were calculated overall and stratified by
multidrug-resistant organism. Denominator data were
retrieved from official annual reports on hospital beds
and patient turnover issued by the National Health
Insurance Fund in Hungary .
The analyses were performed using Stata v10
The proportion of hospitals that reported at least one
patient with HAI due to a multidrug-resistant organ-
ism to the NNSR gradually increased from 27.8% (50
of 180) in 2005 to 43.6% (75 of 172) in 2010. In 2005,
reporting hospitals received 64.0% of hospitalisations
and accounted for 58.5% of patient-days in Hungary,
while in 2010 the corresponding figures were 87.8%
Overall, 8,673 case-patients were reported between
2004 and 2010. After applying exclusion criteria, 6,845
case-patients (59.8% men; median age at admission:
65 years, range: 1–98 years) were included in the anal-
ysis as study population (Table 2). The most frequently
reported concomitant diseases were cardiovascular
(44.0%) and chronic respiratory diseases (15.7%). The
number of reported case-patients increased from 590
in 2005 to 1,807 in 2010. The median length of hos-
pital stay was 25 days (IQR: 14–42 days) in the study
population. The proportion of case-patients infected
with more than one multidrug-resistant organism dur-
ing the same hospital stay was around 18% each year;
the median length of their hospital stay was 39 days
Selected characteristicsa of patients with reported hospital-
acquired infection due to multidrug-resistant organism in
Hungary, 2005–10 (n=6,845)
Patient characteristics Number Propor tion of study
Male case-patients 4,095 59.8
Female case-patients 2,750 40.2
Age group (age at admission)
0–10 years 211 3.1
11–20 years 93 1.4
21–30 years 189 2.8
31–40 years 291 4.2
41–50 years 556 8.1
51–60 years 1,315 19.2
61–70 years 1,614 23.6
71–80 years 1,715 25.1
81–90 years 807 11.8
91–100 years 54 0.8
Lifest yle characteristics
Smoking 597 8.7
Alcohol abuse 538 7.9
Cardiovascular disease 3,015 44.0
disease 1,072 15.7
Cancer 970 14.2
Chronic kidney disease 545 8.0
a Based on relevance and frequency.
(IQR: 24–61 days). The median number of days elapsed
between date of admission and date of first micro-
biological confirmation of an HAI due to a multidrug-
resistant organism was 12 (IQR: 6–21 days).
The number of case-patients notified by primary, sec-
ondary, tertiary, specialised and chronic care/reha-
bilitation hospitals was 1,163 (17.0%), 3,099 (45.3%),
2,433 (35.5%), 104 (1.5%) and 46 (0.7%), respectively.
Fourteen hospitals accounted for more than half (3,560
of 6,845) of all reported case-patients. Almost one
third of all case-patients (1,950 of 6,845) were reported
from hospitals located in the capital city, Budapest.
In Table 3, data on hospital stay (ward at admission,
medical procedures and devices applied) are reported.
Among surgical specialties, the most frequently
reported wards were general surgery (40.7%), trau-
matology (24.7%) and urology (11.5%), and among
medical specialties general internal medicine (46.8%),
haematology-oncology (12.1%) and infectious diseases
(9.7%). Fifty-five per cent of case-patients underwent
prior surgical intervention, most commonly gastro-
intestinal and liver surgery (24.4%, excluding trans-
plantations), orthopedic surgery (19.0%), neurosurgery
(5.1%) and head and neck surgery (4.6%).
Case-patients with prior surgery had a lower preva-
lence of cardiovascular disease (41% versus 47%,
p<0.001), chronic respiratory disease (11% versus 21%,
p<0.001) and chronic kidney disease (5% versus 11%,
p<0.001) compared to those without. No difference
was found in age and sex distribution between the two
groups. Among case-patients who underwent prior sur-
gery the most common types of HAI were 54.6% surgi-
cal site infection (SSI), 9.7% bloodstream infection and
9.6% urinary tract infection (UTI). The most frequent
types of infection among those without prior surgery
were bloodstream infection (21.9%), UTI (17.2%) and
Information on the outcome during the current hospi-
tal stay was available for 6,388 case-patients (93.3%).
Of them, 2,772 (43.4%) recovered, 1,470 (23.0%) were
transferred to another hospital, and 2,146 (33.6%)
died. Patients infected with multidrug-resistant P.
aeruginosa and A. baumannii had the highest case-
fatality (43.8% and 40.2%, respectively); case fatal-
ity for MRSA infection was 32.6%. Patients infected
with more than one multidrug-resistant organism had
a case-fatality of 48.7%. Among all deaths, according
to the reports, 14.2% were related directly or indirectly
to the HAI.
Reported hospital-acquired infections
Of the 6,845 case-patients, 5,482 (80.1%) were infected
with one multidrug-resistant organism at one anatomi-
cal site, 1,094 (16.0%) with one multidrug-resistant
organism at more than one anatomical site, 129 (1.9%)
with more than one multidrug-resistant organism at
one anatomical site, and 140 (2.0%) with more than
one multidrug-resistant organism at more than one
anatomical site. The overall number of individual HAIs
reported was 8,732. The overall incidence of HAI due
to multidrug-resistant organisms increased from 5.4
in 2005 to 14.7 per 100,000 patient-days in 2010. The
overall yearly incidence (per 100,000 patient-days) of
HAI in primary, secondary, tertiary, specialised and
chronic care/rehabilitation hospitals was 9.4, 9.1, 11.2,
7.5 and 3.2, respectively.
MRSA was the most frequent single cause of HAI dur-
ing the study period (n=4,477, 52.2%), but while MRSA
numbers stabilised after 2007 (annual notifications
were 471 in 2005, 826 in 2007 and 824 in 2010), noti-
fications of all the other multidrug-resistant organisms
kept increasing during 2005 to 2010 from 247 to 1,468.
As a result, MRSA represented 65.6% and 36.0% of all
HAIs in 2005 and 2010, respectively. Incidence rates of
reported HAIs by type of multidrug-resistant organism
(excluding vancomycin-resistant Enterococcus sp., co-
trimoxazole-resistant S. maltophilia and intermediate
vancomycin-resistant S. aureus, which never exceeded
an annual incidence rate of 0.1 per 100,000 patient-
days in any given year) are shown in Figure 1.
SSI and bloodstream infection were the two most fre-
quently reported sites during the whole study period;
Characteristics of hospital stay of case-patients with
reported hospital-acquired infection due to multidrug-
resistant organism in Hungary, 2005–10 (n=6,845)
hospital stay Number Propor tion of study
Ward at admission
Surgical ward 2,523 36.9
Intensive care unit 2,082 30.4
Medical ward 1,754 25.6
Rehabilitation ward 256 3.7
Obstetrics and g ynaecolog y ward 47 0.7
Paediatrics ward 41 0.6
Psychiatry ward 39 0.6
Other/mixed 38 0.6
Missing 65 1.0
Medical interventions and devices
Prior surgical intervention 3,762 55.0
Urinary catheter 3,888 56.8
Peripheral catheter 3,711 54.2
Central venous catheter 2,706 39.5
Endotracheal tube 2,029 29.6
Parenteral nutrition 1,671 24.4
Tracheostomy 1,007 14.7
Gastrostomy 150 2.2
Exter nal ventricular drain 143 2.1
yet their proportion among all reported HAIs due to
multidrug-resistant organisms decreased from 31.9%
to 25.1% and from 25.9% to 21.7%, respectively, from
2005 to 2010. The proportion of reported urinary tract
infections increased from 7.7% in 2005 to 19.3% in
Considerable differences were found in the distribution
of the type of infections by multidrug-resistant organ-
ism (Figure 2). MRSA was the most frequently reported
multidrug-resistant organism for all sites of infection
in 2010 except for urinary tract and lower respira-
tory tract (Figure 3). However, the proportion of MRSA
as cause of HAI decreased at each site of infection
between 2005 and 2010, while an increase was seen in
the proportion of multidrug-resistant A. baumannii (at
all infection sites, except for urinary tract), E. coli (par-
ticularly bloodstream and urinary tract infections) and
Klebsiella sp. (particularly surgical site and soft tissue
The coverage of Hungarian hospitals by the NNSR has
constantly grown over the years. Although less than
half of all hospitals notified at least one infection due
to multidrug-resistant organisms in 2010, these health-
care institutions accounted for the vast majority of
hospitalisations and patient-days in the country during
that year. Efforts to further expand the coverage of the
surveillance system should focus on those hospitals
not currently reporting: mainly smaller facilities and
chronic care hospitals.
The proportion of reports sent by primary, specialised
and chronic care/rehabilitation hospitals was lower
than their relative proportion of overall number of
acute and chronic beds in Hungary. The opposite was
observed for tertiary-level hospitals, while no differ-
ence was found for secondary-level hospitals. Varying
compliance with reporting, case-mix of patients and
presence or absence of high-risk specialties are the
most plausible explanations for these differences.
Annual incidence rates of reported hospital-acquired infections due to multidrug-resistant organisms in Hungary, 2005–10
2005 2006 2007 2008 2009 2010
HAIs/patient-days at hospital (x 100,000)
HAI: healthcare-associated infection; MACI: multidrug-resistant Acinetobacter baumannii; MECO: multidrug-resistant Escherichia coli;
MENB: multidrug-resistant Enterobacter sp.; MKLE: multidrug-resistant Klebsiella sp; MPAE: multidrug-resistant Pseudomonas aeruginosa;
MRSA: methicillin-resistant Staphylococcus aureus.
Surgical departments were the most frequent hospi-
tal wards concerned, and further investigations are
needed to disentangle the possible impact of paral-
lel surveillance activities linked to the SSI module of
the NNSR, and specific issues in perioperative care.
ICUs were the second in line which is likely due to the
presence of high-risk patients, better patient monitor-
ing, including higher frequency of sampling and more
timely microbiological diagnosis. Similarly, an influ-
ence of the dedicated ICU surveillance module can-
not be excluded. A more in-depth description should
assess differences by region, individual hospitals and
The population of case-patients affected by HAI due
to multidrug-resistant organisms was characterised
by old age at admission, a high prevalence of comor-
bidities, and a large proportion of prior surgical inter-
ventions and indwelling medical devices. All these
are known risk factors for developing an HAI, either
by impairing the immune system or by facilitating the
entry of a multidrug-resistant organism through a med-
ical procedure .
One third of the case-patients died during their hospi-
talisation. This figure is probably biased downwards
considering that no information on final outcome is
available for patients who were transferred to another
hospital. According to the notification data, 14.2% of
deaths could directly be ascribed to the HAI; however,
no definition of HAI-related death exists in the NNSR to
which reporting personnel must adhere.
MRSA was the most frequent cause of HAI at most
anatomical sites except for UTIs and lower respiratory
tract infections (LRTIs), exceeding 50% of all reported
HAIs at surgical site as well as skin and soft tissues.
Multidrug-resistant A. baumannii was the most fre-
quent cause of LRTI, probably linked to ventilation and
oral care practices. Extended-spectrum beta-lacta-
mase (ESBL)-producing bacteria are increasingly caus-
ing UTI in inpatients and outpatients worldwide .
Also in Hungary, the proportion of reported UTIs due to
multidrug-resistant organisms more than doubled over
the study period; multidrug-resistant K. pneumoniae
and multidrug-resistant E. coli accounted for approxi-
mately 70% of reports. This is most likely due to both
the increased occurrence, spread and microbiological
diagnoses of these pathogens. Improved awareness
can also be a contributing factor since the issue has
been extensively discussed at infection control meet-
ings in Hungary since 2009, and a recommendation
on the prevention of catheter-associated urinary tract
infections was published in the same year.
The overall incidence of reported HAIs due to mul-
tidrug-resistant organisms in Hungary has shown a
significant increase in recent years, but different ten-
dencies are seen for Gram-positive and Gram-negative
pathogens. Concerning Gram-positive pathogens,
the incidence of MRSA infections has lately reached
a plateau in some European countries  and in the
United States . Similarly in Hungary, MRSA inci-
dence seemed to have stabilised around six infections
per 100,000 patient-days over the last four years of the
study period, when the reporting system was already
established in major hospitals. In other words, at the
beginning of surveillance, the continuously improving
reporting of MRSA infections could have been the rea-
son for the increase in observed incidence. After this
initial period, we assume that the observed incidence
approached the true incidence which has remained sta-
ble since then. Nonetheless, this figure is lower than
those reported by most other European [3,25-27] and
non-European countries [23,28,29]. For instance, the
incidence of hospital-onset MRSA in Germany was 23
per 100,000 patient-days in 2009, approximately four
times higher than the Hungarian result . In Canada
, the figure was 34.3 per 100,000 patient-days in
2007, around six times higher than in Hungary. The
Most frequent types of reported hospital-acquired
infections due to multidrug-resistant organisms in
Hungary in 2010 (n=2,252)
MACI: multidrug-resistant Acinetobacter baumannii; MECO:
multidrug-resistant Escherichia coli; MENB: multidrug-resistant
Enterobacter sp.; MKLE: multidrug-resistant Klebsiella sp; MPAE:
multidrug-resistant Pseudomonas aeruginosa; MRSA: meticillin-
resistant Staphylococcus aureus.
Other anatomical sites
Skin and soft tissues infection
Lower respiratory tract infection
Urinary tract infection
Surgical site infection
number of reported cases per 100,000 population in
2010 was 8.8 in Norway  and 16.8 and Sweden ,
to be compared with a value of 8.24 in Hungary. How
much this is due to underreporting or true differences
in incidence is hard to establish; differences in the
frequency of microbiological sampling, availability of
microbiological services, structure of surveillance sys-
tems and general compliance with reporting may also
play an important role.
Prevention and control of infections caused by meticil-
lin/oxacillin resistant S. aureus has been facilitated by
a national guidance available in Hungary since 2001.
Due to improved knowledge over time, not only infec-
tion control practitioners, but also healthcare work-
ers have become familiar with necessary actions to
be taken in case of MRSA in hospitals. Nonetheless it
serves as a warning that the proportion of S. aureus
resistant to meticillin isolated from blood is currently
around 30% in Hungary, with a significant increase
seen between 2007 and 2010 .
In contrast to the incidence pattern of Gram-
positive MRSA, the incidence of infections caused by
multidrug-resistant Gram-negative organisms has con-
tinuously increased since the establishment of NNSR.
The magnitude of this increase is striking (the ratio
of incidences in 2010 versus 2005 is 11 for multidrug-
resistant E. coli, 9 for multidrug-resistant A. bauman-
nii, 6 for co-trimoxazole-resistant S. maltophilia, 5 for
multidrug-resistant Enterobacter sp. and 5 for multi-
drug-resistant Klebsiella sp.), similarly to what has
been observed in the EU  and also countries out-
side the EU [30-33] in the same time period. Therefore
there appears to be a true increase in their incidence
in Hungary, whereas the impact of improved report-
ing due to better awareness of the problem may obvi-
ously play a role, too. Recent surveillance results show
that incidences of most multidrug-resistant organ-
isms in 2011 are comparable to their respective values
observed in 2010, except for multidrug-resistant A.
baumannii, whose incidence further increased.
While extensive or inappropriate antimicrobial use may
be the key factor in the striking emergence of multid-
rug-resistant Gram-negative organisms, their current
successful spread, compared to MRSA, could also be
attributed to particular microbiological characteristics
(e.g. a successful decolonisation strategy is not avail-
able) and more efficient survival strategies through
dissemination of acquired mechanisms of antibiotic
resistance. Interestingly, Hungary is in the lower third
of European countries regarding the quantity of out-
patient antimicrobial consumption and had the low-
est hospital use of antimicrobials for systemic use in
2009, nevertheless quality indicators of antibiotic use
suggest issues need to be addressed both in ambula-
tory and hospital care [34-36]. We hypothesise that
limited collecting of appropriate and early microbiolog-
ical samples before initiating empiric antibiotic ther-
apy, and therefore limited streamlining of antibiotic
treatment based on culture results, may be the most
relevant problem areas in practice.
A comprehensive evaluation of the National Nosocomial
Surveillance System is planned in 2013 to assess
its impact on the prevention and control of HAI in
Hungary. At national level, surveillance results formed
the basis for a decree issued by the Ministry of Health
in 2009 (extended in its scope in 2012) on the preven-
tion and control of HAI, surveillance of antimicrobial
consumption and professional minimum requirements
. Governmental bodies and institutions with public
health function were involved in the organisation of
national campaigns linked to the European Antibiotic
Awareness Day targeting both professionals and
the public. National recommendations have already
been issued for MRSA, VISA, ESBL-producing Gram-
negative pathogens, VRE, and carbapenemase-pro-
ducing Enterobacteriaceae [38-44]. However, partially
as a reaction to the current epidemiological trends, a
new comprehensive recommendation on prevention
of infections caused by Gram-positive and emerging
Gram-negative multidrug-resistant pathogens is being
Most frequently reported multidrug-resistant organisms
by type of hospital-acquired infection in Hungary in 2010
MACI: multidrug-resistant Acinetobacter baumannii; MECO:
multidrug-resistant Escherichia coli; MENB: multidrug-resistant
Enterobacter sp.; MKLE: multidrug-resistant Klebsiella sp; MPAE:
multidrug-resistant Pseudomonas aeruginosa; MRSA: meticillin-
resistant Staphylococcus aureus.
While national actions are essential, prevention efforts
will have the desired effect only if existing guidelines
and protocols are effectively and efficiently imple-
mented in hospitals and followed in routine practice,
tailored to the situation described by local surveillance
results. Measures implemented at hospital level over
the years also have to be reviewed and evaluated.
Additional financial resources are needed for hospitals
to be able to meet all legal requirements and provide
continuous training for their personnel. Promotion of
microbiological diagnosis would also be highly rel-
evant. A number of obstacles should be addressed, for
example healthcare reimbursement through diagnosis-
related groups without separate budget for diagnostics
and treatment, which may currently act as a disincen-
tive to taking samples for microbiological tests.
In summary, our results highlight that, in addition to
the efforts made until now, further actions are needed
in Hungary, both at locally and nationally to reduce the
burden of HAIs due to multidrug-resistant organisms.
We would like to thank Dr. Ákos Tóth at the National Center
for Epidemiology, Dr. Carl Suetens and Dr. Biagio Pedalino
at the European Centre for Disease Prevention and Control
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