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Hospital-acquired infections due to multidrug-resistant organisms in Hungary, 2005-2010

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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 overall incidence of infections increased from 5.4 in 2005 to 14.7 per 100,000 patient-days in 2010. Meticillinresistant Staphylococcus aureus (MRSA) was the most frequently reported pathogen (52.2%), but while its incidence seemed to stabilise after 2007, notifications of multidrug-resistant Gram-negative organisms have significantly increased from 2005 to 2010. Surgical wound and bloodstream were the most frequently 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-resistant organisms are needed in Hungary. Continuing promotion 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 implementation of existing guidelines and protocols are essential.
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1www.eurosurveillance.org
S   
Hospital-acquired infections due to multidrug-resistant
organisms in Hungary, 2005-2010
S Caini (saverio.caini@gmail.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.
Introduction
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 [1]. 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-
ognised [7].
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 [9].
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 [9] and Acinetobacter baumannii [11] 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
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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.
Methods
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) [12]. 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 [13]. 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
admission [12].
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
collected.
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
T 1
Pathogens included in the module for hospital-acquired
infections due to multidrug-resistant organisms of the
national surveillance system for nosocomial infections in
Hungary, 2005–10
ESBL: extended spectrum beta-lactamase; MRSA: meticillin-
resistant Staphylococcus aureus; VISA: intermediate
vancomycin-resistant S. aureus; VRE: vancomycin-resistant
Enterococcus sp.
a VISA was added to the surveillance module in 2008.
Microorganism Antibiotic resistance
Staphylococcus
aureus (MRSA) Meticillin/oxacillin
Klebsiella sp. Third generation cephalosporins for ESBL-
production, imipenem and/or meropenem
Acinetobacter
baumannii Imipenem and/or meropenem
Escherichia coli Third generation cephalosporins for E SBL-
production, imipenem and/or meropenem
Pseudomonas
aeruginosa
Sensitive to maximum two of the following
agents: piperacillin/tazobactam, cef tazidin,
cefepim, imipenem, meropenem,
ciprofloxacin, gentamicin, tobramycin,
amikacin, aztreonam
Enterobacter sp. Third generation cephalosporins for ESBL-
production, imipenem and/or meropenem
Stenotrophomonas
maltophilia Cotrimaxazol (sumetrolim)
Staphylococcus
aureus (VISA)aIntermediate sensitivit y to vancomycin
Enterococcus sp.
(VRE) Vancomycin
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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
care/rehabilitation hospitals.
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 [20].
The analyses were performed using Stata v10
(StataCorp LP).
Results
Reporting hospitals
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%
and 78.7%.
Patient population
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
T 2
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
population (%)
Sex
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
Concomitant diseases
Cardiovascular disease 3,015 44.0
Chronic respiratory
disease 1,072 15.7
Cancer 970 14.2
Chronic kidney disease 545 8.0
a Based on relevance and frequency.
4www.eurosurveillance.org
(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
pneumonia (13.9%).
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;
T 3
Characteristics of hospital stay of case-patients with
reported hospital-acquired infection due to multidrug-
resistant organism in Hungary, 2005–10 (n=6,845)
Characteristics of
hospital stay Number Propor tion of study
population (%)
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
5www.eurosurveillance.org
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
2010.
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
infections).
Discussion
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.
F 1
Annual incidence rates of reported hospital-acquired infections due to multidrug-resistant organisms in Hungary, 2005–10
(n=8,732)
0.0
1.0
2.0
3.0
4.0
5.0
6.0
7.0
2005 2006 2007 2008 2009 2010
MRSA MKLE
MACI MECO
MPAE MENB
HAIs/patient-days at hospital (x 100,000)
Year
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.
6www.eurosurveillance.org
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
ward types.
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 [21].
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 [22].
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 [23] and in the
United States [24]. 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 [3]. In Canada
[28], the figure was 34.3 per 100,000 patient-days in
2007, around six times higher than in Hungary. The
F 2
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.
0%
50%
100%
MRSA
(N=824)
MKLE
(N=470)
MACI
(N=401)
MECO
(N=309)
MPAE
(N=165)
MENB
(N=83)
Other anatomical sites
Skin and soft tissues infection
Lower respiratory tract infection
Pneumonia
Urinary tract infection
Bloodstream infection
Surgical site infection
7www.eurosurveillance.org
number of reported cases per 100,000 population in
2010 was 8.8 in Norway [27] and 16.8 and Sweden [26],
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 [9].
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 [9] 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
[37]. 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
developed.
F 3
Most frequently reported multidrug-resistant organisms
by type of hospital-acquired infection in Hungary in 2010
(n=2,143)
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.
0%
10%
20%
30%
40%
50%
60%
70%
80%
90%
100%
Pneumonia
(N=304)
Lower
respiratory
tract
infection
(N=221)
Other MDRO
MENB
MPAE
MECO
MACI
MKLE
MRSA
Skin and
soft
tissues
infection
(N=102)
Surgical
site
infection
(N=576)
Bloodstream
infection
(N=498)
Urinary
tract
infection
(N=442)
8www.eurosurveillance.org
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.
Acknowledgments
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
(ECDC) for their valuable comments to the manuscript.
References
1. Ben-David D, Novikov I, Mermel LA. Are there differences in
hospital cost between patients with nosocomial methicillin-
resistant Staphylococcus aureus bloodstream infection and
those with methicillin-susceptible Staphylococcus aureus
bloodstream infection? Infect Control Hosp Epidemiol.
2009;30(5):453-60.
2. Centers for Disease Control and Prevention (CDC). National
Healthcare Safety Network (NHSN). Atlanta: CDC. [Accessed: 19
Dec 2012]. Available from: http://www.cdc.gov/nhsn/
3. Nationales Referenzzentrum für Surveillance von nosokomialen
Infektionen (NRZ) [German National Reference Center for
the Surveillance of Nosocomial Infections]. MRSA-KISS
Reference Data, 2009. Berlin: NRZ. [Accessed: 19 Dec 2012].
Available from: http://www.nrz-hygiene.de/en/surveillance/
hospital-infection-surveillance-system/mrsa-kiss/
4. Geffers C, Gastmeier P. Nosocomial infections and multidrug-
resistant organisms in Germany: epidemiological data from
KISS (the Hospital Infection Sur veillance System). Dtsch
Arztebl Int. 2011;108(6):87-93.
5. Centres de Coordination de la Lutte contre les Infections
Nosocomiales (CCLIN) [Infection Control Coordinating Centres].
Homepage. Nancy: CCLIN. [Accessed: 19 Dec 2012]. French.
Available from : http://www.cclin-france.fr/
6. Carlet J, Astagneau P, Brun-Buisson C, Coignard B, Salomon
V, Tran B, et al. French national program for prevention of
healthcare associated infections and antimicrobial resistance,
1992-2008: positive trends, but perseverance needed. Infect
Control Hosp Epidemiol. 2009;30(8):737-45.
7. Transatlantic Taskforce on Antimicrobial Resistance (TATFAR).
Recommendations for future collaboration between the U.S.
and EU. TATFAR; 2011. Available from: http://www.cdc.gov/
drugresistance/pdf/tatfar-report.pdf
8. European Centre for Disease Prevention and Control. Annual
Epidemiological Report 2011. Reporting on 2009 surveillance
data and 2010 epidemic intelligence data. Stockholm:
ECDC; 2011. Available from: http://www.ecdc.europa.eu/en/
publications/Publications/Forms/ECDC_DispForm.aspx?ID=767
9. European Centre for Disease Prevention and Control (ECDC).
Antimicrobial resistance surveillance in Europe 2010. Annual
Report of the European Antimicrobial Resistance Surveillance
Network (EARS-Net). Stockholm: ECDC; 2011. Available from:
http://ecdc.europa.eu/en/publications/Publications/1111_
SUR_AMR_data.pdf.pdf
10. Vatopoulos A. High rates of metallo-beta-lactamase-
producing Klebsiella pneumoniae in Greece--a review of
the current evidence. Euro Surveill. 2008;13(4):pii=8023.
Available from: http://www.eurosurveillance.org/ViewArticle.
aspx?ArticleId=8023
11. Durante-Mangoni E, Zarrilli R. Global spread of drug resistant
Acinetobacter baumannii: molecular epidemiology and
management of antimicrobial resistance. Future Microbiol.
2011; 6(4):407-22.
12. Horan TC, Andrus M, Dudeck MA . CDC/NHSN surveillance
definition of health care-associated infection and criteria for
specific types of infections in the acute care setting. Am J
Infect Control. 2008;36(5):309-32.
13. Országos Epidemiológiai Központ [National Center for
Epidemiology]. Tájékoztató a Nemzeti Nosocomialis
Surveillance Rendszer (NNSR) és a Nemzeti Bakteriológiai
Surveillance (NBS) 2010. évi eredményeiről [Annual Reports
of the National Surveillance System for Nosocomial Infections
(NNSR) and the National Bacteriological Surveillance System
(NBS), 2010] Epinfo. 2011;6. supplement. Hungarian. Available
from: http://www.oek.hu/oek.web?to=839,1890&nid=964&pi
d=1&lang=hun
14. Clinical and Laboratory Standards Institute (CLSI). Performance
Standards for Antimicrobial Susceptibility Testing: Fifteenth
Informational Supplement M100-S15. Wayne: CLSI; 2005.
15. Clinical and Laboratory Standards Institute (CLSI). Performance
Standards for Antimicrobial Susceptibility Testing: Sixteenth
Informational Supplement M100-S16. CLSI Wayne: CLSI; 2006.
16. Clinical and Laboratory Standards Institute (CLSI). Performance
Standards for Antimicrobial Susceptibility Testing: Seventeenth
Informational Supplement M100-S17. Wayne: CLSI; 2007.
17. Clinical and Laboratory Standards Institute (CLSI). Performance
Standards for Antimicrobial Susceptibility Testing: Eighteenth
Informational Supplement M100-S18. Wayne: CLSI; 2008.
18. Clinical and Laboratory Standards Institute (CLSI). Performance
Standards for Antimicrobial Susceptibility Testing: Nineteenth
Informational Supplement M100-S19. Wayne: CLSI; 2009.
19. Clinical and Laboratory Standards Institute (CLSI). Performance
Standards for Antimicrobial Susceptibility Testing: Twentieth
Informational Supplement M100-S20. Wayne: CLSI; 2010.
9www.eurosurveillance.org
20. Országos Egészségbiztosítási Pénztár [National Health
Insurance Fund Administration of Hungary]. Kórházi Ágyszám-
és Betegforgalmi Kimutatás. [Hospital beds and patient
turnover account]. [Date of access: 19 Dec 2012] Hungarian.
Available from http://www.gyogyinfok.hu/magyar/archiv.html
21. Puhto T, Ylipalosaari P, Ohtonen P, Syrjala H. Point prevalence
and risk factors for healthcare-associated infections in primary
healthcare wards. Infection. 2011;39( 3):217-23.
22. Coque TM, Baquero F, Canton R. Increasing prevalence of
ESBL-producing Enterobacteriaceae in Europe. Eurosurveill.
2008;13(47):pii=19044. Available from: http://www.
eurosurveillance.org/ViewArticle.aspx?ArticleId=19044
23. Pearson A, Chronias A, Murray M. Voluntary and mandatory
surveillance for methicillin-resistant Staphylococcus aureus
(MRSA) and methicillin-susceptible Staphylococcus aureus
(MSSA) bacteraemia in England. J Antimicrob Chemother.
2009;64 Suppl 1:i11-7.
24. Kallen AJ, Mu Y, Bulens S, Reingold A, Petit S, Gershman K, et
al. Health care-associated invasive MRSA infections, 2005-
2008. JAMA. 2010;304(6):641-8.
25. Health Protection Agency (HPA). Quarterly epidemiological
commentar y: mandatory MRSA, MSSA and E. coli bacteraemia,
and C.difficile infection data (up to July-September 2012).
London: HPA; 13 Dec 2012. Available from: http://www.hpa.
org.uk/webc/HPAwebFile/HPAweb_C/1284473407318
26. Smittskyddsinstitutet (SMI) [Swedish Institute
for Communicable Disease Control]. Statistik för
meticillinresistenta gula stafylokocker (MRSA). [Statistics for
meticillin-resistant Staphylococcus aureus (MRSA)) Swedish.
Available from: http://www.smittskyddsinstitutet.se/statistik/
meticillinresistenta-gula-stafylokocker-mrsa/
27. Elstrøm P, Kacelnik O, Bruun T, Iversen B, Hauge SH, Aavitsland
P. Meticillin-resistant Staphylococcus aureus in Norway, a low-
incidence country, 2006-2010. J Hosp Infect. 2012;80(1):36-40.
28. Simor AE, Gilbert NL, Gravel D, Mulvey MR, Bryce E, Loeb M,
et al. Methicillin-resistant Staphylococcus aureus colonization
or infection in Canada: National Surveillance and Changing
Epidemiology, 1995-2007. Infect Control Hosp Epidemiol.
2010;31(4):348-56.
29. Lessa FC, Mu Y, Davies J, Murray M, Lillie M, Pearson A,
et al. Comparison of incidence of bloodstream infection
with methicillin-resistant Staphylococcus aureus between
England and United States, 2006-2007. Clin Infect Dis.
2010;51(8):925-8.
30. Lautenbach E, Synnestvedt M, Weiner MG, Bilker WB, Vo
L, Schein J, et al. Epidemiolog y and impact of imipenem
resistance in Acinetobacter baumannii. Infect Control Hosp
Epidemiol. 2009;30(12):1186-92.
31. Lautenbach E, Synnestvedt M, Weiner MG, Bilker WB, Vo
L, Schein J, et al. Imipenem resistance in Pseudomonas
aeruginosa: emergence, epidemiology, and impact on clinical
and economic outcomes. Infect Control Hosp Epidemiol.
2010;31(1):47-53.
32. Ramsey AM, Zilberberg MD. Secular trends of hospitalization
with vancomycin-resistant enterococcus infection in the
United States, 2000-2006. Infect Control Hosp Epidemiol.
2009;30(2):184-6.
33. Lee K, Kim MN, Kim JS, Hong HL, Kang JO, Shin JH, et al. Further
increases in carbapenem-, amikacin-, and fluoroquinolone-
resistant isolates of Acinetobacter spp. and P. aeruginosa in
Korea: KONSAR study 2009. Yonsei Med J. 2011;52(5):793-802.
34. European Surveillance of Antimicrobial Consumption (ESAC).
ESAC Yearbook 2009. Antwerp: ESAC. [Accessed: 19 Dec 2012].
ISBN: 9789057283307. Available from: http://www.ecdc.
europa.eu/en/activities/surveillance/ESAC-Net/publications/
Pages/documents.aspx
35. Adriaenssens N, Coenen S, Verspor ten A, Muller A,
Vankerckhoven V, Goossens H; ESAC Project Group. European
Surveillance of Antimicrobial Consumption (ESAC): quality
appraisal of antibiotic use in Europe. J Antimicrob Chemother.
2011;66Suppl 6:vi71-77. doi: 10.1093/jac/dkr459.
36. Benko R, Matuz M, Peto Z, Bogár L, Viola R, Doró P, et al.
Variations and determinants of antibiotic consumption in
Hungarian adult intensive care units. Pharmacoepidemiol Drug
Saf. 2012;21(1):104-9.
37. 20/2009. (VI. 18.) EüM rendelet az egészségüg yi ellátással
összefüggő fertőzések megelőzéséről, e tevékenységek
szakmai minimumfeltételeiről és felügyeletéről. [Decree of
the Ministry of Health on prevention of healthcare-associated
infections, related professional minimum requirements
and control activities]. [Accessed: 18 Dec 2012]. Hungarian.
Available from: http://www.complex.hu/jr/gen/hjegy_doc.
cgi?docid=A0900020.EUM
38. Országos Epidemiológiai Központ [National Center for
Epidemiology]. Módszertani levél a Methicillin/Oxacillin
Rezisztens Staphylococcus Aureus (MRSA) fertőzések
megelőzésére. [Methodological letter on the prevention
of infections caused by meticillin/oxacillin-resistant
Staphylococcus aureus (MRSA)].Epinfo. 2001;8(5. különszám).
Hungarian. Available from: http://www.oek.hu/oek.web?nid=4
44&pid=2&to=16&lang=hun
39. Országos Epidemiológiai Központ [National Center for
Epidemiology]. A széles spektrumú béta-laktamázokat
termelő Gram-negatív baktériumok jelentősége és az általuk
okozott nosocomialis járványok leküzdése. [The impor tance of
extended-spectrum beta-lactamase producing Gram-negative
bacteria and control of such nosocomial outbreaks]. Epinfo.
2002;30:349-52. Hungarian. Available from: http://www.oek.
hu/oek.web?nid=1080&pid=1
40. Országos Epidemiológiai Központ [National Center for
Epidemiology]. Vancomycin-rezisztens Enterococcus (VRE)
fertőzések megelőzése az egészségügyi intézményekben.
[Prevention of infections caused by vancomycin-resistant
enterococci (VRE) in healthcare facilities]. Epinfo. 2004;42:522-
26. Hungarian. Available from: http://www.oek.hu/oek.
web?nid=1080&pid=1
41. Országos Epidemiológiai Központ [National Center for
Epidemiology]. A multirezisztens kórokozók felügyelete az
egészségügyi intézményekben. [Control of multidrug-resistant
pathogens in healthcare facilities]. Epinfo. 2007;10-11:89-
98. Hungarian. Available from: http://www.oek.hu/oek.
web?nid=1080&pid=1
42. Országos Epidemiológiai Központ [National Center for
Epidemiology]. Ajánlás a hVISA/VISA azonosítása esetén
szükséges teendőkről és a kórokozó terjedésének megelőzését
célzó infekciókontroll intézkedésekről. [Recommendations
on actions required upon the detection of hVISA/VISA and
on infection control measures to prevent its spread]. Epinfo.
2008;15:173-6. Hungarian. Available from: http://www.oek.hu/
oek.web?to=1493,1494,1495,1480&nid=41&pid=8&lang=hun
43. Országos Epidemiológiai Központ [National Center for
Epidemiology]. A S. aureus vancomycinnel szembeni
rezisztenciája. [Vancomycin resistance of S. aureus]. Epinfo.
2008;15:177-9. Hungarian. Available from: http://www.oek.hu/
oek.web?to=1493,1494,1495,1480&nid=41&pid=8&lang=hun
44. Országos Epidemiológiai Központ [National Center
for Epidemiology]. Ajánlás a karbapenemáz-termelő
Enterobacteriaceae törzsek azonosítására és terjedésük
megelőzésére az egészségügyi intézményekben.
[Recommendation on identification of carbapenemase-
producing enterobacteriaceae strains and prevention of
their spread in healthcare facilities]. Epinfo. 2011;47:541-50.
Hungarian. Available from: http://www.oek.hu/oek.web?to=83
9,1866&nid=41&pid=11&lang=hun
... The typically employed, generic patient safety training has its limitations. Despit the general rising awareness of the importance of SSI prevention, registered data has lon shown a rise of HAI again in Hungary [13] (Figure 1), while the data was only made avai able combined for multi-resistant infections (MR), Clostridium difficile (CDI), and blood stream infections (BSI). The rising number of incidences once again drew the attention t the importance of effective training. ...
... The total number of reported infections in Hungary until the Coronavirus outbreak, whe the data reporting scheme was fundamentally changed by the authorities. (Source: OEK 2019,[13] ...
... The total number of reported infections in Hungary until the Coronavirus outbreak, when the data reporting scheme was fundamentally changed by the authorities. (Source: OEK 2019,[13]). ...
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... The history of nosocomial infections can be traced to the origin of hospitals themselves and have been defined by the WHO as infections that develop in a patient during his/her stay in a hospital or other types of clinical facilities which were not present at the time of admission [1], [2]. Patient safety studies published in 1991 reveal the most frequent types of adverse events affecting hospitalized patients are adverse drug events, nosocomial infections, and surgical complications [3], [4]. ...
... Patient safety studies published in 1991 reveal the most frequent types of adverse events affecting hospitalized patients are adverse drug events, nosocomial infections, and surgical complications [3], [4]. According to Samuel et al. [1], these infections usually become clinically apparent either during hospitalization or after discharge and as such, organisms that cause these infections are termed nosocomial pathogens [2]. Furthermore, Samuel et al. [1], Saka et al. [5] and Amoran et al. [6] reported that infections acquired by staff or visitors to the hospital or other health care settings may also be considered as nosocomial. ...
... [7,25], Enterobacter spp. [2,26], Citrobacter spp. [18], Acinetobacter spp. ...
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The history of nosocomial infections can be traced to the origin of hospitals themselves and have been defined by the WHO as infections that develop in a patient during his/her stay in a hospital or other types of clinical facilities which were not present at the time of admission. Nosocomial infections are a major public health problem globally and are on the increase despite efforts in hospital infection control measures and contribute significantly to morbidity and mortality. Naturally, any microorganism has the potential to cause infection in hospitalized patients however, only a few including Staphylococci, Escherichia coli, Pseudomonas aeruginosa, Enterococci, fungi and to a lesser extent, viruses and parasites are responsible for the majority of nosocomial infections. In sub-Saharan Africa, data available show that the incidence of nosocomial infections ranges from 2-49% with patients in intensive care units having the highest rate ranging from 21.2-35.6%. The prevalence of nosocomial infections have been reported to vary between 1.6%-28.7% in Burkina Faso, United Republic of Tanzania, Ghana, Mali, Cameroon, Gabon, Uganda, Burundi, Democratic republic of Congo and Senegal. In Nigeria and Ethiopia, the total accruing occurrence in surgical wards has been reported to vary from 5.7%-45.8% with the later having an incidence as high as 45.8% and an incidence density equal 26.7 infections per 1000 patient days in paediatric surgical patients. In addition, 3.4-10.9% of hospital-associated infections often result to mortality in most developed countries though these figures are suspected to be higher in developing countries of sub-Saharan Africa including Nigeria. However, simple and effective control programmes together with effective training of healthcare workers will go a long way in reducing the endemic nature of nosocomial infections in sub Saharan Africa. This paper highlights the natural history, distribution, risk factors of nosocomial infections especially in sub Saharan Africa as well as its contributory factors. Nosocomial infections are endemic in sub Saharan Africa and are further enhanced by emerging and re-emerging resistant agents. Simple and effective control programme together with computer-based epidemiological surveillance carried out as a global project with considerable inputs from developing countries for monitoring will enable the development of nosocomial infections to be halted if not eliminated. In addition, it is necessary to review the current infection control practices in all hospitals particularly in developing countries including Nigeria so as to incorporate molecular techniques which have been proven to be effective in keeping the spread of nosocomial infections under check. The training and retraining of health care givers on principles of infection control is strongly recommended. Also, the principles of infection control should be incorporated into student nurses, medical students, and other paramedical curriculum as well as employment of adequately competent health workers to avoid over labour which sometimes cause workers to be inefficient resulting in disease outbreaks. Finally, hand washing and other standard infection control practices should be adhered to so that nosocomial infections can be controlled effectively.
... The history of nosocomial infections can be traced to the origin of hospitals themselves and have been defined by the WHO as infections that develop in a patient during his/her stay in a hospital or other types of clinical facilities which were not present at the time of admission [1], [2]. Patient safety studies published in 1991 reveal the most frequent types of adverse events affecting hospitalized patients are adverse drug events, nosocomial infections, and surgical complications [3], [4]. ...
... Patient safety studies published in 1991 reveal the most frequent types of adverse events affecting hospitalized patients are adverse drug events, nosocomial infections, and surgical complications [3], [4]. According to Samuel et al. [1], these infections usually become clinically apparent either during hospitalization or after discharge and as such, organisms that cause these infections are termed nosocomial pathogens [2]. Furthermore, Samuel et al. [1], Saka et al. [5] and Amoran et al. [6] reported that infections acquired by staff or visitors to the hospital or other health care settings may also be considered as nosocomial. ...
... [7,25], Enterobacter spp. [2,26], Citrobacter spp. [18], Acinetobacter spp. ...
... Furthermore, the widespread use of disinfectants may be itself a threat to human health, negatively affecting water and earth pollution, 9,10 and potentially inducing further increases in the antimicrobial resistance (AMR) of pathogens known to complicate COVID-19 clinical care. [11][12][13][14][15] Considering the current spread of AMR, responsible for the death of over 37,000 people/year in Europe alone, 16 the risk of future AMR pandemics has been recently highlighted by WHO. 17 AMR is particularly frequent in healthcare settings, due to the selective pressure exerted by the continuous use of disinfectants and antibiotics, where it is closely associated with the severity of healthcare-associated infections (HAIs), 18,19 affecting up to 15% of all hospitalized inpatients, 20 with mortality rates reaching up to 30% in Italy. 21 HAI incidence is particularly high in pediatric wards, due to the high susceptibility of children to infections. ...
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... Self-disinfecting method can be proposed as an alternative method in which hospital surfaces are smeared with a bactericidal agent using silver and copper. This method is expensive and not suitable for all surfaces (14). The issue of minimizing the risk of nosocomial infection and preventing the increase in drug resistance has turned the attention of researchers to the management of "hospital environment sanitation" instead of "patients' physical health" (15,16). ...
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The sanitation of the hospital environment for the purpose of preventing the transmission of nosocomial infections has a major role in reducing the infection of hospitalized patients with the bacteria living on hospital surfaces. The excessive use of chemical detergents in recent decades has led to microbial resistance in nosocomial infectious bacteria. Researchers’ attention has therefore been drawn to the use of probiotics for disinfecting hospital surfaces. The present study was conducted to assess the potential effectiveness of probiotic products in controlling the contamination of inert surfaces in the environment and medical instruments in health centers and investigate the claim that the antagonistic property of probiotic microorganisms offers an effective method for controlling nosocomial infections and a suitable alternative to conventional disinfection methods. A search was carried out for relevant articles published from 2000 to 2018 in databases including ISI, PubMed, Scopus, EMBASE, and Google Scholar, using the keywords "nosocomial infections", "disinfection", "sanitation", "probiotics" and "infected surfaces". The articles published from 2000 to 2018 confirmed the greater effectiveness of probiotic disinfection (by up to 90%) compared to conventional chemical disinfection in controlling nosocomial infections. Nevertheless, more extensive studies are needed on probiotics to determine the possibility of replacing good bacteria with bad bacteria in future decades.
... In addition, antimicrobial resistance (AMR) is currently spreading worldwide, representing one of the major threats for human health, and is particularly dangerous in healthcare settings, where antimicrobials are heavily used, exerting an important selective pressure on microbes. Not surprisingly, AMR is strongly associated with HAI severity, as many HAIs are caused by multidrug resistant (MDR) or even pan-drug resistant (PDR) microbes [7,8]. ...
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The hospital environment significantly contributes to the onset of healthcare associated infections (HAIs), representing the most frequent and severe complications related to health care. The monitoring of hospital surfaces is generally addressed by microbial cultural isolation, with some performance limitations. Hence there is need to implement environmental surveillance systems using more effective methods. This study aimed to evaluate next-generation sequencing (NGS) technologies for hospital environment microbiome characterization, in comparison with conventional and molecular methods, in an Italian pediatric hospital. Environmental samples included critical surfaces of randomized rooms, surgical rooms, intensive care units and delivery rooms. The resistome of the contaminating population was also evaluated. NGS, compared to other methods, detected with higher sensitivity the environmental bacteria, and was the only method able to detect even unsearched bacteria. By contrast, however, it did not detect mycetes, nor it could distinguish viable from dead bacteria. Microbiological and PCR methods could identify and quantify mycetes, in addition to bacteria, and PCR could define the population resistome. These data suggest that NGS could be an effective method for hospital environment monitoring, especially if flanked by PCR for species identification and resistome characterization, providing a potential tool for the control of HAI transmission.
... Furthermore, chemical-based sanitation can favour the selection of resistant strains, a highly undesirable "side effect" associated with this type of cleaning, that might worsen pathogens' AMR. Disinfectant-induced resistance may be directed either against disinfectants themselves (Caini et al. 2013;Cornejo-Juarez et al. 2015) but even against antibiotics, as recently reported for Chlorhexidine induction of resistance against Colistin antibiotic, considered as a last-resort drug for treatment of difficult-totreat infections sustained by MDR Gram-negative bacteria (Bock et al. 2016;Wand et al. 2017). ...
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Antimicrobial resistance (AMR) is currently one of the main concerns for human health.Due to its rapid increase and global diffusion, several common microbial infections might become not curable in the future decades, making it impossible to apply other lifesaver therapies, such as transplant or chemotherapy.AMR is frequently observed in hospital pathogens, due to selective pressure exerted by antibiotic use, and consistently with this, in the recent years, many actions have been proposed to limit AMR spread, including hygiene measures for hospital professionals and a wiser antibiotic usage.Indeed, the hospital environment itself represents a reservoir of pathogens, whose control was so far addressed by conventional sanitation procedures, which however cannot prevent recontamination and might further favour the selection of resistant strains.Here we report the results collected by studying an innovative sanitation strategy based on the use of probiotic bacteria, capable of reducing in a stable way the surface load of pathogens and their AMR. Collected data suggest that this system might contribute significantly to AMR control and might be thus considered as one of the tools for AMR and infection prevention and control.
... MDR, this showed that there are a few options to treat patients in the study area. Which was almost similar to others finding like, Studies reported from Mexico [30], Ethiopia [31], Hungary [32]. In general, we can say that antibiotics resistance will be a great challenge in the study area if there is no appropriate solution set on time. ...
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Abstract Background: Antibiotic resistance is a worldwide problem that crosses international boundaries and spread between continents easily. Hence, information on the existence of the causative microorganisms and their susceptibility to commonly used antibiotics are essential to enhance therapeutic outcome. Method: A cross-sectional study was conducted retrospectively at Hawassa University Comprehensive Specialized Hospital. The culture and antibiotic sensitivity data of the isolates were collected from the record books of the microbiology unit for the study period after official permission obtained from the institutional review board. The data entered and analyzed using statistical package for social science software version 20. Result: A total of 693 bacteria were retrieved, of these 435(62.77%) were gram-negative and the rest 258(37.23%) were gram-positive. Most of the isolates were from a urine sample. Among gram positives isolates, S. aureus and from gram negatives Klebsiella spp are the most recurrent isolate. Almost a remarkable resistance was observed to most of the antibiotics mainly, penicillin G (81.8%) and cotrimoxazole (81.1%), for gram-positive bacteria. The gramnegative bacteria also show resistance to ampicillin (92.5%), tetracycline (85%) and cotrimoxazole (93.1%). Conclusions: Nearly all isolate show substantial rates of resistance to most of the antibiotic that is frequently used in the study area. As already known we want to emphases on the importance of performing continuous monitoring of drug susceptibility to help the empirical treatment of bacterial agents to a health professional in the region. In addition, this data might help policymakers to control of antibiotics resistance. Keywords: Antibiotics resistance, Clinical samples, Southern Ethiopia
... MDR, this showed that there are a few options to treat patients in the study area. Which was almost similar to others finding like, Studies reported from Mexico [30], Ethiopia [31], Hungary [32]. In general, we can say that antibiotics resistance will be a great challenge in the study area if there is no appropriate solution set on time. ...
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