Академический Документы
Профессиональный Документы
Культура Документы
The boundaries and names shown and the designations used on the
maps do not imply the expression of any opinion whatsoever on the
part of the World Health Organization concerning the legal status of
any country, territory, city or area or of its authorities, or concerning
the delimitation of its frontiers or boundaries. Dotted lines on maps
represent approximate border lines for which there may not yet be full
agreement.
CONTENTS
Acknowledgements 1
Abbreviations 2
Summary 3
Introduction 4
4. The burden of endemic health care-associated infection in low- and middle-income countries . . . . . . . . . . . . . 16
References 26
Appendix 34
ACKNOWLEDGMENTS
Developed by the Clean Care is Safer Care Team (Patient Safety
Programme - Innovation, Information, Evidence and Research
Cluster).
Content contribution
Lead author:
Benedetta Allegranzi
WHO Patient Safety Programme, Geneva, Switzerland
Technical contribution
Marie-Noëlle Chraiti
WHO Collaborating Centre on Patient Safety
University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Statistical Analysis
Christophe Combescure
Division of Clinical Epidemiology
University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Homa Attar
WHO Collaborating Centre on Patient Safety
University of Geneva Hospitals and Faculty of Medicine, Geneva, Switzerland
Reviewers
Najeeb Al Shorbaji
WHO Patient Safety Programme, Geneva, Switzerland
Edward Kelley
WHO Patient Safety Programme, Geneva, Switzerland
Colin Mathers
WHO Mortality and Burden of Disease, Geneva, Switzerland
Editor
Rosemary Sudan
Freelance editor
Figures
Laurens Zwakhals
WHO Public Health Information and Geographic Information Systems, Geneva,
Switzerland
1
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
ABBREVIATIONS
BSI bloodstream infection
CL central line
* CR-BSI is used as a generic term throughout the report when referring to different categories included in the retrieved articles, e.g. “central
venous catheter-associated”, “central venous catheter-related”, “central line-associated”, or “catheter-related bloodstream infection”.
2
SUMMARY
Health care-associated infection (HCAI) is acquired by patients Among adult ICU patients in high-income countries, pooled
while receiving care and represents the most frequent adverse cumulative incidence densities of catheter-related BSI (CR-BSI),
event. However, the global burden remains unknown because of the urinary catheter-related UTI (CR-UTI), and ventilator-associated
difficulty to gather reliable data. In many settings, from hospitals to pneumonia (VAP) were 3.5 per 1000 CL-days, 4.1 per 1000 urinary
ambulatory and long-term care, HCAI appears to be a hidden, catheter-days, and 7.9 per 1000 ventilator-days, respectively. In low-
cross-cutting problem that no institution or country can claim to and middle-income countries, pooled cumulative incidence
have solved yet. HCAI surveillance is complex and requires the use densities of CR-BSI, CR-UTI, and VAP were 12.2 per 1000 CL-days,
of standardized criteria, availability of diagnostic facilities and 8.8 per 1000 urinary catheter-days, and 23.9 per 1000 ventilator-
expertise to conduct it and interpret the results. Surveillance days, respectively. Newborns are also a high-risk population in
systems for HCAI exist in several high-income countries but are developing countries and neonatal infection rates are three to 20
virtually nonexistent in most low- and middle-income countries. times higher than in industrialized countries.
Data included in this report are the results of systematic reviews of The impact of HCAI implies prolonged hospital stay, long-term
the literature on endemic HCAI from 1995 to 2010 in high- and low/ disability, increased resistance of microorganisms to antimicrobials,
middle-income countries. According to published national or a massive additional financial burden for health systems, high costs
multicentre studies, pooled HCAI prevalence in mixed patient for patients and their families, and excess deaths. In Europe, HCAIs
populations was 7.6% in high-income countries. The European cause 16 million extra-days of hospital stay, 37 000 attributable
Centre for Disease Prevention and Control (ECDC) estimated that deaths, and contribute to an additional 110 000 every year. Annual
4 131 000 patients are affected by approximately 4 544 100 financial losses are estimated at approximately € 7 billion, including
episodes of HCAI every year in Europe. The estimated HCAI direct costs only. In the USA, approximately 99 000 deaths were
incidence rate in the USA was 4.5% in 2002, corresponding to 9.3 attributed to HCAI in 2002 and the annual economic impact was
infections per 1000 patient-days and 1.7 million affected patients. estimated at approximately US$ 6.5 billion in 2004. Information is
again very scanty from low- and middle-income countries and no
The systematic review of the literature revealed clearly an extremely data are available at national or regional levels. According to a
fragmented picture of the endemic burden of HCAI in the developing report on device-associated infections in 173 ICUs from 25
world. Only very scanty information was available from some countries in Latin America, Asia, Africa, and Europe, crude excess
regions and no data at all for several countries (66%). Many studies mortality in adult patients was 18.5%, 23.6%, and 29.3% for CR-
conducted in health-care settings with limited resources reported UTI, CR-BSI, and VAP, respectively. A review of several studies
HCAI rates higher than in developed countries. Hospital-wide showed that increased length of stay associated with HCAI varied
prevalence of HCAI varied from 5.7% to 19.1% with a pooled between 5 and 29.5 days.
prevalence of 10.1%. Of note, the pooled HCAI prevalence was
significantly higher in high- than in low-quality studies (15.5% vs Although HCAI global estimates are not yet available, by integrating
8.5%, respectively). Surgical site infection (SSI) is the most data from published studies, there is clear evidence that hundreds
surveyed and most frequent type of infection in low- and middle- of millions of patients are affected every year worldwide, with the
income countries with incidence rates ranging from 1.2 to 23.6 per burden of disease much higher in low- and middle-income
100 surgical procedures and a pooled incidence of 11.8%. By countries. There is an urgent need to establish reliable systems for
contrast, SSI rates vary between 1.2% and 5.2% in developed HCAI surveillance and to gather data on the actual burden on a
countries. regular basis. Evaluation of the key determinants of HCAI is an
essential step to identify strategies and measures for improvement.
The risk of acquiring HCAI is significantly higher in intensive care Robust evidence exists that HCAI can be prevented and the burden
units (ICUs), with approximately 30% of patients affected by at least reduced by as much as 50% or more. Solid recommendations have
one episode of HCAI with substantial associated morbidity and been issued by national and international organizations, but their
mortality. Pooled cumulative incidence density was 17.0 episodes application needs to be strengthened and accompanied by
per 1000 patient-days in adult high-risk patients in industrialized performance monitoring both in high-income and low- and middle-
countries. By contrast, the incidence of ICU-acquired infection income countries. HCAI must be treated as a priority patient safety
among adult patients in low- and middle-income countries ranged issue within comprehensive approaches to be tackled effectively.
from 4.4% up to 88.9% and pooled cumulative incidence density The WHO Patient Safety programme integrates efforts with other
was 42.7 episodes per 1000 patient-days. WHO programmes to reduce HCAI by assisting with the
assessment, planning, and implementation of infection prevention
High frequency of infection is associated with the use of invasive and control policies, including timely actions at national and
devices, in particular central lines, urinary catheters, and ventilators. institutional levels.
3
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
INTRODUCTION
Health care-associated infections (HCAIs) are infections that
Box 1
patients acquire while receiving treatment for medical or surgical
conditions and are the most frequent adverse event during care Methodology used for systematic reviews
delivery.1 HCAI is a major problem for patient safety and its impact and analysis included in this report
can result in prolonged hospital stay, long-term disability, increased
resistance of microorganisms to antimicrobial agents, a massive Type of infection
additional financial burden for the health system, high costs for Overall HCAI, health care-associated urinary tract infection (UTI),
patients and their families, and excess deaths.2,3 The risk to acquire surgical site infection (SSI), hospital-acquired pneumonia (HAP),
HCAI is universal and pervades every health-care facility and ventilator-associated infection (VAP), and health care-associated
system worldwide, but the true burden remains unknown in many bloodstream infection (BSI).
nations, particularly in developing countries. Sources
PubMed, Cochrane Library, World Health Organization (WHO)
Data on the burden of diseases worldwide are regularly published regional medical databases (Appendix). A comprehensive list
by the World Health Organization (WHO) to inform health-care of search terms (Appendix) including MeSH terms “cross infec-
workers, policy-makers, and the public of the most important tion”, “infection control”, “developing countries” and “developed
diseases in terms of morbidity and mortality.4 HCAI does not appear countries” was used, together with the individual names of high-,
on the list of over 100 diseases evaluated. The most likely reason is middle- and low-income countries.
that the diagnosis of HCAI is complex and relies on multiple criteria
Inclusion criteria
and not on a single laboratory test. In addition, national systems of
All studies reporting full or partial data related to infection rates,
continuous surveillance are seldom in place. In many settings, from
risk factors, mortality, excess length of stay, costs, HCAI aetiol-
hospitals to ambulatory and long-term care, HCAI appears to be
ogy in general, and health care-associated UTI, BSI, SSI, and
a hidden, cross-cutting problem that no institution or country can
HAP/VAP. For high-income countries, only national or multicen-
claim to have solved yet.
tre studies were included.
This report presents the evidence available from the scientific Exclusion criteria
literature on the endemic burden of the most frequent types of Duplicate references and publications reporting the same data;
HCAI and provides an assessment of epidemiological differences studies reporting outbreaks; studies including community-ac-
among countries according to income levels. The report aims also quired infections.
to identify major obstacles and gaps to assess the magnitude of Time limits
the HCAI burden worldwide and to identify solutions and future January 1995 to December 2010.
perspectives for improvement. All data presented were compiled
Language
from systematic reviews of studies published in the scientific
No language restrictions.
literature from 1995 to 2010. Methods and key definitions used are
described in Boxes 1 and 2. Criteria to define high-quality studies
prospective design; use of standardized definitions (i.e. accord-
ing to the USA CDC NHSN system); 5 detection of at least all four
major infections for studies related to HCAI in general; and pub-
lication in a peer-reviewed journal.
Statistical analysis
Descriptive statistics of data retrieved from high, low- and mid-
dle-income countries were performed; studies were classified
according to patient population (adult, neonatal and paediatric),
level of risk (high-risk patients, i.e. those admitted to ICUs, burn
and transplant recipients vs mixed patient populations, including
© University of Geneva Hospitals
4
INTRODUCTION
Box 2
Epidemiological definitions used in this report
HCAI prevalence
Number of infection episodes or infected patients per 100 patients
present in the health-care setting or ward at a given point in time.
HCAI incidence
Number of new infection episodes or new patients acquiring an
infection per 100 patients followed up for a defined time period.
Periods vary according to the patient population. For SSI, it is
usually 30 days after surgery (1 year in the case of prosthesis or
implant), whereas it refers to the duration of hospital or ward stay
for other infections.
HCAI incidence density
Number of infection episodes per 1000 patient-days or
device-days.
Developed countries
High-income countries according to the World Bank classifica-
tion 2009.6
Developing countries
Low- and middle-income countries according to the World Bank
classification 2009.6
© WHO
© WHO
5
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
1.
Health care-associated infection in different
settings and risk factors
HCAI is defined as: “An infection occurring in a patient during The term “HCAI” has replaced the former ones used to refer
the process of care in a hospital or other health-care facility to such infections, i.e. “nosocomial” or “hospital” infection, as
which was not present or incubating at the time of admission. evidence has shown that this event can affect patients in any
This includes infections acquired in the hospital, but appearing settings where they receive care. Only scanty data exist on the
after discharge, and also occupational infections among staff burden of HCAI outside hospitals because the culture of infection
of the facility”.7 Given this definition and before focusing on prevention and control and the systems for the surveillance
epidemiological data, it is important to scrutinize the issue of of these events are inexistent or poorly developed in these
HCAI in depth, to identify how it can be related to different types settings. For instance, many patients probably acquire respiratory
of health-care settings, and to determine the factors leading infections while seeking care for other diseases and waiting in
to an increased risk of transmission of health care-associated ambulatory care facilities, especially in overcrowded settings in
pathogens and of infection onset. developing countries, or during epidemic periods. As the patient
returns to the community, it is almost impossible to identify the
Most studies reporting data on the burden of endemic HCAI were occurrence of an infection acquired while accessing a primary
conducted in acute-care settings and in high-income countries. care facility. Although no systematic data are available on the
However, an increasing body of evidence has highlighted the epidemiology of HCAI in primary and secondary care, the need
epidemiological differences in non-acute care settings and in low- for a targeted approach to infection control in these settings
and middle-income countries. The modern evidence-based has been highlighted 8 and specific recommendations have been
approach to infection prevention and control clearly emphasizes issued in some countries, e.g. in England.9
that no type of health-care facility in any country can claim to be Home care has also become highly prevalent. For example, in
free from the risk of HCAI. 1996 in the USA, 8 million patients received care at home; of
these, 774 113 had at least one indwelling medical device, mostly
intravascular.10 HCAI is no longer restricted to basic hospital care
as in the past and now requires the implementation of specific
infection control measures in other settings.
© WHO
6
1. health care-associated infection IN DIFFERENT SETTINGS AND RISK FACTORS
© WHO
resident living in these facilities develops one to three infections two or more underlying diseases.19-28 Although not demonstrated
per year on average, most frequently urinary tract infection (UTI) as independent risk factors, general barriers to optimal infection
and pneumonia. It was also demonstrated that the onset of control practices in low- and middle-income countries are lack of
infection represents the most common cause of hospital admission financial support, inadequate numbers of trained personnel working
and death for residents in long-term care facilities, mainly from in infection control, understaffed hospital units, and insufficient
pneumonia.12,13 equipment and supplies.3
7
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
2.
Methods and challenges of health
care-associated infection surveillance
Most HCAIs become evident 48 hours or more following admission as health-care workers, visitors, patient care equipment, medical
(typical incubation period).5 Infection may present also after patient devices, or the health-care environment. HCAIs are not restricted
discharge. In these cases, the patient has become colonized or only to patients; health-care workers, ancillary staff, and visitors can
infected while in hospital, but the pathogen incubation period also be affected.
exceeds the patient’s hospital stay. For instance, several studies
report that over 50% of surgical site infections (SSI) manifest post- HCAIs occur both as part of an endemic (ongoing) trend within a
discharge.29-38 health-care facility or as epidemic situations, i.e. when new cases in
a given population and during a given period substantially exceed
HCAI may be caused by infectious agents from endogenous or what is expected, based on local endemic data. The endemic
exogenous sources. Endogenous sources are body sites, such situation and occurrence of outbreaks in a health-care setting
as the skin, nose, mouth, gastrointestinal tract, or vagina, that are are important indicators of the quality and safety of patient care.
normally colonized by local microbial flora. These microorganisms For this reason, surveillance is at the heart of infection prevention
can become invasive under certain favourable conditions and/or and control. Surveillance is defined as “the ongoing, systematic
cause infection when they contaminate sterile sites. Transmission collection, analysis, and interpretation of health data essential
to these sites occurs most frequently via health-care workers’ to the planning, implementation and evaluation of public health
hands.39 Exogenous sources are those external to the patient, such practice, closely integrated with the timely dissemination of these
© WHO
8
2. Methods and challenges of health care-associated infection surveillance
data to those who need to know”.40 Surveillance activities are an these systems are usually lacking, medical and nurse records are
essential tool to reduce HCAI as they are the important first step in often not well organized and detailed, and access to laboratory and
identifying problems and priorities. Furthermore, it has been shown radiological facilities is very limited and frequently of low quality. In
that conducting prospective surveillance activities, especially if addition, in low- and middle-income countries, a lack of expertise
prolonged, help to raise awareness of the problem and, finally, to in the field of infection prevention and control, understaffing,
decrease infection rates.41-43 overcrowding, and limited financial resources constitute real
constraints to HCAI surveillance performance.
The use of standardized definitions is crucial to the reliability of
HCAI surveillance. These allow to establish that the infection HCAI surveillance is a challenging task also because it requires a
was acquired during hospital stay, to ascertain that the condition particular expertise after obtaining epidemiological data to assess the
is a true infection and not a colonization (i.e. the presence of quality of the information produced, and to interpret its meaning and
microorganisms on skin or mucous membranes, in open wounds, or root cause in order to tailor intervention and prevention measures.
in excretions/secretions, but without any overt adverse clinical signs The establishment and maintenance of surveillance encompasses
or symptoms) or contamination (i.e. the exceptional and accidental various steps including specific components (Table 2.1).
presence of microorganisms in normally sterile body sites or
fluids that does not reflect actual infection status), and to define
the type of infection according to the body site. The most reliable Table 2.1
definitions are those issued by the USA National Nosocomial Main steps and components of a HCAI surveillance system
Infections Surveillance (NNIS) system and recently revised by the
National Healthcare Safety Network (NHSN) 5. The application Surveillance steps Components
of standardized definitions is one of the minimum requirements
for data comparisons at local, national, and international levels, 1. Planning • Assessment of available expertise,
although other variables need to be taken into account to allow facilities and resources.
appropriate benchmarking. • Identification of specific objectives,
scope, and methods, according to
the local reality.
• Selection of standardized definitions
and preparation of surveillance
protocols.
9
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
A few days later, the patient developed neck oedema and sep-
tic thrombosis of the left internal jugular, subclavian, and axillary
veins was diagnosed. Intravenous rifampin was added to the pre-
vious antibiotic therapy and a trans-oesophageal echocardiog-
raphy was performed to exclude endocarditis. The examination
proved negative. After three weeks of antibiotic therapy, the pa-
tient developed vaginal candidiasis that was treated with topical
antifungal drugs.
10
2. Methods and challenges of health care-associated infection surveillance
The patient was at risk because she probably developed • extensive vascular complications occurred (septic thrombosis
immunosuppression due to long-term corticosteroid treatment. She of jugular, subclavian, and axillary veins);
was found to be colonized by MRSA and underwent standard topical • an invasive diagnostic procedure was performed to exclude
eradication treatment, but she remained positive at first follow-up. endocarditis (trans-oesophageal echocardiography);
She subsequently developed signs of infection following insertion of • an additional surgical intervention was required to remove the
PAC: fever >38°C; inflammatory syndrome; and signs of a localized PAC;
infection (purulent discharge of the catheter insertion site). • there was a need for long-term antibiotic treatment;
• multiple peripheral venous lines and one central venous line
The following criteria indicated that the patient developed a deep were inserted for supportive and antibiotic therapy;
surgical site infection associated with catheter-related bacteraemia: • vaginal mycosis occurred due to prolonged antibiotic therapy;
• an infection occurring 30 days following a surgical procedure; • there was a delay in the treatment of the pulmonary cancer;
• purulent discharge at the PAC insertion site; • the patient (mother of three children) was hospitalized and
• deliberate opening of the PAC insertion site and PAC removal away from home for 35 days.
by the surgeon;
• positivity of the purulent secretions, blood cultures and cath-
eter tip for the same microorganism (MRSA).
© WHO
11
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
3.
The burden of endemic health care-associated
infection in high-income countries
National HCAI surveillance systems exist in several high-income Germany, and Japan, have coordinated surveillance at national or
countries and data are usually available through national reports state level. Our literature review on high-income countries identified
and/or nationwide, or multicentre studies published in the scientific 55 studies with a national scope, mostly conducted in countries
literature (Figure 3.1). According to our review, 131 national or with a national surveillance system in place.
multicentre studies conducted in 23 high-income countries were
published from 1995 to 2010. The European Centre for Disease In national and multicentre studies identified, the prevalence of
Prevention and Control (ECDC) reported that 13/28 (46.4%) hospitalized patients who acquired at least one HCAI ranged from
European high-income countries had national surveillance systems 3.5%47 to 12%48 (Figure 3.2). Pooled HCAI prevalence obtained
in place in 2008 to monitor either ICU-acquired infections, SSI, or through meta-analysis from studies conducted in mixed patient
both, and were regularly reporting to the Hospitals in Europe Link populations was 7.6 episodes per 100 patients (95% CI 6.9-8.5) and
for Infection Control through Surveillance (HELICS) network.46 In the 7.1 affected patients per 100 patients (95% CI 6.5-7.8).14-18,47-75 HCAI
USA, more than 3000 health-care facilities regularly report data on prevalence figures reported in the most recent studies available
ICU-acquired infections to the NHSN ( http://www.cdc.gov/nhsn/), from high-income countries are shown in Figure 3.3.
established by the Centers for Disease Control and Prevention
(CDC). Other high-income countries, such as Australia, France,
Figure 3.1
Number of national and multicentre studies reporting health care-associated infection in high-income coutries, 1995-2010
6 - 10 6 - 10
12
3. THE BURDEN OF ENDEMIC health care-associated infection IN HIGH-INCOME COUNTRIES
Figure 3.2
Health care-associated infection prevalence in high-income countries versus low- and middle-income countries, 1995-2010
20
Infections or infected patients (per 100 patients)
15
10
5
0
Inf/100 pts Inf pts/100 pts Inf/100 pts Inf pts/100 pts
Figure 3.3
Prevalence of health care-associated infection in high-income coutries, 1995-2010*
Canada
11.6%
Slovenia
4.6%
France
4.4%
Spain Italy
8.1% 6.7%
Greece
7.9%
* For countries with more than one study, the most recent figures are included.
13
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
The ECDC reported that approximately 4 131 000 patients are The HCAI burden is much more severe in high-risk populations,
affected by about 4 544 100 episodes of HCAI every year in Europe, such as patients admitted to ICUs, burn and transplant patients,
with a mean HCAI prevalence of 7.1%.76 The estimated HCAI and neonates. According to a recent European multicentre study,
incidence rate in the USA was 4.5% in 2002, corresponding to 9.3 the proportion of infected patients in the ICU can be as high as
infections per 1000 patient-days and 1.7 million affected patients.77 51%; most of these are health care-associated.89 In high-income
In the USA and Europe, UTI was the most frequent type of infection countries, approximately 30% of ICU patients are affected by at
hospital-wide (36% and 27%, respectively).76,77 In the USA, this was least one episode of HCAI with substantial associated morbidity
followed by SSI (20%), bloodstream infection (BSI), and pneumonia and mortality.90 Based on large studies from USA and Europe
(both 11%).77 In Europe, the second most frequent type was lower included in our review, HCAI incidence density ranged from 13.0
respiratory tract infection (24%), followed by SSI (17%), and BSI to 20.3 episodes per 1000 patient-days (Figure 3.4) and pooled
(10.5%).76 According to several studies, the frequency of SSI varies cumulative incidence was 17.0 episodes per 1000 patient-days
between 1.2% and 5.2% in high-income countries.43,44,77-88 in adult high-risk patients in industrialized countries (Table 3.1
and Figure 3.4).77,91-94 High frequency of infection is associated
with the use of invasive devices, in particular central lines, urinary
catheters, and ventilators. In a report from the USA NNIS system,
• 13/28 (46.4%) European high-income countries 83% of episodes of hospital-acquired pneumonia were associated
reporting either ICU-acquired infections, SSI, or both, to with mechanical ventilation, 97% of UTIs occurred in catheterized
the HELICS network in 2008. patients, and 87% of primary BSI in patients with a central line.93
• HCAI pooled prevalence in mixed patient populations in Among adult ICU patients in high-income countries, pooled
high-income countries: 7.6%. cumulative incidence densities of catheter-related BSI (CR-BSI),
• More than 4 million patients affected by HCAI every urinary catheter-related UTI (CR-UTI), and ventilator-associated
year in Europe; 1.7 million affected patients in USA. pneumonia (VAP) were 3.5 (95% CI 2.8-4.1) per 1000 CL-days,95-110
• Frequency of SSI varies between 1.5% and 5.2% in 4.1 (95% CI 3.7-4.6) per 1000 urinary catheter-days,98-110 and 7.9
high-income countries. (95% CI 5.7-10.1) per 1000 ventilator-days,98-111 respectively (Table
• In high-income countries, approximately 30% of ICU 3.1 and Figure 3.4). Comparisons with data available from the
patients are affected by at least one episode of HCAI. NHSN system109 and the German hospital infection surveillance
system (Krankenhaus Infektions Surveillance System [KISS])112
Figure 3.4
Incidence of overall health care-associated infection and device-associated infection in high-risk adult patients in high-income
countries, 1995-2010
15
10
5
0
14
3. THE BURDEN OF ENDEMIC health care-associated infection IN HIGH-INCOME COUNTRIES
highlight that these pooled values are similar, although slightly in our review,16-18,48,51,56,57,62,65,66,71,125 E. coli (20.1%) and S. aureus
higher. On average, VAP is the most frequent type of infection (17.8%) were the most frequent single pathogens causing HCAI in
in the ICU (32%), followed by CR-UTI and CR-BSI (both 20%), mixed patient populations, thus reflecting the fact that UTI and SSI
according to studies included in our review.91-96,98-111,113-118 are the most common types of infection encountered. Other key
pathogens were: Pseudomonas spp. (11.5%), enterobacteriaceae
Very low birth weight (<1500g) neonates requiring intensive care (10.6%); Candida spp. (6.7%); enterococci (6.5%); Acinetobacter
are a population at high risk for HCAI. Data from recent multicentre spp. (5.8%); and coagulase-negative staphylococci (5.3%).
studies conducted in Canada and Germany reported that 23.5%
and 12.3% of patients are affected, respectively.119,120 Lower HCAI
rates are reported in paediatric ICUs. For instance, in the USA,
HCAI incidence in this patient population was reported to be
5.7%.121 Device-associated infection densities were 1.8 episodes
per 1000 ventilator-days, 3 episodes per 1000 CL-days, and 4.2
episodes per 1000 urinary catheter-days, for VAP, CR-BSI, and
CR-UTI, respectively.109
Table 3.1
Pooled cumulative incidence density of HCAI and device-associated infection in adult ICU patients in high-, middle- and low-income
countries.
Surveillance HCAI/ 1000 Patient days CR-BSI/ Catheter-days CR-UTI/ Urinary VAP/ 1000 Ventilator-days
networks/reviews, patient-days 1000 central 1000 urinary catheter-days ventilator days
study period, country (95% CI) line days catheter days (95% CI)
(95% CI) (95% CI)
NHSN, 2006–2008, / / 2.1 699 300 3.4 546 824 2.9 383 068
USA#109
KISS, 2004-2009, / / 1.3 4 002 108 2.0 4 757 133 5.1 2 391 381
Germany112
Systematic review, 17.0 32 537 324 3.5 5 339 322 4.1 13 614 567 7.9 5 339 322
high-income (14.2-19.8) (2.8-4.1) (3.7-4.6) (5.7-10.1)
countries 1995-2010*
INICC, 2003–2008, / / 7.4 362 882 6.1 403 545 14.7 275 111
25 developing
countries†158
Systematic review, 42.7 193 139 12.2 891 220 8.8 970 710 23.9 679 950
low- and middle- (34.8-50.5) (10.5-13.9) (7.4-10.3) (20.7-27.1)
income countries
(1995-2010)*
HCAI = health care-associated infection; CR-BSI = catheter-related bloodstream infection; CR-UTI = catheter-related urinary tract infection; VAP = ventilator-
associated pneumonia; NHSN = National Healthcare Safety Network; KISS=Krankenhaus Infektions Surveillance System; INICC=International Nosocomial Infection
Control Consortium.
15
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
4.
The burden of endemic health care-associated infection
in low- and middle-income countries
While HCAI surveillance systems are in place at national/sub- The Clean Care is Safer Care team of WHO Patient Safety, in
national level in many developed countries, only 23 developing collaboration with the University of Geneva Hospitals, recently
countries (23/147 [15.6%]) reported a functioning national published a systematic review and meta-analysis on the endemic
surveillance system, according to a survey conducted by the WHO burden of HCAI in developing countries.3 Data included in this
First Global Patient Safety Challenge (Clean Care is Safer Care; report represent an update of this work. In our review, covering the
http://www.who.int/gpsc/en/) in 2010. As highlighted in section 2, period from 1995 to 2010 (Box 1), 276 papers included relevant
HCAI surveillance is a highly demanding and challenging task and information on the epidemiology of the four most frequent types of
settings with limited resources experience many constraints to HCAI (SSI, UTI, BSI, health-care associated pneumonia [HAP]/VAP)
evaluate the burden of HCAI. In low- and middle-income countries, in low- and middle-income countries. Only 46% (126/276) met the
regular monitoring of HCAI occurrence may be unfeasible at criteria usually defining high-quality epidemiological studies (Box 1).
national level and, thus, Ministries of Health are unable to report
information on the burden of HCAI. In addition, a limited number A review of countries where studies were performed and regional
of studies in these settings have been published in the scientific coverage revealed clearly an extremely fragmented picture of the
literature. endemic burden of HCAI in the developing world, with very scanty
Figure 4.1
Number of studies* reporting health care-associated infection in low- and middle-income coutries, 1995-2010
6 - 10 6 - 10
* Studies with any scope (i.e. conducted at the unit, facility, multicenter, or national level) are included.
16
4. THE BURDEN OF ENDEMIC health care-associated infection IN LOW- AND MIDDLE-INCOME COUNTRIES
information available from some regions (particularly Africa and programme of the International Nosocomial Infection Control
the Western Pacific) (Figure 4.1). However, even in regions where Consortium (INICC) (http://www.inicc.org/) is of great assistance
overall more studies were conducted and published (Europe to help bridge some of the gaps and to gauge the extent of the
and the Americas), several countries are covered by several problem. This fast-growing network coordinates data collection on
reports, whereas others are not represented by any published device-associated infections in several low- and middle-income
surveillance study (Figure 4.1). Brazil, India, Mexico, Thailand, and countries and has published already four international studies158,170-173
Turkey were identified as the countries with the highest number and many reports from individual countries or facilities.137,139,144,147,174,175
of studies. Only nine studies from four countries (Cuba, Mexico,
Thailand, and Turkey) were conducted at national level.20,25,126-132 Many studies conducted in health-care settings with limited
An additional 39 multicentre studies were reported from different resources reported HCAI rates higher than in developed countries.
countries, either conducted in multiple hospitals in one city or in Hospital-wide prevalence of HCAI varied from 5.7% to 19.1%
a country territory.38,133-169 According to our review, 66% (97/147) (Figures 3.2 and 4.2) with a pooled prevalence of 10.1 per 100
of developing countries have no published data at all. The limited patients (95% CI 8.4-12.2) and most studies reported proportions
number of studies with a broad scope, together with the lack of of infected patients higher than 10%; the pooled prevalence
national surveillance systems, significantly hamper any attempts to of affected patients was 10.2 per 100 patients (95% CI 9.0-
estimate the burden of HCAI at country or regional level in low- and 13.0).25,27,126,128-130,149,157,164,166,167,169,176-188 Of note, it was calculated that
middle-income countries. Studies from single hospitals cannot be the pooled HCAI prevalence was significantly higher in high- than
considered representative of the endemic epidemiology of HCAI in in low-quality studies (15.5% vs 8.5%, respectively).3 Similarly, the
a country. In particular, most studies were conducted in teaching/ proportion of infected patients was higher in high-quality studies
university hospitals (144/276 [52.2%]), which represent a specific (13.5% vs 7.2%).3 The most frequent type of infection in these mixed
type of context and not the broad range of health-care settings patient populations was SSI (29.1%), followed by UTI (23.9%), BSI
in place in countries. Most importantly, the HCAI surveillance (19.1%), HAP (14.8%), and other infections (13.1%).3
Figure 4.2
Prevalence of health care-associated infection in low- and middle-income coutries, 1995-2010
Latvia
5.7%
Lithuania
9.2%
Mongolia
5.4%
Serbia
17.4%
Morocco
17.8% Albania
Cuba 19.1% Turkey
7.3% 12.5%
Lebanon
Ghana Islamic 6.8%
6.7% Republic Thailand
of Iran 6.5%
8.8% Malaysia
14%
United
Republic
Brazil Senegal Mali Tunisia of Tanzania Indonesia
14% 10.9% 18.7% 17.9% 14.8% 7.1%
17
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
18
4. THE BURDEN OF ENDEMIC health care-associated infection IN LOW- AND MIDDLE-INCOME COUNTRIES
Figure 4.3
Incidence of overall health care-associated infection and device-associated infection in high-risk patients in low- and
middle-income countries, 1995-2010
100
50
40
30
20
10
0
19
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
5.
The impact of health care-associated infection
worldwide
The burden of HCAI worldwide needs to be highlighted not only care professionals. The case of a 13-year-old patient illustrates the
because of the large number of patients affected every year, but incredible long-term suffering, pain. and fear that one HCAI can
also for its significant impact in terms of excess costs, prolonged cause (Patient case story).
hospital stay, attributable mortality, and other complications.
Data on these important indicators are difficult to retrieve as they
Core evidence available from high-income countries
require complex evaluation, particularly to confirm that they are
directly linked to HCAI episodes and not to other factors. Methods Overall estimates of HCAI impact are available for some high-
of recording and filing patient clinical data vary worldwide, with income countries and help understand the magnitude of its
a limited availability of electronic-based systems in developing consequences. European estimates indicate that HCAIs cause 16
countries. Health-care financial systems also differ with a broad million extra-days of hospital stay and 37 000 attributable deaths
range of payer sources (e.g. a governmental agency, private annually, but also contribute to an additional 110 000 deaths.76
insurance company, or even the patients themselves) and local
charges, thus leading to complex estimates and calculations The burden of HCAI is also reflected in significant financial losses.
of costs and potentially limiting inter-hospital and international According to a report from the ECDC, these infections account
comparisons. for approximately € 7 billion per year, including direct costs only.76
Recent national estimates from Belgium showed that about 900
Similar to many other adverse events experienced by patients 000 bed-days are complicated every year by at least one episode
while seeking health care, HCAIs lead to added suffering and the of HCAI.52 Similar dramatic figures were reported in the USA and
psychological and financial burden to patients. Given that HCAI is around 99 000 deaths were attributed to HCAI in 2002.77 Of these,
inherently linked to health-care workers’ behaviour (e.g. sub-optimal approximately 36 000 were due to pneumonia, 31 000 to BSI, 13
hand hygiene practices) and, in some cases, to health-care system 000 to UTI, 8 200 to SSI, and 11 062 to other infections. The annual
gaps (e.g. lack of adequate equipment), this burden translates into economic impact of HCAI in the USA was approximately US$ 6.5
a profound frustration and loss of trust in the system and health- billion in 2004.77
20
5. THE IMPACT OF health care-associated infection WORLDWIDE
In studies mainly conducted in high-income countries, crude burden of HCAI in terms of mortality, costs and increased length of
mortality rates associated with HCAI vary from 12% to 80%, stay in health-care settings.20,22,24-28,126,133,135,138,139,142-146,148, 158,160,164,170,175,
depending on the patient population.90 As mentioned previously, 177,180,189,190,193,195,206,208,210,211,214-216,218,224,226,227,230,232,233,235,237,238,239,253-292
estimating the excess mortality due to HCAI is challenging, However, in most cases, only crude mortality rates in patients
especially in high-risk patients who are at greater risk of death affected by HCAI were reported, without taking into account other
because of severe underlying diseases. For example, Soufir and risk factors or major confounders, or by comparing these with non-
colleagues247 reported that crude mortality rates were significantly infected patients. Thus, no conclusions can be drawn on the risk
higher in critically-ill patients affected by CR-BSI compared to of death actually attributable to HCAI. Several studies reported
those non-affected (50% vs 21%, respectively). When adjusting for significantly higher mortality in infected patients, in particular in
admission prognostic factors, infection remained associated with paediatric and adult ICUs.133,135,139,194,211,216,261,269,273,277 According to
mortality, but not after taking into account severity scores before the 2003-2008 INICC report related to 173 ICUs in Latin America,
infection onset. Several additional studies brought controversial Asia, Africa, and Europe, crude excess mortality in adult patients
results, some corroborating the hypothesis that HCAI patients are was 18.5%, 23.6% and 29.3%, for CR-UTI, CR-BSI and VAP,
at higher risk of death. Among these, a prevalence study conducted respectively.158 Increased length of stay associated with HCAI varied
in 17 Western European countries showed that clinical sepsis, between 5 and 29.5 days.22,24,126,133,135,139,143,160,175,189,193,194,206,210,211,214-
pneumonia, and BSI were all independently associated with an 216,218,230,237-239,253,257,260,265,267,274,282,283,289,290,292,293
Very limited data are available at the national level to assess the
impact of HCAI in low- and middle-income countries. Conversely,
an increasing body of information has been published at the
institutional level. We identified 89 studies reporting data on the
21
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
6.
Lessons learned and the way forward
By mapping and scrutinizing the studies in the scientific literature, Interestingly, UTI, especially related to urinary catheter use, is
a global picture of the endemic burden of HCAI can be captured the most frequent infection detected hospital-wide in mixed
for the first time with compiled data from many countries and, patient populations in high-income countries. However, this type
importantly, an assessment of differences between high-, low- of infection has usually less severe consequences than other
and middle-income countries. The key finding is that the burden device-associated infections in terms of attributable mortality,
of HCAI worldwide is very high in terms of morbidity, mortality, related complications, and associated costs. Conversely, in low-
extra-costs, and other outcome indicators. This is particularly and middle-income countries, SSI is the most frequent HCAI and
true for developing countries where awareness of the problem affects up to one-third of operated patients. Frequencies reported
remains extremely limited, and because other health priorities take for SSI are probably largely underestimated as, according to some
precedence over patient safety considerations. studies, most are detected through post-discharge surveillance,
which is very difficult to perform in developing countries.32-38 SSI
Of every 100 hospitalized patients at any given time, 7 and 10 of can prolong hospital stay up to 21 days in settings with limited
them will acquire a HCAI in developed and developing countries, resources. 230 In addition, it can bring a huge burden in terms of
respectively. According to high-quality studies, this proportion medium-term sequelae, personal suffering for the patient, and
increases to 15 per 100 patients in developing countries.3 HCAI additional financial costs.
is more frequent in critically-ill patients admitted to ICUs. In this
patient population, the increased risk in settings with limited With regard to data availability, this report shows that information
resources is particularly disturbing with an overall frequency at the national level is regularly provided by several national
of infection as high as 42.7 episodes per 1000 patient-days in surveillance systems and international networks in high-income
developing countries vs 17.0 episodes per 1000 patient-days in countries. By contrast, very few national studies are available
industrialized countries. Furthermore, in these high-risk settings, from low- and middle-income countries and the vast majority has
incidence densities of infections associated with the use of no regular HCAI reporting system in place. Furthermore, even
invasive devices (central vascular lines, ventilators and urinary when considering studies related to single institutions, data are
catheters) are on average at least three-fold higher in low- and not available for many developing countries and some regions are
middle-income than in high-income countries (Figures 3.4 and poorly represented overall (Figure 4.1).
4.3). Pooled incidence density of CR-BSI and VAP in some
developing countries were even shown to be up to 19 and 16 Although national figures on the burden of HCAI are available only
times higher than those reported from Germany and the USA.3 for a few countries, based on data from Europe and the USA, it
Newborns are also at higher risk of acquiring HCAI, with infection can be estimated that hundreds of millions of patients suffer from
rates in developing countries three to 20 times higher than in high- HCAI every year worldwide. However, it is important to note that
income countries. 205 infections acquired by health-care workers, data on outbreaks
and blood-borne pathogens transmitted through transfusion,
contaminated injections, and other procedures are not included in
these estimates. For this reason, and because of reporting gaps
even when surveillance systems are in place, the burden of HCAI is
certainly greatly underestimated.
22
6. LESSONS LEARNED AND THE WAY FORWARD
definitions; lack of expertise and dedicated personnel; and the in these settings, awareness and knowledge of HCAI are often poor,
overall lack of financial resources to invest in this field. Further and well-known, evidence-based, infection prevention and control
research is very much needed to identify mathematical models strategies could be enforced and implemented more effectively.
in order to obtain more predictive global estimates of HCAI.
Although these should be partly based on findings from published In developing countries, the nature of this problem is partially
epidemiological reports, the reliability of the study results must different because, in addition to general determinants similar to
be considered as the quality can be very poor, particularly high-income countries, a combination of numerous unfavourable
those conducted in developing countries. In addition, minimum factors play an important role to increase the risk of HCAI. These
requirements and standards should be set to allow countries to are much more inherent to the situation and reality of these
establish robust surveillance systems and report national figures. countries, such as poor hygiene and sanitation, lack or shortage of
Case definitions need to be homogenized, together with the method basic equipment, inadequate infrastructures, unfavourable social
of calculating the denominator, e.g. calculation of days at-risk until background, and a population largely affected by malnutrition and
the first infectious episode or for the entire period of hospitalization. other types of infection and/or diseases.
Adaptation of definitions to make HCAI detection more feasible in
settings with limited resources should be considered and validated Data from this report highlighting the serious burden of HCAI bring
through scientifically sound investigations. Standardization would strong evidence that these determinants, as well as surveillance
help to gather a more comprehensive picture and to optimize inter- issues, must be carefully assessed and tackled as much as
hospital and international comparisons. Ideally, countries should possible at all levels if any significant progress is to be made in
adopt definitions and methods used by prominent surveillance the future. Table 6.1 summarizes the most relevant actions and
networks, such as HELICS, NHSN, KISS and INICC. It would be also perspectives for the improvement of HCAI surveillance and control.
important to encourage these networks to join their efforts and use
the same definitions, and even to explore possibilities to merge their
data on a regular basis. Table 6.1
Key solutions and perspectives for improvement
Evaluation of the key determinants of HCAI burden is complex, but of HCAI surveillance and control
it remains an essential step to identify strategies and measures for
improvement. In advanced settings in high-income countries, HCAI Solutions and perspectives for improvement
may occur as a potentially expected adverse event of sophisticated
care techniques and treatments typical of modern medicine. • Identifying local determinants of the HCAI burden.
However, it is also evident that frequently it represents a health-care • Improving reporting and surveillance
delivery system failure. Despite the broader availability of resources systems at the national level.
• Ensuring minimum requirements in terms of
facilities and dedicated resources available
for HCAI surveillance at the institutional level,
including microbiology laboratories’ capacity.
• Ensuring that core components for infection control are
in place at the national and health-care setting levels.
• Implementing standard precautions, particularly
best hand hygiene practices at the bedside.
• Improving staff education and accountability.
• Conducting research to adapt and validate surveillance
protocols based on the reality of developing countries.
• Conducting research on the potential involvement of
patients and their families in HCAI reporting and control.
23
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
24
25
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
REFERENCES
1. Bates DW et al. Global priorities for patient 15. Maugat S, Carbonne A, Astagneau P. 27. Dia NM et al. [Prevalence of nosocomial
safety research. British Medical Journal, 2009, [Significant reduction of nosocomial infectious: infections in a university hospital (Dakar,
338:b1775. stratified analysis of prevalence national studies Senegal)]. Médecine et Maladies Infectieuses,
performed in 1996 and 2001 in French north 2008, 38:270–274.
2. Burke JP. Infection control - a problem for
interegion]. Pathologie Biologie (Paris), 2003,
patient safety. New England Journal of 28. Cevik MA et al. Relationship between
51:483–489.
Medicine, 2003, 348:651–656. nosocomial infection and mortality in a
16. Kritsotakis EI et al. Case-mix adjustment neurology intensive care unit in Turkey.
3. Allegranzi B et al. Burden of endemic health
approach to benchmarking prevalence rates Journal of Hospital Infection, 2005, 59:324–330.
care-associated infection in developing
of nosocomial infection in hospitals in Cyprus
countries: systematic review and meta-analysis. 29. Fernandez-Ayala M et al. Surgical site infection
and Greece. Infection Control and Hospital
Lancet, 2011, 377:228–241. during hospitalization and after discharge in
Epidemiology, 2008, 29:685–692.
patients who have undergone cardiac surgery.
4. The global burden of disease: 2004 update.
17. Klavs I et al. Prevalence of and risk factors Infection Control and Hospital Epidemiology,
Geneva, World Health Organization, 2008.
for hospital-acquired infections in Slovenia – 2006, 27:85–88.
5. Horan TC, Andrus M, Dudeck MA. CDC/NHSN results of the first national survey, 2001.
30. Huenger F et al. Evaluation of postdischarge
surveillance definition of health care-associated Journal of Hospital Infection, 2003, 54:149–157.
surveillance of surgical site infections after total
infection and criteria for specific types of
18. Lanini S et al. Healthcare-associated infection hip and knee arthroplasty. American Journal of
infections in the acute care setting. American
in Italy: annual point-prevalence surveys, Infection Control, 2005, 33:455–462.
Journal of Infection Control, 2008, 36:309–332.
2002-2004. Infection Control and Hospital
31. Mitt P et al. Surgical-site infections following
6. World Bank list of economies. Washington, DC, Epidemiology, 2009, 30:659–665.
cesarean section in an Estonian university
The World Bank, 2009.
19. de Gentile A et al. Nosocomial infections in a hospital: postdischarge surveillance and
7. Prevention of hospital-acquired infections: children’s hospital in Argentina: impact of a analysis of risk factors. Infectiont Control and
a practical guide. Geneva, World Health unique infection control intervention program. Hospital Epidemiology, 2005, 26:449–454.
Organization, 2002:64. Infection Control and Hospital Epidemiology,
32. Oliveira AC, Carvalho DV. Postdischarge
2001, 22:762–766.
8. Cole M. Infection control: worlds apart surveillance: the impact on surgical site
primary and secondary care. British Journal of 20. Avila-Figueroa C et al. [Prevalence of infection incidence in a Brazilian university
Community Nursing, 2007, 12:301,303–306. nosocomial infections in children: survey of 21 hospital. American Journal of Infection Control,
hospitals in Mexico]. Salud Pública de México, 2004, 32:358–361.
9. Pellowe CM et al. Evidence-based guidelines
1999, 41(Suppl. 1):S18–S25.
for preventing healthcare-associated infections 33. Santos KR et al. Incidence surveillance of
in primary and community care in England. 21. Tapia-Rombo CA et al. Risk factors for wound infection in hernia surgery during
Journal of Hospital Infection, 2003, 55(Suppl. intrahospital infection in newborns. Archives of hospitalization and after discharge in a
2):S2–127. Medical Research, 2001, 32:304–311. university hospital. Journal of Hospital Infection,
1997, 36:229–233.
10. Manangan LP et al. Feasibility of national 22. Hajdu A et al. A point prevalence survey of
surveillance of health-care-associated hospital-acquired infections and antimicrobial 34. Wagner MB et al. Hospital-acquired infections
infections in home-care settings. Emerging use in a paediatric hospital in north-western among surgical patients in a Brazilian hospital.
Infectious Diseases, 2002, 8:233–236. Russia. Journal of Hospital Infection, 2007, Journal of Hospital Infection, 1997, 35:277–285.
66:378–384.
11. Moro ML et al. The burden of healthcare- 35. Ferraz EM et al. Postdischarge surveillance for
associated infections in European long-term 23. Pawa AK et al. Neonatal nosocomial infection: nosocomial wound infection: does judicious
care facilities. Infection Control and Hospital profile and risk factors. Indian Pediatrics, 1997, monitoring find cases? American Journal of
Epidemiology, 2010, 31(Suppl. 1):S59–S62. 34:297–302. Infection Control, 1995, 23:290–294.
12. Moro ML, Mongardi M, Marchi M. Healthcare- 24. Ben Jaballah N et al. [Epidemiology of 36. Giri BR et al. Surgical site infection and
related infections outside the hospital: nosocomial bacterial infections in a neonatal antibiotics use pattern in a tertiary care
a new frontier for infection control. New and pediatric Tunisian intensive care unit]. hospital in Nepal. Journal of Pakistan Medical
Microbiologica, 2007, 30:350–354. Médecine et Maladies Infectieuses, 2006, Association, 2008, 58:148–151.
36:379–385.
13. Eriksen HM et al. Healthcare-associated 37. Eriksen HM et al. Surgical-site infections at
infection among residents of long-term care 25. Izquierdo-Cubas F et al. National prevalence of Kilimanjaro Christian Medical Center. Journal of
facilities: a cohort and nested case-control nosocomial infections. Cuba 2004. Journal of Hospital Infection, 2003, 55:14–20.
study. Journal of Hospital Infection, 2007, Hospital Infection, 2008, 68:234–240.
38. Kasatpibal N et al. Risk of surgical site infection
65:334–340.
26. Sallam SA et al. Device-related nosocomial and efficacy of antibiotic prophylaxis: a cohort
14. Gravel D et al. Point prevalence survey for infection in intensive care units of Alexandria study of appendectomy patients in Thailand.
healthcare-associated infections within University Students Hospital. Eastern BMC Infectious Diseases, 2006, 6:111.
Canadian adult acute-care hospitals. Journal of Mediterranean Health Journal, 2005, 11:52–61.
Hospital Infection, 2007, 66:243–248.
26
REFERENCES
39. Pittet D et al. Evidence-based model for hand 54. Sartor C et al. Assessment of the value of 67. Durando P et al. Surveillance of hospital-
transmission during patient care and the role of repeated point-prevalence surveys for analyzing acquired infections in Liguria, Italy: results
improved practices. Lancet Infectious Diseases, the trend in nosocomial infections. Infection from a regional prevalence study in adult and
2006, 6:641–652. Control and Hospital Epidemiology, 2005, paediatric acute-care hospitals. Journal of
26:369–373. Hospital Infection, 2009, 71:81–87.
40. CDC surveillance update. Atlanta, GA, Centers
for Disease Control and Prevention, 1988. 55. van der Kooi TI et al. Prevalence of nosocomial 68. Emmerson AM et al. The second national
infections in The Netherlands, 2007-2008: prevalence survey of infection in hospitals-
41. Haley RW et al. The efficacy of infection
results of the first four national studies. Journal -overview of the results. Journal of Hospital
surveillance and control programs in preventing
of Hospital Infection, 75:168–172. Infection, 1996, 32:175–190.
nosocomial infections in U.S. hospitals.
American Journal of Epidemiology, 1985, 56. The French Prevalence Survey Study Group. 69. Reilly J et al. Results from the Scottish national
121:182–205. Prevalence of nosocomial infections in France: HAI prevalence survey. Journal of Hospital
results of the nationwide survey in 1996. Journal Infection, 2008, 69:62–68.
42. Schwab F et al. Reducing neonatal nosocomial
of Hospital Infection, 2000, 46:186–193.
bloodstream infections through participation 70. Golliot F et al. Nosocomial infections in geriatric
in a national surveillance system. Journal of 57. Pellizzer G et al. Prevalence and risk factors for long-term-care and rehabilitation facilities:
Hospital Infection, 2007, 65:319–325. nosocomial infections in hospitals of the Veneto exploration in the development of a risk index
region, north-eastern Italy. Infection, 2008, for epidemiological surveillance. Infection
43. Gastmeier P et al. Effectiveness of a nationwide
36:112–119. Control and Hospital Epidemiology, 2001,
nosocomial infection surveillance system for
22:746–753.
reducing nosocomial infections. Journal of 58. Vaque J, Rossello J, Arribas JL. Prevalence of
Hospital Infection, 2006, 64:16–22. nosocomial infections in Spain: EPINE study 71. Pittet D et al. Prevalence and risk factors
1990-1997. EPINE Working Group. Journal of for nosocomial infections in four university
44. Moro ML et al. Rates of surgical-site infection:
Hospital Infection, 1999, 43(Suppl.):S105–S111. hospitals in Switzerland. Infection Control and
an international comparison. Infection Control
Hospital Epidemiology, 1999, 20:37–42.
and Hospital Epidemiology, 2005, 26:442–448. 59. Vaque J et al. Nosocomial infections in Spain:
results of five nationwide serial prevalence 72. Eriksen HM, Iversen BG, Aavitsland P.
45. Mannien J et al. Impact of postdischarge
surveys (EPINE Project, 1990 to 1994). Prevalence of nosocomial infections in hospitals
surveillance on surgical site infection rates
Nosocomial Infections Prevalence Study in Norway, 2002 and 2003. Journal of Hospital
for several surgical procedures: results from
in Spain. Infection Control and Hospital Infection, 2005, 60:40–45.
the nosocomial surveillance network in The
Epidemiology, 1996, 17:293–297.
Netherlands. Infection Control and Hospital 73. Scheel O, Stormark M. National prevalence
Epidemiology, 2006, 27:809–816. 60. Sax H, Pittet D. [pour le comité de rédaction survey on hospital infections in Norway. Journal
de Swiss-NOSO et le réseau Swiss-NOSO of Hospital Infection, 1999, 41:331–335.
46. Annual epidemiological report on
Surveillance]. Résultats de l’enquête nationale
communicable diseases in Europe 2010. 74. Zotti CM et al. Hospital-acquired infections in
de prévalence des infections nosocomiales de
Stockholm, European Centre for Disease Italy: a region wide prevalence study. Journal of
2004 (snip04). Swiss-NOSO, 2005, 12:1–4.
Prevention and Control, 2010:1–185. Hospital Infection, 2004, 56:142–149.
61. Gikas A et al. Prevalence of nosocomial
47. Gastmeier P et al. Prevalence of nosocomial 75. Di Pietrantoni C, Ferrara L, Lomolino G.
infections after surgery in Greek hospitals:
infections in representative German hospitals. Multicenter study of the prevalence of
results of two nationwide surveys. Infection
Journal of Hospital Infection, 1998, 38:37–49. nosocomial infections in Italian hospitals.
Control and Hospital Epidemiology, 2004,
Infection Control and Hospital Epidemiology,
48. Nicholls TM, Morris AJ. Nosocomial infection 25:319–324.
2004, 25:85–87.
in Auckland Healthcare hospitals. New Zealand
62. Nicastri E et al. Prevalence of nosocomial
Medical Journal, 1997, 110:314–316. 76. Annual epidemiological report on
infections in 15 Italian hospitals: first point
communicable diseases in Europe 2008. Report
49. Thiolet J et al. Prevalence of nosocomial prevalance study for the INF-NOS project.
on the state of communicable diseases in
infections, France, 2006. Bulletin Infection, 2003, 31(Suppl. 2):10–15.
the EU and EEA/EFTA countries. Stockholm,
Epidémiologique Hebdomadaire, 2007, 51-
63. Smyth ET et al. Four country healthcare European Centre for Disease Prevention and
52:429–432.
associated infection prevalence survey 2006: Control, 2008.
50. Lizioli A et al. Prevalence of nosocomial overview of the results. Journal of Hospital
77. Klevens RM et al. Estimating health care-
infections in Italy: result from the Lombardy Infection, 2008, 69:230–248.
associated infections and deaths in U.S.
survey in 2000. Journal of Hospital Infection,
64. Sax H. [Nationwide surveillance of nosocomial hospitals, 2002. Public Health Reports, 2007,
2003, 54:141–148.
infections in Switzerland-methods and 122:160–166.
51. Lepoutre A et al. Deuxième enquête nationale results of the Swiss nosocomial infection
78. Rioux C, Grandbastien B, Astagneau P. The
de prévalence des infections nosocomiales, prevalence studies (SNIP) in 1999 and 2002].
standardized incidence ratio as a reliable tool
France, 2001: réseau d’alerte d’investigation et Therapeutische Umschau, 2004, 61:197–203.
for surgical site infection surveillance. Infection
de surveillance des infections nosocomiales. St
65. Lyytikainen O et al. Healthcare-associated Control and Hospital Epidemiology, 2006,
Maurice, Institut de veille sanitaire, 2005:11.
infections in Finnish acute care hospitals: a 27:817–824.
52. Gordts B et al. The 2007 Belgian national national prevalence survey, 2005. Journal of
79. Rioux C, Grandbastien B, Astagneau P. Impact
prevalence survey for hospital-acquired Hospital Infection, 2008, 69:288–294.
of a six-year control programme on surgical
infections. Journal of Hospital Infection, 2010,
66. Gikas A et al. Prevalence study of hospital- site infections in France: results of the INCISO
75:163–167.
acquired infections in 14 Greek hospitals: surveillance. Journal of Hospital Infection, 2007,
53. Floret N et al. Results from a four-year study planning from the local to the national 66:217–223.
on the prevalence of nosocomial infections surveillance level. Journal of Hospital Infection,
80. Gulacsi L et al. Risk-adjusted infection rates in
in Franche-Comté: attempt to rank the risk 2002, 50:269–275.
surgery: a model for outcome measurement in
of nosocomial infection. Journal of Hospital
hospitals developing new quality improvement
Infection, 2006, 63:393–398.
programmes. Journal of Hospital Infection,
2000, 44:43–52.
27
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
81. Petrosillo N et al. Surgical site infections in 95. Maugat S et al. [Standardized incidence 107. Edwards JR et al. National Healthcare Safety
Italian hospitals: a prospective multicenter ratio: a risk index for catheter-related Network (NHSN) report, data summary for
study. BMC Infectious Diseases, 2008, 8:34. infection surveillance in intensive care units 2006 through 2007, issued November 2008.
(REACAT network) in Northern France]. Revue American Journal of Infection Control, 2008,
82. Fiorio M et al. Incidence of surgical site
d’Epidémiologique et de Santé Publique, 2005, 36:609–626.
infections in general surgery in Italy. Infection,
53(Suppl. 1):S39–S46.
2006, 34:310–314. 108. Larson EL, Quiros D, Lin SX. Dissemination of
96. Gastmeier P, Weist K, Ruden H. Catheter- the CDC’s hand hygiene guideline and impact
83. Geubbels EL et al. An operating surveillance
associated primary bloodstream infections: on infection rates. American Journal of Infection
system of surgical-site infections in The
epidemiology and preventive methods. Control, 2007, 35:666–675.
Netherlands: results of the PREZIES
Infection,1999,27(Suppl. 1):S1–S6.
national surveillance network. [Preventie van 109. Edwards JR et al. National Healthcare Safety
Ziekenhuisinfecties door Surveillance.] Infection 97. Hansen S et al. National influences on catheter- Network (NHSN) report: data summary for
Control and Hospital Epidemiology, 2000, associated bloodstream infection rates: 2006 through 2008, issued December 2009.
21:311–318. practices among national surveillance networks American Journal of Infection Control, 2009,
participating in the European HELICS project. 37:783–805.
84. Gaynes RP et al. Surgical site infection (SSI)
Journal of Hospital Infection, 2009, 71:66–73.
rates in the United States, 1992-1998: the 110. Edwards JR et al. National Healthcare Safety
National Nosocomial Infections Surveillance 98. National Nosocomial Infections Surveillance Network (NHSN) report, data summary for
System basic SSI risk index. Clinical Infectious (NNIS) system report, data summary from 2006, issued June 2007. American Journal of
Diseases, 2001, 33(Suppl. 2):S69–S77. January 1992 through June 2003, issued Infection Control, 2007, 35:290–301.
August 2003. American Journal of Infection
85. Carlet J et al. French national program for 111. Suka M et al. Incidence and outcomes of
Control, 2003, 31:481–498.
prevention of healthcare-associated infections ventilator-associated pneumonia in Japanese
and antimicrobial resistance, 1992-2008: 99. Martone WJ et al. National Nosocomial intensive care units: the Japanese nosocomial
positive trends, but perseverance needed. Infections Surveillance (NNIS) semiannual infection surveillance system. Infection Control
Infection Control and Hospital Epidemiology, report, May 1995. A report from the National and Hospital Epidemiology, 2007, 28:307–313.
2009, 30:737–745. Nosocomial Infections Surveillance (NNIS)
112. Krankenhaus-Infektions-Surveillance-System
system. American Journal of Infection Control,
86. Astagneau P et al. Reducing surgical site (KISS). [Modul ITS-KISS-Referenzdaten-
1995, 23:377–385.
infection incidence through a network: results Berechnungszeitraum: Januar 2005
from the French ISO-RAISIN surveillance 100. National Nosocomial Infections Surveillance bis Dezember 2009.] Berlin, Nationales
system. Journal of Hospital Infection, 2009, (NNIS) system report, data summary from Referenzzentrum für Surveillance von
72:127–134. January 1992-April 2000, issued June 2000. nosokomialen Infektionen, 2010.
American Journal of Infection Control, 2000,
87. Szilagyi E et al. The national nosocomial 113. Réseau REA-Raisin. [Surveillance des
28:429–448.
surveillance network in Hungary: results of two infections nosocomiales en réanimation
years of surgical site infection surveillance. 101. National Nosocomial Infections Surveillance adulte. Résultats 2006.] Paris, Institut de veille
Journal of Hospital Infection, 2009, 71:74–80. (NNIS) system report, data summary from sanitaire, 2007:1–46.
January 1992 through June 2004, issued
88. Horwitz JR et al. Pediatric wound infections: 114. Malacarne P et al. Building a continuous
October 2004. American Journal of Infection
a prospective multicenter study. Annals of multicenter infection surveillance system in the
Control, 2004, 32:470–485.
Surgery, 1998, 227:553–558. intensive care unit: findings from the initial data
102. National Nosocomial Infections Surveillance set of 9,493 patients from 71 Italian intensive
89. Vincent JL et al. International study of the
(NNIS) system report, data summary from care units. Critical Care Medicine, 2008,
prevalence and outcomes of infection in
January 1992 to June 2002, issued August 36:1105–1113.
intensive care units. Journal of the American
2002. American Journal of Infection Control,
Medical Association, 2009, 302:2323–2329. 115. Malacarne P et al. Epidemiology of nosocomial
2002, 30:458–475.
infection in 125 Italian intensive care units.
90. Vincent JL. Nosocomial infections in adult
103. National Nosocomial Infections Surveillance Minerva Anestesiologica, 2010, 76:13–23.
intensive-care units. Lancet, 2003, 361:2068–
(NNIS) system report, data summary from
2077. 116. Suka M, Yoshida K, Takezawa J.
October 1986-April 1998, issued June 1998.
Epidemiological approach to nosocomial
91. Gikas A et al. Device-associated infections in American Journal of Infection Control, 1998,
infection surveillance data: the Japanese
the intensive care units of Cyprus: results of the 26:522–533.
nosocomial infection surveillance system.
first national incidence study. Infection, 2010,
104. National Nosocomial Infections Surveillance Environmental Health and Preventive Medicine,
38:165–171.
(NNIS) system report, data summary from 2008, 13:30–35.
92. Legras A et al. Nosocomial infections: January 1990-May 1999, issued June 1999.
117. Olaechea PM et al. Factors related to hospital
prospective survey of incidence in five French American Journal of Infection Control, 1999,
stay among patients with nosocomial infection
intensive care units. Intensive Care Medicine, 27:520–532.
acquired in the intensive care unit. Infection
1998, 24:1040–1046.
105. National Nosocomial Infections Surveillance Control and Hospital Epidemiology, 2003,
93. Richards MJ et al. Nosocomial infections in (NNIS) report, data summary from October 24:207–213.
combined medical-surgical intensive care units 1986-April 1996, issued May 1996. A report
118. National Nosocomial Infections Surveillance
in the United States. Infection Control and from the National Nosocomial Infections
(NNIS) system report, data summary from
Hospital Epidemiology, 2000, 21:510–515. Surveillance (NNIS) system. American Journal
January 1992-June 2001, issued August 2001.
of Infection Control, 1996, 24:380–388.
94. Richards MJ et al. Nosocomial infections in American Journal of Infection Control, 2001,
medical intensive care units in the United 106. National Nosocomial Infections Surveillance 29:404–421.
States. National Nosocomial Infections (NNIS) report, data summary from October
119. Aziz K et al. Variations in rates of nosocomial
Surveillance System. Critical Care Medicine, 1986-April 1997, issued May 1997. A report from
infection among Canadian neonatal intensive
1999, 27:887–892. the NNIS system. American Journal of Infection
care units may be practice-related. BMC
Control, 1997, 25:477–487.
Pediatrics, 2005, 5:22.
28
REFERENCES
120. Geffers C et al. Use of central venous catheter 133 Rosenthal VD et al. The attributable cost and 145. Wojkowska-Mach J et al. Hospital-acquired
and peripheral venous catheter as risk factors length of hospital stay because of nosocomial pneumonia in the intensive care units of Polish
for nosocomial bloodstream infection in very- pneumonia in intensive care units in 3 hospitals hospitals. Infection Control and Hospital
low-birth-weight infants. Infection Control and in Argentina: a prospective, matched analysis. Epidemiology, 2006, 27:784–786.
Hospital Epidemiology, 2010, 31:395–401. American Journal of Infection Control, 2005,
146. Danchaivijitr S et al. Effect of an education
33:157–161.
121. Richards MJ et al. Nosocomial infections in program on the prevention of ventilator-
pediatric intensive care units in the United 134. Rosenthal VD, Guzman S, Crnich C. Device- associated pneumonia: a multicenter study.
States. National Nosocomial Infections associated nosocomial infection rates in Journal of the Medical Association of Thailand,
Surveillance system. Pediatrics, 1999, 103:e39. intensive care units of Argentina. Infection 2005, 88(Suppl. 10):S36–S41.
Control and Hospital Epidemiology, 2004,
122. Gastmeier P et al. Risk factors for death due 147. Leblebicioglu H et al. Device-associated
25:251–255.
to nosocomial infection in intensive care hospital-acquired infection rates in Turkish
unit patients: findings from the Krankenhaus 135. Rosenthal VD, Guzman S, Orellano PW. intensive care units. Findings of the
Infektions Surveillance System. Infectiont Nosocomial infections in medical-surgical International Nosocomial Infection Control
Control and Hospital Epidemiology, 2007, intensive care units in Argentina: attributable Consortium (INICC). Journal of Hospital
28:466–472. mortality and length of stay. American Journal Infection, 2007, 65:251–257.
of Infection Control, 2003, 31:291–295.
123. De Rosa FG et al. SPIR01 and SPIR02: a two- 148. Esen S, Leblebicioglu H. Prevalence of
year 1-day point prevalence multicenter study 136. Rosenthal VD, Guzman S, Crnich C. Impact nosocomial infections at intensive care units in
of infections in intensive care units in Piedmont, of an infection control program on rates of Turkey: a multicentre 1-day point prevalence
Italy. New Microbiologica, 2008, 31:81–87. ventilator-associated pneumonia in intensive study. Scandinavian Journal of Infectious
care units in 2 Argentinean hospitals. American Diseases, 2004, 36:144–148.
124. Spencer RC. Predominant pathogens found
Journal of Infection Control, 2006, 34:58–63.
in the European Prevalence of Infection in 149. Azzam R, Dramaix M. A one-day prevalence
Intensive Care study. European Journal of 137. Salomao R et al. Device-associated infection survey of hospital-acquired infections in
Clinical Microbiology and Infectious Diseases, rates in intensive care units of Brazilian Lebanon. Journal of Hospital Infection, 2001,
1996, 15:281–285. hospitals: findings of the International 49:74–78.
Nosocomial Infection Control Consortium.
125. Kim JM et al. Multicenter surveillance study 150. Pishori T, Siddiqui AR, Ahmed M. Surgical
Revista Panamericana de Salud Pública, 2008,
for nosocomial infections in major hospitals wound infection surveillance in general surgery
24:195–202.
in Korea. Nosocomial infection surveillance procedures at a teaching hospital in Pakistan.
committee of the Korean Society for 138. Moreno CA et al. Device-associated infection American Journal of Infection Control, 2003,
Nosocomial Infection Control. American Journal rate and mortality in intensive care units 31:296–301.
of Infection Control, 2000, 28:454–458. of 9 Colombian hospitals: findings of the
151. Brown S et al. Prevalence and predictors of
International Nosocomial Infection Control
126. Danchaivijitrmd S et al. Prevalence and impacts surgical site infection in Tbilisi, Republic of
Consortium. Infection Control and Hospital
of nosocomial infection in Thailand 2001. Georgia. Journal of Hospital Infection, 2007,
Epidemiology, 2006, 27:349–356.
Journal of the Medical Association of Thailand, 66:160–166.
2005, 88(Suppl. 10):S1–S9. 139. Mehta A et al. Device-associated nosocomial
152. Brown SM et al. Prospective surveillance for
infection rates in intensive care units of seven
127. Danchaivijitr S et al. Development of quality surgical site infection in St. Petersburg, Russian
Indian cities. Findings of the International
indicators of nosocomial infection control. Federation. Infection Control and Hospital
Nosocomial Infection Control Consortium
Journal of the Medical Association of Thailand, Epidemiology, 2007, 28:319–325.
(INICC). Journal of Hospital Infection, 2007,
2005, 88(Suppl. 10):S75–S82.
67:168–174. 153. Kasatpibal N, Jamulitrat S, Chongsuvivatwong
128. Danchaivijitr S et al. Efficacy of hospital V. Standardized incidence rates of surgical
140. Askarian M, Williams C, Assadian O.
infection control in Thailand 1988-1992. Journal site infection: a multicenter study in Thailand.
Nosocomial infection rates following
of Hospital Infection, 1996, 32:147–153. American Journal of Infection Control, 2005,
cardiothoracic surgery in Iran. International
33:587–594.
129. Danchaivijitr S, Tangtrakool T, Chokloikaew Journal of Infectious Diseases, 2006, 10:185–
S. The second Thai national prevalence study 187. 154. Kasatpibal N et al. Impact of surgeon-specific
on nosocomial infections 1992. Journal of feedback on surgical site infection rates in
141. Ramirez Barba EJ et al. Device-associated
the Medical Association of Thailand, 1995, Thailand. Journal of Hospital Infection, 2006,
nosocomial infection rates in intensive care
78(Suppl. 2):S67–S72. 63:148–155.
units in four Mexican public hospitals. American
130. Danchaivijitr S et al. Prevalence of nosocomial Journal of Infection Control, 2006, 34:244–247. 155. Yalcin AN et al. Postoperative wound infections.
infection in Thailand 2006. Journal of the Journal of Hospital Infection, 1995, 29:305–309.
142. de Leon-Rosales SP et al. Prevalence of
Medical Association of Thailand, 2007, 90:1524–
infections in intensive care units in Mexico: a 156. Nguyen D et al. Incidence and predictors of
1529.
multicenter study. Critical Care Medicine, 2000, surgical-site infections in Vietnam. Infection
131. Danchaivijitr S et al. A national study on surgical 28:1316–1321. Control and Hospital Epidemiology, 2001,
wound infections 1992. Journal of the Medical 22:485–492.
143. Higuera F et al. Attributable cost and length of
Association of Thailand, 1995, 78(Suppl.
stay for patients with central venous catheter- 157. Ider BE et al. Prevalence of hospital-acquired
2):S73–S77.
associated bloodstream infection in Mexico infections and antibiotic use in two tertiary
132. Leblebicioglu H, Esen S. Hospital-acquired City intensive care units: a prospective, Mongolian hospitals. Journal of Hospital
urinary tract infections in Turkey: a nationwide matched analysis. Infection Control and Infection, 2010, 75:214–219.
multicenter point prevalence study. Journal of Hospital Epidemiology, 2007, 28:31–35.
158. Rosenthal VD et al. International Nosocomial
Hospital Infection, 2003, 53:207–210.
144. Cuellar LE et al. Device-associated infection Infection Control Consortium (INICC) report,
rates and mortality in intensive care units of data summary for 2003-2008, issued June
Peruvian hospitals: findings of the International 2009. American Journal of Infection Control,
Nosocomial Infection Control Consortium. 2010, 38:95–104 e2.
Revista Panamericana de Salud Pública, 2008,
24:16–24.
29
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
159. Gopal Katherason S et al. Ventilator-associated 173. Rosenthal VD et al. Impact of International 187. Allegranzi B et al. Successful implementation
nosocomial pneumonia in intensive care units Nosocomial Infection Control Consortium of the World Health Organization hand hygiene
in Malaysia. Journal of Infection in Developing (INICC) strategy on central line-associated improvement strategy in a referral hospital in
Countries, 2009, 3:704–710. bloodstream infection rates in the intensive Mali, Africa. Infection Control and Hospital
care units of 15 developing countries. Infection Epidemiology, 2010, 31:133–141.
160. Mesiano ER, Merchan-Hamann E. Bloodstream
Control and Hospital Epidemiology, 2010,
infections among patients using central venous 188. Newman MJ. Nosocomial and community
31:1264–1272.
catheters in intensive care units. Revista Latino- acquired infections in Korle Bu Teaching
Americana Enfermagem, 2007, 15:453–459. 174. Dogru A et al. The rate of device-associated Hospital, Accra. West African Journal of
nosocomial infections in a medical surgical Medicine, 2009, 28:300–303.
161. Gopal Katherason S et al. Baseline assessment
intensive care unit of a training and research
of intensive care-acquired nosocomial infection 189. Velasco E et al. Nosocomial infections in an
hospital in Turkey: one-year outcomes.
surveillancein three adult intensive care units oncology intensive care unit. American Journal
Japanese Journal of Infectious Diseases, 2010,
in Malaysia. Journal of Infection in Developing of Infection Control, 1997, 25:458–462.
63:95–98.
Countries, 2008, 2:364–368.
190. Habibi S,et al. Epidemiology of nosocomial
175. Madani N et al. Health-care associated
162. Rosenthal VD et al. Effect of an infection control infections in medicine intensive care unit at a
infections rates, length of stay, and bacterial
program using education and performance tertiary care hospital in northern India. Tropical
resistance in an intensive care unit of Morocco:
feedback on rates of intravascular device- Doctor, 2008, 38:233–235.
findings of the International Nosocomial
associated bloodstream infections in intensive
Infection Control Consortium (INICC). 191. Khuri-Bulos NA et al. Nosocomial infections in
care units in Argentina. American Journal of
International Archives of Medicine, 2009, 2:29. the intensive care units at a university hospital
Infection Control, 2003, 31:405–409.
in a developing country: comparison with
176. Faria S et al. The first prevalence survey of
163. Starling CE, Couto BR, Pinheiro SM. Applying National Nosocomial Infections Surveillance
nosocomial infections in the university hospital
the Centers for Disease Control and Prevention intensive care unit rates. American Journal of
centre ‘Mother Teresa’ of Tirana, Albania.
and National Nosocomial Surveillance system Infection Control, 1999, 27:547–552.
Journal of Hospital Infection, 2007, 65:244–250.
methods in Brazilian hospitals. American
192. Inan D et al. Device-associated nosocomial
Journal of Infection Control, 1997, 25:303–311. 177. Ribas RM, Gontijo Filho PP. Comparing hospital
infection rates in Turkish medical-surgical
infections in the elderly versus younger adults:
164. Rezende EM, Couto BR, Starling CE, Modena intensive care units. Infection Control and
an experience in a Brazilian University Hospital.
CM. Prevalence of nosocomial infections in Hospital Epidemiology, 2006, 27:343–348.
Brazilian Journal of Infectious Diseases, 2003,
general hospitals in Belo Horizonte. Infection
7:210–215. 193. Meric M et al. Intensive care unit-acquired
Control and Hospital Epidemiology, 1998,
infections: incidence, risk factors and
19:872–876. 178. Raka L et al. Prevalence of nosocomial
associated mortality in a Turkish university
infections in high-risk units in the university
165. de Oliveira AC et al. Surgical site infection in hospital. Japanese Journal of Infectious
clinical center of Kosova. Infection Control and
patients submitted to digestive surgery: risk Diseases, 2005, 58:297–302.
Hospital Epidemiology, 2006, 27:421–423.
prediction and the NNIS risk index. American
194. Erbay H et al. Nosocomial infections in intensive
Journal of Infection Control, 2006, 34:201–207. 179. Valinteliene R, Jurkuvenas V, Jepsen OB.
care unit in a Turkish university hospital: a
Prevalence of hospital-acquired infection
166. Duerink DO et al. Surveillance of healthcare- 2-year survey. Intensive Care Medicine, 2003,
in a Lithuanian hospital. Journal of Hospital
associated infections in Indonesian hospitals. 29:1482–1488.
Infection, 1996, 34:321–329.
Journal of Hospital Infection, 2006, 62:219–229.
195. Chen YY et al. Incidence rate and variable cost
180. Hughes AJ et al. Prevalence of nosocomial
167. Lahsaeizadeh S, Jafari H, Askarian M. of nosocomial infections in different types
infection and antibiotic use at a university
Healthcare-associated infection in Shiraz, Iran of intensive care units. Infection Control and
medical center in Malaysia. Infection Control
2004-2005. Journal of Hospital Infection, 2008, Hospital Epidemiology, 2009, 30:39–46.
and Hospital Epidemiology, 2005, 26:100–104.
69:283–287.
196. Rosenthal VD, Guzman S, Safdar N. Reduction
181. Jroundi I et al. Prevalence of hospital-acquired
168. Arabshahi KS, Koohpayezade J. Investigation of in nosocomial infection with improved hand
infection in a Moroccan university hospital.
risk factors for surgical wound infection among hygiene in intensive care units of a tertiary
American Journal of Infection Control, 2007,
teaching hospitals in Tehran. International care hospital in Argentina. American Journal of
35:412–416.
Wound Journal, 2006, 3:59–62. Infection Control, 2005, 33:392–397.
182. El Rhazi K et al. [Prévalence et facteurs de
169. Dumpis U et al. Prevalence of nosocomial 197. Thongpiyapoom S et al. Device-associated
risque des infections nosocomiales au CHU
infections in two Latvian hospitals. Euro infections and patterns of antimicrobial
Hassan II de Fès (Maroc).] La Revue de Santé
Surveillance, 2003, 8:73–78. resistance in a medical-surgical intensive care
de la Méditerranée orientale, 2007, 13:56–63.
unit in a university hospital in Thailand. Journal
170. Rosenthal VD et al. Device-associated
183. Gosling R et al. Prevalence of hospital-acquired of the Medical Association of Thailand, 2004,
nosocomial infections in 55 intensive care units
infections in a tertiary referral hospital in 87:819–824.
of 8 developing countries. Annals of Internal
northern Tanzania. Annals of Tropical Medicine
Medicine, 2006, 145:582–591. 198. Turgut H et al. Evaluation of device associated
and Parasitology, 2003, 97:69–73.
infection rates in intensive care units of
171. Rosenthal VD et al. International Nosocomial
184. Kallel H et al. Prevalence of hospital-acquired Pamukkale University Hospital. Infection, 2008,
Infection Control Consortium report, data
infection in a Tunisian hospital. Journal of 36:262–265.
summary for 2002-2007, issued January 2008.
Hospital Infection, 2005, 59:343–347.
American Journal of Infection Control, 2008, 199. Higuera F et al. The effect of process control
36:627–637. 185. Dridi E, Chetoui A, Zaoui A. [Investigation of the on the incidence of central venous catheter-
prevalence of nosocomial infection in a Tunisian associated bloodstream infections and
172. Rosenthal VD. Device-associated nosocomial
regional hospital]. Sanée Publique, 2006, mortality in intensive care units in Mexico.
infections in limited-resources countries:
18:187–194. Critical Care Medicine, 2005, 33:2022–2027.
findings of the International Nosocomial
Infection Control Consortium (INICC). American 186. Metintas S et al. Prevalence and characteristics
Journal of Infection Control, 2008, 36:S171. of nosocomial infections in a Turkish university
e7–12. hospital. American Journal of Infection Control,
2004, 32:409–413.
30
REFERENCES
200. Lobo RD et al. Impact of an educational 213. Martinez-Aguilar G, Anaya-Arriaga MC, 227. Fehr J et al. Risk factors for surgical site
program and policy changes on decreasing Avila-Figueroa C. [Incidence of nosocomial infection in a Tanzanian district hospital:
catheter-associated bloodstream infections in a bacteremia and pneumonia in pediatric unit]. a challenge for the traditional National
medical intensive care unit in Brazil. American Salud Pública de Mexico, 2001, 43:515–523. Nosocomial Infections Surveillance system
Journal of Infection Control, 2005, 33:83–87. index. Infection Control and Hospital
214. Petdachai W. Ventilator-associated pneumonia
Epidemiology, 2006, 27:1401–1404.
201. Rosenthal VD, Guzman S, Safdar N. Effect of in a newborn intensive care unit. Southeast
education and performance feedback on rates Asian Journal of Tropical Medicine and Public 228. Luksamijarulkul P et al. Nosocomial surgical
of catheter-associated urinary tract infection Health, 2004, 35:724–729. site infection among Photharam Hospital
in intensive care units in Argentina. Infection patients with surgery: incidence, risk factors
215. Petdachai W. Nosocomial pneumonia in a
Control and Hospital Epidemiology, 2004, and development of risk screening form.
newborn intensive care unit. Journal of the
25:47–50. Journal of the Medical Association of Thailand,
Medical Association of Thailand, 2000, 83:392–
2006, 89:81–89.
202. Simsek S et al. Ventilator-associated 397.
pneumonias in a cardiothoracic surgery centre 229. Kehachindawat P et al. Incidence and time
216. Ben Jaballah N et al. Epidemiology of
postoperative intensive care unit. Journal of trend of surgical site infection in Ramathibodi
hospital-acquired bloodstream infections
Hospital Infection, 2001, 47:321–324. Hospital during the years 2003-2005. Journal
in a Tunisian pediatric intensive care unit: a
of the Medical Association of Thailand, 2007,
203. Erdem I et al. Incidence, etiology, and 2-year prospective study. American Journal of
90:1356–1362.
antibiotic resistance patterns of gram-negative Infection Control, 2007, 35:613–618.
microorganisms isolated from patients with 230. Kasatpibal N et al. Extra charge and extra
217. Koigi-Kamau R, Kabare LW, Wanyoike-Gichuhi
ventilator-associated pneumonia in a medical- length of postoperative stay attributable to
J. Incidence of wound infection after caesarean
surgical intensive care unit of a teaching surgical site infection in six selected operations.
delivery in a district hospital in central Kenya.
hospital in Istanbul, Turkey (2004-2006). Journal of the Medical Association of Thailand,
East African Medical Journal, 2005, 82:357–361.
Japanese Journal of Infectious Diseases, 2008, 2005, 88:1083–1091.
61:339–342. 218. Raka L et al. Surgical site infections in an
231. Dhidah L et al. [The role of surgical wounds
abdominal surgical ward at Kosovo Teaching
204. Osvaldo Iribarren B et al. [Factores de riesgo in nosocomial infections. Prevalence study
Hospital. Journal of Infection in Developing
para mortalidad en neumonía asociada a at Sahloul university hospital.] Tunis Medical,
Countries, 2007, 1:337–341.
ventilación mecánica.] Revista Chilena de 1998, 7:401–407.
Infectiologia, 2009, 26:227–232. 219. Kanafani ZA et al. Surgical site infections
232. Erman T et al. Risk factors for surgical site
following spinal surgery at a tertiary care center
205. Zaidi AK et al. Hospital-acquired neonatal infections in neurosurgery patients with
in Lebanon: incidence, microbiology, and risk
infections in developing countries. Lancet, antibiotic prophylaxis. Surgical Neurology,
factors. Scandinavian Journal of Infectious
2005, 365:1175–1188. 2005, 63:107–112.
Diseases, 2006, 38:589–592.
206. Abramczyk ML et al. Nosocomial infection in 233. Kaya E et al. Risk factors for and effect of a
220. Vilar-Compte D et al. Surgical site infections
a pediatric intensive care unit in a developing one-year surveillance program on surgical
in ambulatory surgery: a 5-year experience.
country. Brazilian Journal of Infectious site infection at a university hospital in Turkey.
American Journal of Infection Control, 2001,
Diseases, 2003, 7:375–380. Surgical Infection (Larchmont), 2006, 7:519–
29:99–103.
526.
207. de Brito CS et al. Occurrence of bloodstream
221. Vilar-Compte D et al. Surgical site infections at
infection with different types of central vascular 234. Hodges AM, Agaba S. Wound infection
the National Cancer Institute in Mexico: a case-
catheter in critically neonates. Journal of in a rural hospital: the benefit of a wound
control study. American Journal of Infection
Infection, 2010, 60:128–132. management protocol. Tropical Doctor,
Control, 2000, 28:14–20.
1997,27:174–175.
208. Nagata E, Brito AS, Matsuo T. Nosocomial
222. Vilar-Compte D et al. [Surveillance of surgical
infections in a neonatal intensive care unit: 235. Sohn AH et al. Prevalence of surgical-site
wound infections. 18-month experience in the
incidence and risk factors. American Journal of infections and patterns of antimicrobial use in
Instituto Nacional de Cancerologia.] Salud
Infection Control, 2002, 30:26–31. a large tertiary-care hospital in Ho Chi Minh
Pública de México, 1999, 41(Suppl. 1):S44–S50.
City, Vietnam. Infection Control and Hospital
209. Cai XD et al. [Investigation of nosocomial
223. Chadli M et al. [Incidence of surgical wound Epidemiology, 2002, 23:382–387.
infection in the neonatal intensive care unit].
infections a prospective study in the Rabat
Zhongguo Dang Dai Er Ke Za Zhi [Chinese 236. Le TA et al. Reduction in surgical site infections
Mohammed V military hospital, Morocco.]
Journal of Contemporary Pediatrics], 2010, in neurosurgical patients associated with a
Médecine et Maladies Infectieuses, 2005,
12:81–84. bedside hand hygiene program in Vietnam.
35:218–222.
Infection Control and Hospital Epidemiology,
210. El-Nawawy AA et al. One year study of bacterial
224. Sangrasi AK et al. Surgical site infection rate 2007, 28:583–588.
and fungal nosocomial infections among
and associated risk factors in elective general
patients in pediatric intensive care unit (PICU) in 237. Le TA et al. Microbiology of surgical site
surgery at a public sector medical university in
Alexandria. Journal of Tropical Pediatrics, 2006, infections and associated antimicrobial
Pakistan. International Wound Journal, 2008,
52:185–191. use among Vietnamese orthopedic and
5:74–78.
neurosurgical patients. Infection Control and
211. Asembergiene J et al. Nosocomial infections in
225. Hernandez K et al. Incidence of and risk Hospital Epidemiology, 2006, 27:855–862.
the pediatric intensive care units in Lithuania.
factors for surgical-site infections in a Peruvian
Medicina (Kaunas), 2009, 45:29–36. 238. Thu LT et al. Incidence of surgical site infections
hospital. Infection Control and Hospital
and accompanying risk factors in Vietnamese
212. Gurskis V et al. Reduction of nosocomial Epidemiology, 2005, 26:473–477.
orthopaedic patients. Journal of Hospital
infections and mortality attributable to
226. Maksimovic J et al. Surgical site infections in Infection, 2005, 60:360–367.
nosocomial infections in pediatric intensive care
orthopedic patients: prospective cohort study.
units in Lithuania. Medicina (Kaunas), 2009, 239. Ameh EA et al. Surgical site infection in
Croatian Medical Journal,2008, 49:58–65.
45:203–213. children: prospective analysis of the burden and
risk factors in a sub-Saharan African setting.
Surgical Infections, 2008, 10:5.
31
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
240. Morhason-Bello IO et al. Determinants of post- 253. Cavalcante SS et al. Risk factors for developing 268. Merchant M, Karnad DR, Kanbur AA. Incidence
caesarean wound infection at the University nosocomial infections among pediatric patients. of nosocomial pneumonia in a medical intensive
College Hospital, Ibadan, Nigeria. Nigerian Pediatric Infectious Diseases Journal, 2006, care unit and general medical ward patients in
Journal of Clinical Practice, 2009, 12:1–5. 25:438–445. a public hospital in Bombay, India. Journal of
Hospital Infection, 1998, 39:143–148.
241. Ghelase MS et al. [A study of the incidence 254. Contreras-Cuellar GA et al. Device-associated
and the specific risk factors for surgical site infections in a Colombian neonatal intensive 269. Pawar M et al. Central venous catheter-related
nosocomial infections.] Chirurgia (Bucur), 2009, care unit. Revista de Salud Pública (Bogota), blood stream infections: incidence, risk factors,
104:41–47. 2007, 9:439–447. outcome, and associated pathogens. Journal of
Cardiothoracic and Vascular Anesthesia, 2004,
242. Duque-Estrada EO et al. Wound infections 255. Lakshmi KS et al. Study of nosocomial primary
18:304–308.
in pediatric surgery: a study of 575 patients bloodstream infections in a pediatric intensive
in a university hospital. Pediatric Surgery care unit. Journal of Tropical Pediatrics, 2007, 270. Mukhopadhyay C, Bhargava A, Ayyagari A.
International, 2003, 19:436–438. 53:87–92. Role of mechanical ventilation & development
of multidrug resistant organisms in hospital
243. Sanchez-Arenas R et al. [Incidence of 256. Juarez-Munoz IE et al. [The costs of hospital
acquired pneumonia. Indian Journal of Medical
nosocomial surgical-site infections. Application infections in a group of patients in a tertiary-
Research, 2003, 118:229–235.
of National Nosocomial Infections Surveillance care hospital.] Gaceta Médica México, 1999,
System (NNIS) index and description of 135:457–462. 271. Pawar M et al. Ventilator-associated
clinical and biochemical features from patients pneumonia: Incidence, risk factors, outcome,
257. Navarrete-Navarro S, Armengol-Sanchez G.
undergoing first-time ventriculoperitoneal and microbiology. Journal of Cardiothoracic
[Secondary costs due to nosocomial infections
shunt.] Cirugia y Cirujanos, 2009, 77:13–19. and Vascular Anesthesia, 2003, 17:22–28.
in 2 pediatric intensive care units.] Salud
244. Garcia HJ et al. [Risk factors for surgical site Pública de México, 1999, 41(Suppl. 1):S51–S58. 272. Bhatia JY et al. Postoperative wound infection
infections in newborns in a neonatal intensive in patients undergoing coronary artery bypass
258. Perez-Gonzalez LF, Ruiz-Gonzalez JM, Noyola
care unit.] Revista de Investigación Clínica, graft surgery: a prospective study with
DE. Nosocomial bacteremia in children: a 15-
2005, 57:425–433. evaluation of risk factors. Indian Journal of
year experience at a general hospital in Mexico.
Medical Microbiology, 2003, 21:246–251.
245. Kesah CN et al. Aerobic bacterial nosocomial Infection Control and Hospital Epidemiology,
infections in paediatric surgical patients at a 2007, 28:418–422. 273. Kothari A et al. Costs associated with hospital-
tertiary health institution in Lagos, Nigeria. acquired bacteraemia in an Indian hospital:
259. Porras-Hernandez JD et al. A prospective study
Nigerian Postgraduate Medical Journal, a case-control study. Journal of Hospital
of surgical site infections in a pediatric hospital
2004,11:4–9. Infection, 2009, 71:143–148.
in Mexico City. American Journal of Infection
246. Okeke IN et al. Antimicrobial resistance in Control, 2003, 31:302–308. 274. Askarian M, Gooran NR. National nosocomial
developing countries. Part I: recent trends and infection surveillance system-based study in
260. Onen A et al. Epidemiology and control of
current status. Lancet Infectious Diseases, Iran: additional hospital stay attributable to
nosocomial infections in paediatric surgery.
2005, 5:481–493. nosocomial infections. American Journal of
Journal of Hospital Infection, 2002, 52:166–170.
Infection Control, 2003, 31:465–468.
247. Soufir L et al. Attributable morbidity and
261. Soares de Macedo JL, Santos JB. Nosocomial
mortality of catheter-related septicemia in 275. Askarian M et al. Incidence and outcome of
infections in a Brazilian Burn Unit. Burns, 2006,
critically ill patients: a matched, risk-adjusted, nosocomial infections in female burn patients
32:477–481.
cohort study. Infection Control and Hospital in Shiraz, Iran. American Journal of Infection
Epidemiology, 1999, 20:396–401. 262. Giamberardino HI et al. Risk factors for Control, 2004, 32:23–26.
nosocomial infection in trauma patients.
248. Vincent JL et al. The prevalence of nosocomial 276. Kanafani ZA et al. Ventilator-associated
Brazilian Journal of Infectious Diseases, 2007,
infection in intensive care units in Europe. pneumonia at a tertiary-care center in a
11:285–289.
Results of the European Prevalence of developing country: incidence, microbiology,
Infection in Intensive Care (EPIC) study. EPIC 263. Toufen C, Jn. Prevalence rates of infection and susceptibility patterns of isolated
International Advisory Committee. Journal in intensive care units of a tertiary teaching microorganisms. Infection Control and Hospital
of the American Medical Association, 1995, hospital. Revista do Hospital das Clinicas da Epidemiology, 2003, 24:864–869.
274:639–644. Faculdade de Medicina da Universidade de Sao
277. Vosylius S, Sipylaite J, Ivaskevicius J. Intensive
Paulo, 2003, 58:254–259.
249. Hugonnet S et al. Impact of ventilator- care unit acquired infection: a prevalence
associated pneumonia on resource utilization 264. Santos KR et al. Surgical site infection: and impact on morbidity and mortality. Acta
and patient outcome. Infection Control and rates, etiology and resistance patterns to Anaesthesiologica Scandinavica, 2003,
Hospital Epidemiology, 2004, 25:1090–1096. antimicrobials among strains isolated at Rio 47:1132–1137.
de Janeiro University Hospital. Infection, 1997,
250. Safdar N et al. Clinical and economic 278. Rozaidi SW, Sukro J, Dan A. The incidence
25:217–220.
consequences of ventilator-associated of nosocomial infection in the intensive care
pneumonia: a systematic review. Critical Care 265. Boas PJ, Ruiz T. [Occurrence of hospital unit, hospital universiti Kebangsaan Malaysia:
Medicine, 2005, 33:2184–2193. infection among interned elderly in a university ICU-acquired nosocomial infection surveillance
hospital.] Revista de Saúde Pública, 2004, program 1998-1999. Medical Journal of
251. O’Grady NP et al. Guidelines for the prevention
38:372–378. Malaysia, 2001, 56:207–222.
of intravascular catheter-related infections.
Centers for Disease Control and Prevention. 266. Jaimes F et al. Incidence and risk factors 279. Sanchez-Velazquez LD, Ponce de Leon
Morbidity and Mortality Weekly Report, 2002, for ventilator-associated pneumonia in a Rosales S, Rangel Frausto MS. The burden of
51(RR-10):1–29. developing country: where is the difference? nosocomial infection in the intensive care unit:
Respiratory Medecine, 2007,101:762–767. effects on organ failure, mortality and costs. A
252. Tacconelli E et al. Epidemiology, medical
nested case-control study. Archives of Medical
outcomes and costs of catheter-related 267. Agarwal R et al. Epidemiology, risk factors
Research, 2006, 37:370–375.
bloodstream infections in intensive care units and outcome of nosocomial infections in a
of four European countries: literature- and respiratory intensive care unit in North India.
registry-based estimates. Journal of Hospital Journal of Infection, 2006, 53:98–105.
Infection, 2009, 72:97–103.
32
REFERENCES
280. Thanamee N, Sujaritjan N, Techasena W. matched analysis. American Journal of Infection 309. Nguyen KV, Nguyen PT, Jones SL.
Pneumonia in mechanically ventilated patients Control, 2003, 31:475–480. Effectiveness of an alcohol-based hand hygiene
in Nan hospital intensive care unit. Journal programme in reducing nosocomial infections
295. Pittet D et al. Effectiveness of a hospital-wide
of the Medical Association of Thailand, 1995, in the urology ward of Binh Dan hospital,
programme to improve compliance with hand
78(Suppl. 2):S102–S104. Vietnam. Tropical Medicine & International
hygiene. Lancet, 2000, 356:1307–1312.
Health, 2008, 13:1297–1302.
281. Elatrous S et al. Elatrous S et al. Incidence and
296. Eggimann P et al. Impact of a prevention
risk factors of ventilator-associated pneumonia: 310. Core components for infection prevention
strategy targeted at vascular-access care on
a one-year prospective survey. Clinical and control programmes. Report of the
incidence of infections acquired in intensive
Intensive Care, 1996, 7:276–281. second meeting informal network on infection
care. Lancet, 2000, 355:1864–1868.
prevention and control in health care. Geneva,
282. Oncul O et al. The evaluation of nosocomial
297. Pronovost P et al. An intervention to decrease World Health Organization, 2009.
infection during 1-year-period in the burn unit
catheter-related bloodstream infections in the
of a training hospital in Istanbul, Turkey. Burns, 311. Essential environmental health standards in
ICU. New England Journal of Medicine, 2006,
2002, 28:738–744. health care. Geneva, World Health Organization,
355:2725–2732.
2008.
283. Esatoglu AE et al. Additional cost of hospital-
298. Kollef M. SMART approaches for reducing
acquired infection to the patient: a case study in 312. Sehulster LM et al. Guidelines for environmental
nosocomial infections in the ICU. Chest, 2008,
Turkey. Health Services Management Research, infection control in health-care facilities.
134:447–456.
2006, 19:137–143. Recommendations from CDC and the
299. WHO Guidelines on Hand Hygiene in Health Healthcare Infection Control Practices Advisory
284. Inan D et al. Daily antibiotic cost of nosocomial
Care. Geneva: World Health Organization, 2009. Committee (HICPAC). Chicago, IL, American
infections in a Turkish university hospital. BMC
Society for Healthcare Engineering/American
Infectious Diseases, 2005, 5:5. 300. Tablan OC et al. Guidelines for preventing
Hospital Association, 2004.
health-care--associated pneumonia, 2003:
285. Erbay RH et al. Costs and risk factors for
recommendations of CDC and the Healthcare 313. Rutala WA. CDC guideline for disinfection and
ventilator-associated pneumonia in a Turkish
Infection Control Practices Advisory sterilization in healthcare facilities. Atlanta, GA,
university hospital’s intensive care unit: a case-
Committee. Morbidty and Mortality Weekly Centers for Disease Prevention and Control,
control study. BMC Pulmonary Medecine, 2004,
Report, 2004, 53(RR-3):1–36. 2008.
4:3.
301. Practical guidelines for infection control in 314. Acosta-Gnass SI, de Andrade Stempliuk
286. Ertugrul BM et al. Ventilator-associated
health care facilities. Geneva, World Health V. Sterilization manual for health centers.
pneumonia in surgical emergency intensive care
Organization/Western Pacific Regional Office/ Washington, DC, Pan American Health
unit. Saudi Medical Journal, 2006, 27:52–57.
South-East Asia Regional Office, 2004. Organization, World Health Organization,
287. Gol MK et al. Bloodstream, respiratory, and 2009:1–167.
302. Anderson DJ et al. Strategies to prevent
deep surgical wound infections after open heart
surgical site infections in acute care hospitals. 315. WHO best practices for injections and related
surgery. Journal of Cardiac Surgery, 1998,
Infectiont Control and Hospital Epidemiology, procedures toolkit. Geneva, World Health
13:252–259.
2008, 29(Suppl. 1):S51–S61. Organization, 2010.
288. Khan MM, Celik Y. Cost of nosocomial infection
303. Coffin SE et al. Strategies to prevent ventilator- 316. Waste management publications. Geneva,
in Turkey: an estimate based on the university
associated pneumonia in acute care hospitals. World Health Organization. (http://www.who.
hospital data. Health Services Management
Infection Control and Hospital Epidemiology, int/immunization_safety/publications/waste_
Research, 2001, 14:49–54.
2008, 29(Suppl. 1):S31–S40. management/ISPPpublicationsWM/en/index.
289. Zhang Q et al. Health-associated infections in html; accessed 13 April 2011.)
304. Gould CV et al. Guideline for prevention of
a pediatric nephrology unit in China. American
catheter-associated urinary tract infections 317. Siegel JD et al. Management of multidrug-
Journal of Infection Control, 2010, 38:473–475.
2009. Infection Control and Hospital resistant organisms in health care settings,
290. de Oliveira AC, Kovner CT, da Silva RS. Epidemiology, 2010, 31:319–326. 2006. American Journal of Infection Control,
Nosocomial infection in an intensive care unit in 2007, 35(Suppl. 2):S165–193.
305. Siegel JD et al. Guidelines for isolation
a Brazilian university hospital. Revista Latino-
precautions: preventing transmission of 318. Joint WHO-ILO-UNAIDS policy guidelines for
Americano Enfermagem, 2010, 18:233–239.
infectious agents in healthcare settings 2007. improving health worker access to HIV and
291. Joseph NM et al. Ventilator-associated American Journal of Infection Control, 2007, 35 TB prevention, treatment, care and support
pneumonia in a tertiary care hospital in India: (Suppl 10):S65-S164. services. Geneva, World Health Organization,
role of multi-drug resistant pathogens. Journal 2010.
306. Picheansathian W, Pearson A, Suchaxaya P.
of Infection in Developing Countries, 2010,
The effectiveness of a promotion programme 319. WHO patient safety curriculum guide for
4:218–225.
on hand hygiene compliance and nosocomial medical schools. Geneva, World Health
292. Rodrigues PM et al. Ventilator-associated infections in a neonatal intensive care unit. Organization, 2009.
pneumonia: epidemiology and impact on International Journal of Nursing Practice, 2008,
320. WHO patient safety curriculum guide: multi-
the clinical evolution of ICU patients. Jornal 14:315–321.
professional edition. Geneva, World Health
Brasiliero de Pneumologia, 2009, 35:1084–
307. Caniza MA et al. A practical guide to alcohol- Organization, 2011.
1091.
based hand hygiene infrastructure in a
321. Longtin Y et al. Patient participation: current
293. Apisarnthanarak A et al. Effectiveness of an resource-poor pediatric hospital. American
knowledge and applicability to patient safety.
educational program to reduce ventilator- Journal of Infection Control, 2009, 37:851–854.
Mayo Clinic Proceedings, 2010, 85:53–62.
associated pneumonia in a tertiary care center
308. Bedat B et al. Successful hand hygiene
in Thailand: a 4-year study. Clinical Infectious
improvement strategy in a referral children’s
Diseases, 2007, 45:704–711.
hospital in Armenia. Journal of Hospital
294. Rosenthal VD et al. The attributable cost, length Infection, 2010, 76:362–363.
of hospital stay, and mortality of central line-
associated bloodstream infection in intensive
care departments in Argentina: a prospective,
33
REPORT ON THE BURDEN OF ENDEMIC HEALTH CARE-ASSOCIATED INFECTION WORLDWIDE
APPENDIX
Search terms
Cross-infection [MeSH Term], nosocomial infection, nosocomial
infections, hospital acquired infection, hospital acquired infections,
hospital-acquired infection, hospital-acquired infections, health
care associated infection, health care associated infections, health
care-associated infection, health care-associated infections, and
infection control [Mesh Term], infection control, bloodstream
infection, bloodstream infections, nosocomial bacteremia,
nosocomial bacteraemia, nosocomial septicemia, nosocomial
septicaemia, device-associated infection, device-associated
infections, urinary tract infection, urinary tract infections, surgical
site infection, surgical site infections, wound infection, wound
infections, ventilator-associated pneumonia, ventilator associated
pneumonia, hospital-acquired pneumonia, hospital acquired
pneumonia, developing country, developing countries, and
developing countries [Mesh Terms], developed country, developed
countries, and developed countries [Mesh Terms] and names of the
countries individually.
34
World Health Organization Email
20 Avenue Appia savelives@who.int
CH – 1211 Geneva 27 Please visit us at:
Switzerland www.who.int/patientsafety/en/
Tel: +41 (0) 22 791 50 60 www.who.int/gpsc/en