Articles
Burden of endemic health-care-associated infection in
Lancet 2011; 377: 228–41
Published Online
December 10, 2010
DOI:10.1016/S0140-
6736(10)61458-4
See Comment page 186
First Global Patient Safety
Challenge, WHO Patient Safety,
Geneva, Switzerland
(B Allegranzi MD,
S Bagheri Nejad MD,
W Graafmans PhD, H Attar PhD,
L Donaldson MD,
Prof D Pittet MD); Division of
Clinical Epidemiology,
University of Geneva Hospitals
and Faculty of Medicine,
Geneva, Switzerland
(C Combescure PhD); Infection
Control Programme, and WHO
Collaborating Centre on
Patient Safety (Infection
Control and Improving
Practices), University of Geneva
Hospitals and Faculty of
Medicine, Geneva, Switzerland
(Prof D Pittet); and National
Patient Safety Agency, London,
UK (L Donaldson)
Correspondence to:
Prof Didier Pittet, Infection
Control Programme, University
of Geneva Hospitals and Faculty
of Medicine, 4 Rue Gabrielle
Perret-Gentil, 1211 Geneva 14,
Switzerland
didier.pittet@hcuge.ch
228
developing countries: systematic review and meta-analysis
Benedetta Allegranzi, Sepideh Bagheri Nejad, Christophe Combescure, Wilco Graafmans, Homa Attar, Liam Donaldson, Didier Pittet
Summary
Background Health-care-associated infection is the most frequent result of unsafe patient care worldwide, but few
data are available from the developing world. We aimed to assess the epidemiology of endemic health-care-associated
infection in developing countries.
Methods We searched electronic databases and reference lists of relevant papers for articles published 1995–2008.
Studies containing full or partial data from developing countries related to infection prevalence or
incidence—including overall health-care-associated infection and major infection sites, and their microbiological
cause—were selected. We classified studies as low-quality or high-quality according to predefined criteria. Data
were pooled for analysis.
Findings Of 271 selected articles, 220 were included in the final analysis. Limited data were retrieved from some
regions and many countries were not represented. 118 (54%) studies were low quality. In general, infection frequencies
reported in high-quality studies were greater than those from low-quality studies. Prevalence of health-care-associated
infection (pooled prevalence in high-quality studies, 15·5 per 100 patients [95% CI 12·6–18·9]) was much higher than
proportions reported from Europe and the USA. Pooled overall health-care-associated infection density in adult
intensive-care units was 47·9 per 1000 patient-days (95% CI 36·7–59·1), at least three times as high as densities
reported from the USA. Surgical-site infection was the leading infection in hospitals (pooled cumulative incidence
5·6 per 100 surgical procedures), strikingly higher than proportions recorded in developed countries. Gram-negative
bacilli represented the most common nosocomial isolates. Apart from meticillin resistance, noted in 158 of 290 (54%)
Staphylococcus aureus isolates (in eight studies), very few articles reported antimicrobial resistance.
Interpretation The burden of health-care-associated infection in developing countries is high. Our findings indicate a
need to improve surveillance and infection-control practices.
Funding World Health Organization.
Introduction but also that the effect on patients and health-care
Health-care-associated infections are deemed the most systems is severe and greatly underestimated.
frequent adverse event threatening patients’ safety The aim of this systematic review and meta-analysis
worldwide.1–3 However, reliable estimates of the global is to assess the burden of endemic health-care-associated
burden are hampered by a paucity of data adequately infection in developing countries by collation of
describing endemic infections at national and regional available data from published studies on epidemiology.
levels, particularly in resource-limited settings.4 In We also aim to investigate constraints linked to
countries where less than 5% of the gross national surveillance of health-care-associated infection in
product is spent on health care, and workforce density is resource-limited settings and identify perspectives
less than five per 1000 population,5 other emerging for improvement.
health problems and diseases take priority.6 The
epidemiological gap leading to the absence of reliable Methods
estimates of the global burden is mainly because Search strategy and selection criteria
surveillance of health-care-associated infection expends We undertook a literature search and review process
time and resources and needs expertise in study design, according to a protocol designed before data collection.
data collection, analysis, and interpretation. Very few We aimed to identify studies on the epidemiology of
countries of low and middle income have national health-care-associated infection in developing countries,
surveillance systems for health-care-associated with a particular focus on the most frequent bacterial
infections. Data from the International Nosocomial infections—urinary-tract infection, surgical-site infection,
Infection Control Consortium,7 and findings of two bloodstream infection, hospital-acquired pneumonia, and
systematic reviews on hospital-acquired neonatal ventilator-associated pneumonia. We searched Medline
infections8 and ventilator-associated pneumonia,9 for reports published between January, 1995, and
suggested not only that risks of health-care-associated December, 2008, with no language restriction. We used a
infection are significantly higher in developing countries comprehensive list of terms (panel 1), including MeSH
www.thelancet.com Vol 377 January 15, 2011

Panel 1: Detailed search strategy and WHO databases
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”,
“infection control” [MeSH term], “infection control”,
“bloodstream infection”, “bloodstream infections”,
“nosocomial bacteraemia”, “nosocomial bacteremia”,
“nosocomial septicaemia”, “nosocomial septicemia”,
“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”, “developing countries”
[MeSH term], and names of developing countries individually.
WHO regional medical databases
Western Pacific Region Index Medicus (WPRIM); Latin
America and Caribbean Health Sciences (LILACS); African
Index Medicus (AIM); Index Medicus for the Eastern
Mediterranean Region Database (IMEMR); and Index Medicus
for the South-East Asian Region (IMSEAR-HELLIS).
terms “cross infection”, “infection control”, and
“developing countries”, together with individual names of
countries of low and middle income, according to the 2008
World Bank classification.10 We applied the same search
strategy to the Cochrane database to identify any published
reviews, and we searched WHO regional medical
databases (panel 1). Furthermore, we consulted Embase
but our search did not yield additional publications.
One of us (SBN) screened abstracts of retrieved
references for potentially relevant studies from developing
countries, containing either full or partial data for
proportions of overall health-care-associated infection
and health-care-associated urinary-tract, surgical-site,
and bloodstream infections and hospital-acquired and
ventilator-associated pneumonia, and the microbiological
causes of these infections. We excluded duplicate
references, studies reporting outbreaks or including
community-acquired infections, and publications
reporting the same data. We obtained the full text of
potentially relevant studies and two of us (SBN and BA)
scrutinised these reports independently. We also screened
reference lists of all reviewed studies for further
eligible publications.
Data extraction
Extracted data included: authors; year of publication;
country or countries where the study was done;
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Articles
timescale; setting and scope of study; sample size; type
of patient population (adult, neonatal, and paediatric);
level of risk (high-risk patients, those admitted to
intensive-care units [ICUs], burn and transplant
recipients vs mixed populations, including individuals
admitted to other lower risk areas); type of surveyed
infection (overall health-care-associated infection,
including at least the four most frequent infections
[urinary-tract, surgical-site, and bloodstream infections,
and hospital-acquired or ventilator-associated
pneumonia]); surveillance methods; definitions used
for diagnosis; reported infection prevalence or
cumulative incidence data and corresponding
denominators; microbiological isolates; wound
contamination class and type of surgical-site infection;
and antimicrobial resistance. We only judged
microbiological data suitable for assessment when the
number of bacterial isolates was reported. Selected
studies used variably the terms “central venous
catheter-associated”, “central venous catheter-related”,
“central line-associated”, or “catheter-related bloodstream
infection”; thus, we chose to use catheter-related
bloodstream infection as a generic term throughout this
present report when referring to these different
categories. We further stratified studies into six regions
(Africa, the Americas, Europe, southeast Asia, eastern
Mediterranean, and western Pacific), according to WHO
classification. After in-depth review and data entry into
a dedicated database, we classified studies as high
quality when the following predefined criteria were met:
prospective design; use of standardised definitions
(ie, according to the US Centers for Disease Control and
Prevention National Nosocomial Infection Surveillance
[NNIS]/National Healthcare Safety Network [NHSN]
system);11 detection of at least all four major infections
for studies related to health-care-associated infections in
general; and publication in a peer-reviewed journal.
7719 abstracts identified by the search
7448 abstracts not eligible for inclusion
(not relevant to the study question)
271 abstracts eligible for inclusion and
detailed assessment
29 articles in languages not possible to read
19 articles for which the full text could not
be retrieved
3 articles with data duplication
220 articles included in the analysis
Figure 1: Flow diagram for selection of articles
229
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Africa Americas Eastern Europe Southeast Asia Western Pacific International Total
Mediterranean
Adult Paediatric Adult Paediatric Adult Paediatric Adult Paediatric Adult Paediatric Adult Paediatric Adult Paediatric Adult Paediatric All
General health- 3 1 28 17 12 3 26 2 14 4 3 2 3 0 89 29 118
care-associated
infection
Surgical-site 6 2 15 1 8 0 8 0 12 0 5 0 0 0 54 3 57
infection
Ventilator- 1 0 2 0 6 0 4 1 5 1 0 0 0 0 18 2 20
associated
pneumonia
Bloodstream 0 0 1 1 1 1 3 0 3 3 0 0 0 0 8 5 13
infection
Health-care- 0 0 2 0 0 0 2 0 2 1 0 0 0 0 6 1 7
associated
pneumonia
Urinary-tract 1 0 1 0 1 0 2 0 0 0 0 0 0 0 5 0 5
infection
Total 11 3 49 19 28 4 45 3 36 9 8 2 3 0 180 40 220

Data are number of published studies.

Table 1: Health-care-associated infections in developing countries according to WHO region, patient population, and type of infection (1995–2008)

Statistical analysis gross domestic product dedicated to health per country.

We pooled data from both prevalence and incidence studies
and summarised the results in the same unit. The
prevalence of either infection or infected patients refers to
the number of infection episodes or infected patients per
100 patients present in the hospital or ward at a given point
in time. The cumulative incidence refers to the number of
either 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 surgical-site infection, it is usually 30 days after surgery
whereas for other infections it refers to the duration of
hospital or ward stay. Infection incidence density refers to
the number of infection episodes per 1000 patient-days or
device-days; incidence density data were only available
from studies undertaken in ICUs.
We reported ranges of prevalence, incidence, and
density and gave median values when calculation of
pooled infection frequencies or densities was not possible.
For studies reporting the same outcome measures and
using the same methods, we pooled data when the
appropriate denominator was available. We calculated
pooled proportions and densities with Comprehensive
Meta-Analysis, version 2.0 (Biostat, Englewood, NJ, USA).
Models were systematically applied with random effects.
We measured heterogeneity with the I² statistic (values of
25%, 50%, and 75% represented low, medium, and high
heterogeneity, respectively). We compared groups of
high-quality and low-quality studies with Cochran’s test.
We used the two-sample Kolmogorov-Smirnov
non-parametric test to compare frequencies of
surgical-site infection with wound classification. When
the number of available studies was greater than ten,12 we
did meta-regressions to investigate the association
between outcomes, year of publication, and proportion of
We judged p≤0·05 significant.
Role of the funding source
The sponsor of the study had no role in study design,
data collection, data analysis, data interpretation, or
writing of the report. The corresponding author had full
access to all the data in the study and had final
responsibility for the decision to submit for publication.
Results
Our search yielded 7719 abstracts, of which 271 published
articles were eligible for inclusion. For 48 studies (18%),
the full paper could not be accessed (n=19) or was not
screened owing to language restrictions (n=29); three
articles were further excluded at second reading because
findings were duplicated in other publications (figure 1).
220 articles in English, French, German, and Spanish
were included in the final analysis. Two additional
systematic reviews were retrieved on neonatal health-
care-associated infection8 and ventilator-associated
pneumonia9 in developing countries; no review was
available from the Cochrane database.
Mapping of retrieved studies revealed a scattered global
picture (table 1). Health-care-associated infection was
recorded poorly in some regions, particularly Africa and
the western Pacific region. In regions with the most
reports (Europe and the Americas), studies generally
covered only a few countries (figure 2). Nine studies from
four developing countries were undertaken at national
level13–21 and another 14 were multicentre country-specific
studies (five related to health-care-associated infection in
general,22–26 nine to surgical-site infections).27–35
136 (62%) were undertaken at a single hospital or on one
ward and 110 (50%) were done in teaching hospitals.

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Adults Neonates and children

World Health Organization

1–2 1–2
3–5 3–5 The boundaries shown and the designations used on this map 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,
5–10 5–10 city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines on
>10 >10 maps represent approximate border lines for which there may not yet be full agreement.

Figure 2: Number of studies reporting health-care-associated infection in developing countries, 1995–2008

Size of dots indicates number of studies. Map created with ARCView (version 9.3.1; ESRI, Redlands, CA, USA), using WHO criteria for official borders and disputed borders.

118 of 220 studies (54%) were of overall low quality, 25

according to our criteria.
We identified 22 prevalence and 12 incidence studies 20
Infections or infected patients

reporting proportions of overall health-care-associated

(per 100 patients)

infection in mixed populations of patients (see 15

Statistical analysis for explanation about
units).13–16,18,22–26,36–59 Prevalence of health-care-associated 10

infection varied between 5·7 and 19·1 per 100 patients, and
incidence was 1·7–23·6 per 100 patients (figure 3). Pooled
prevalence and incidence of overall health-care-associated
infection was 10·1 (95% CI 8·4–12·2) and 7·4 (4·4–12·2)
per 100 patients, respectively, and the pooled prevalence of
infected patients was 10·6 (8·1–13·9) per 100 patients.
11 (50%) prevalence studies reported proportions of infected
patients or infection frequencies higher than 10·0 per
100 patients.23,39,40,42–45,51–54 In this population of patients, 29%
of health-care-associated infections were surgical-site
infections, 24% affected the urinary tract, 19% were
bloodstream infections, 15% were health-care-associated
pneumonia, and 13% were other infections.
A high level of heterogeneity was noted between
prevalence studies that included data for overall health-
care-associated infection (I²=97·4%). However, only 41%
(9/22) of reports met high-quality criteria.18,23,25,40,43–45,51,54
Pooled prevalence of overall health-care-associated
infection was 15·5 per 100 patients (95% CI 12·6–18·9) in
high-quality studies and 8·5 (7·1–10·0) in low-quality
studies (p<0·0001). Similarly, the proportion of infected
patients was higher in high-quality than low-quality
studies (13·5 vs 7·2 per 100 patients; p=0·0007).
5
0
Inf/100 pts Inf pts/100 pts Inf/100 pts Inf pts/100 pts
Prevalence Incidence
Figure 3: Prevalence and cumulative incidence of health-care-associated
infection in developing countries, 1995–2008
Box plots indicate range of infection prevalence and cumulative incidence for
first and third quartile. Medians are indicated as a black line. Whiskers indicate
lower and upper end of distribution. Infection proportions are shown as
infections per 100 patients (Inf/100 pts) and infected patients per 100 patients
(Inf pts/100 pts).
Overall health-care-associated infection and device-
associated infection densities in adult high-risk patients
were reported in 38 studies.60–97 Density of overall
health-care-associated infection ranged from 9·0 to
91·7 episodes per 1000 patient-days. In studies undertaken
in ICUs, pooled cumulative incidence and density were
34·7 per 100 patients (95% CI 23·6–47·7) and 47·9 per
1000 patient-days (36·7–59·1), respectively (figure 4A);
high heterogeneity was detected in the results of these
studies (I²=99·6% and 99·4%, respectively). In a study

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A Overall HAI B CR-BSI

Density N Density (95% CI) Density N Density (95% CI)
Velasco et al (1997)92 0·0917 4034 Rosenthal et al (2003)62 0·0446 919
Erbay et al (2003)96 0·0568 7394 Thongpiyapoom et al (2004)83 0·0026 5667
Rosenthal et al (2003)62 0·0900 1422 Rosenthal et al (2004)61 0·0260 6070
Rosenthal et al (2005)91 0·0476 2187 Askarian et al (2006)74 0·0017 1753
Meric et al (2005)95 0·0562 1653 Rosenthal et al (2006)63 0·0069 2469
Cevik et al (2005)97 0·0842 2006 Moreno et al (2006)66 0·0113 11 110
Inan et al (2006)85 0·0342 16 892 Rosenthal et al (2006)72 0·0125 74 641
Mehta et al (2007)68 0·0091 52 518 Ramirez Barba et al (2006)78 0·0231 6450
Leblebicioglu et al (2007)86 0·0339 37 148 Mehta et al (2007)68 0·0079 36 857
Salomao et al (2008)65 0·0298 10 293 Leblebicioglu et al (2007)86 0·0176 22 782
Habibi et al (2008)69 0·0286 3322 Turgut et al (2008)90 0·0041 721
Cuellar et al (2008)81 0·0249 10 024 Cuellar et al (2008)81 0·0077 6514
0·0479 Salomao et al (2008)65 0·0091 9494
Rosenthal et al (2008) 73 0·0092 188 401
0 0·10
0·0113

0 0·10

C CR-UTI D VAP
Density N Density (95% CI) Density N Density (95% CI)
Rosenthal et al (2003)62 0·0230 1286 Simsek et al (2001)87 0·0164 2708
Thongpiyapoom et al (2004)83 0·0138 4790 Rosenthal et al (2003)62 0·0510 629
Rosenthal et al (2004)61 0·0168 8851 Thongpiyapoom et al (2004)83 0·0108 6850
Rosenthal et al (2004)60 0·0213 1779 Salahuddin et al (2004)79 0·0132 3140
Askarian et al (2006)74 0·0029 1586 Rosenthal et al (2004)61 0·0461 3510
Moreno et al (2006)66 0·0043 12 433 Askarian et al (2006)74 0·0032 1586
Rosenthal et al (2006)72 0·0089 100 114 Moreno et al (2006)66 0·0100 8593
Rosenthal et al (2006)63 0·0131 7097 Ramirez Barba et al (2006)78 0·0218 2390
Ramirez Barba et al (2006)78 0·0134 4184 Rosenthal et al (2006)72 0·0241 52 987
Mehta et al (2007)68 0·0014 30 464 Rosenthal et al (2006)63 0·0513 1638
86
Leblebicioglu et al (2007) 0·0083 35 237 Mehta et al (2007)68 0·0105 13 481
Cuellar et al (2008)81 0·0051 7776 Leblebicioglu et al (2007)86 0·0265 23 520
Rosenthal et al (2008)73 0·0065 202 311 Rosenthal et al (2008)73 0·0195 117 143
Salomao et al (2008)65 0·0096 8817 Salomao et al (2008)65 0·0209 6502
Turgut et al (2008)90 0·0153 1106 Erdem et al (2008)89 0·0226 12 345
0·0098 Cuellar et al (2008)81 0·0313 5074
Turgut et al (2008)90 0·0569 931
0 0·10
0·0229

0 0·10

Figure 4: Pooled overall health-care-associated and device-associated infection densities in adult intensive-care units in developing countries, 1995–2008
(A) HAI=health-care-associated infection. Density=HAI episodes per patient-day. N=overall number of patient-days. (B) CR-BSI=catheter-related bloodstream infection. Density=CR-BSI episodes per
catheter-day. N=overall number of catheter-days. (C) CR-UTI=catheter-related urinary-tract infection. Density=CR-UTI episodes per urinary catheter-day. N=overall number of urinary catheter-days.
(D) VAP=ventilator-associated pneumonia. Density=VAP episodes per ventilator-day. N=overall number of ventilator-days.

undertaken in 55 ICUs from eight countries, overall
ICU-acquired, device-associated infection density was as
high as 22·5 episodes per 1000 patient-days.72 In a
multicentre ICU study from Argentina,62 and in other
studies undertaken at oncology and neurology units in
Brazil92 and Turkey,97 density of health-care-associated
infection even exceeded 80 episodes per 1000 patient-days.
In 31 studies,60–90 densities of specific types of
ICU-acquired device-associated infections in adults varied
between 1·7 and 44·6 per 1000 catheter-days for
catheter-related bloodstream infections, 1·4 and 23·0 per
1000 urinary catheter-days for catheter-related urinary-tract
infections, and 3·2 and 56·9 per 1000 ventilator-
days for ventilator-associated pneumonia. Figures 4B–4D
show pooled densities for these three types of
infection,60–63,65,66,68,72–74,78,79,81,83,86,87,89,90 and table 2 presents
a comparison of densities reported by the US
NNIS/NHSN98,99 and the German hospital infection
surveillance system.100,101 A high level of heterogeneity was
detected in studies reporting catheter-related bloodstream
infections (I²=97·2%), catheter-related urinary-tract
infections (I²=98·2%), and ventilator-associated
pneumonia (I²=97·2%). Quality of incidence studies
undertaken in ICUs was judged high in most cases (23/36,
64%). While investigating the association between
infection incidence densities and year of publication of

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Number of ICUs CR-BSI (95% CI) Catheter-days CR-UTI (95% CI) Urinary catheter-days VAP (95% CI) Ventilator-days
Developed countries
NNIS (1995–2003), USA*98 85–133† 5·0‡ 1 356 490 5·3‡ 1 356 490 5·8‡ 115 900
NHSN (2006–2008), USA*99 89–182† 2·1‡ 699 300 3·4‡ 546 824 2·9‡ 383 068
KISS (1997–2003), Germany100 309 1·8‡ 1 993 541 .. .. 8·0‡ 1 177 137
KISS (2004–2009), Germany101 514–583† 1·3‡ 4 002 108 2·0‡ 4 757 133 5·1‡ 2 391 381
Developing countries
INICC (2002–2007), 18 developing 60 8·9‡ 132 061 6·6‡ 1030 19·8‡ 1802
countries*§73
Argentina (1998–2004; current 15 24·7 (7·4–42·0) 9458 17·2 (13·4–21·1) 19 013 48·0 (42·0–54·0) 5777
systematic review)60–63
Turkey (1999–2005; current systematic 16 11·0 (2·2–24·3) 23 503 10·8 (4·2–17·4) 36 343 26·0 (20·0–32·0) 39 504
review)86,87,89,90
Current systematic review 226 11·3 (9·0–13·6) 373 848 9·8 (7·7–11·8) 427 831 22·9 (19·1–26·6) 263 027
(1995–2008)60–63,65,66,68,72–74,78,79,81,83,86,87,89,90

Data are overall (pooled mean) infection episodes per 1000 device-days. ICUs=intensive-care units. CR-BSI=catheter-related bloodstream infection. CR-UTI=catheter-related urinary-tract infection.
VAP=ventilator-associated pneumonia. NNIS=National Nosocomial Infection Surveillance. NHSN=National Healthcare Safety Network. KISS=Krankenhaus Infektions Surveillance System. INICC=International
Nosocomial Infection Control Consortium. *Medical or surgical ICUs in major teaching hospitals. †Range reported because number of ICUs included in data pooling varied according to the type of
device-associated infection. ‡95% CI not reported. §Argentina, Brazil, Colombia, Costa Rica, Cuba, El Salvador, India, Kosovo, Lebanon, Macedonia, Mexico, Morocco, Nigeria, Peru, Philippines, Turkey, Uruguay.

Table 2: Comparison of device-associated infection densities in adult ICUs from developed and developing countries, 1995–2008

A B
35 100
infection (per 100 surgical procedures)
Cumulative incidence of surgical-site

90
of surgical-site infection (%)

30
80
Cumulative incidence

25 70

20 60
50
15 40
10 30
20
5
10
0 0
Episodes/100 surgical patients Episodes/100 surgical procedures Clean Clean- Contaminated Dirty
contaminated
Wound classification

Figure 5: Cumulative incidence of surgical-site infections overall (A) and according to wound classification (B) in developing countries, 1995–2008
Box plots contain results for first and third quartile. Medians are indicated as a black line. Whiskers indicate lower and upper limits of distribution. Incidence is
reported as surgical-site infection episodes, either per 100 surgical patients or per 100 surgical procedures.

the studies included in the meta-analysis (1997–2008; ventilator-associated pneumonia ranged from 4·4 to
figure 4), a significant decrease over time was recorded for 143 episodes per 1000 ventilator-days (median 28·0
the incidence density of overall health-care-associated [IQR 10·9–88·3]), and densities of catheter-related
infections (p<0·0001), catheter-related bloodstream bloodstream infections were between 10·2 and
infections (p=0·0230) and catheter-related urinary-tract 60·0 episodes per 1000 catheter-days (median 18·7
infections (p=0·0008). [12·5–43·0]).112,113,115,117–119,121 Data pooled from four
In 40 published studies, epidemiology of comparable studies undertaken in Brazilian neonatal
health-care-associated infection was reported for neonates ICUs109–112 revealed an overall incidence of
and children (table 1). Cumulative incidence of health-care-associated infections of 40·8 infections per
health-care-associated infections and of infected patients 100 patients (95% CI 16·1–71·1) and a density of
on paediatric wards or in children’s hospitals was 30·0 episodes per 1000 patient-days (25·0–35·0).
0·9–17·7102–105 and 2·7–26·9103,106–108 per 100 patients, Of 101 studies in which specific types of infection were
respectively; respective pooled incidences were addressed, 57 (56%) focused on surgical-site infections.
5·7 (95% CI 2·3–13·1) and 10·9 (2·8–34·5) per Reported cumulative incidence of these infections
100 patients. Densities of overall health-care-associated ranged from 0·4 to 30·9 per 100 patients undergoing
infection in paediatric ICUs were 1·6–46·1 per surgical procedures and from 1·2 to 23·6 per
1000 patient-days, and in neonatal units they were 100 surgical procedures (figure 5A).17,27–35,55,122–161 Pooled
15·2–62·0 per 1000 patient-days.109–121 Densities of cumulative incidence of surgical-site infections was

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High-risk patients Mixed populations Surgical-site infection Ventilator-associated and Bloodstream infection
(17 studies) (11 studies) (11 studies) health-care-associated (3 studies)
pneumonia (5 studies)
Staphylococcus aureus 156 (11%) 266 (21%) 219 (20%) 47 (10%) 154 (19%)
Coagulase-negative staphylococci 151 (11%) 138 (11%) 67 (6%) 15 (3%) 141 (17%)
Enterococcus spp 74 (5%) 4 (<1%) 38 (4%) 1 (<1%) 48 (6%)
Escherichia coli 93 (7%) 116 (9%) 193 (18%) 6 (1%) 23 (3%)
Enterobacteriaceae (excluding E coli) 272 (20%) 231 (18%) 284 (26%) 92 (20%) 127 (15%)
Pseudomonas spp 239 (17%) 214 (17%) 180 (17%) 134 (29%) 96 (12%)
Acinetobacter spp 259 (19%) 112 (9%) 14 (1%) 110 (24%) 146 (18%)
Candida spp 28 (2%) 74 (6%) 6 (1%) 1 (<1%) 44 (5%)
Others 110 (8%) 114 (9%) 77 (7%) 53 (12%) 46 (6%)
Total 1382 (100%) 1269 (100%) 1078 (100%) 459 (100%) 825 (100%)

Data are number of isolates (%). High-risk patients=burn and transplant patients and those in intensive-care units. Mixed populations=patients admitted to other lower risk
areas. *Only studies reporting number of isolates were included.

Table 3: Bacterial isolates identified in health-care-associated infections from developing countries, 1995–2008*

11·8 per 100 patients undergoing surgical procedures Discussion

(95% CI 8·6–16·0) and 5·6 per 100 surgical pro-
cedures (2·9–10·5), and a high level of heterogeneity
was seen in these studies (I²=99·0% and 99·4%,
respectively). Median cumulative incidence of
surgical-site infections in clean, clean-contaminated,
contaminated, and dirty wounds were, respectively, 7·6
(range 1·3–79·0), 13·7 (1·5–81·0), 14·3 (0·5–65·5), and
39·2 (0·2–100·0) episodes per 100 surgical procedures
(figure 5B).17,122,124,127,128,131,137,139–141,143–148,150,153,155,157,158,160 Proportions
of surgical-site infections differed significantly between
wound classes (dirty vs clean, p<0·0001; dirty vs
clean-contaminated, p=0·0006; dirty vs contaminated,
p=0·0291).
Information on pathogens causing health-care-
associated infections in general was available from
28 studies;18,22,23,25,38,40,43–45,51,58,65,66,68,81,85,86,92,93,97,162–169 18 included
microbiological data specifically related to surgical-
site infections, ventilator-associated and health-care-
associated pneumonia, and bloodstream infections
(table 3).64,76,84–86,122,132,138,140,149–151,156,158,170,171 Gram-negative bacilli
represented the most common nosocomial isolates, both
in mixed populations and in high-risk patients. The most
frequent single pathogens were Staphylococcus aureus in
mixed populations and Acinetobacter spp in high-risk
patients. Acinetobacter spp was the second most frequent
pathogen identified for ventilator-associated pneumonia
and, unexpectedly, bloodstream infections. S aureus was
the most frequent single pathogen causing surgical-site
and bloodstream infections. Gram-negative bacilli were
isolated in just under half of surgical-site infections
(table 3). In view of the few isolates and heterogeneous
geographic distribution, country-specific and region-
specific pathogen distribution was not investigated. Apart
from meticillin resistance, reported in 54% of S aureus
isolates (158/290) from eight studies,43–45,58,138,149,151,164 very
few articles included data about antimicrobial resistance
patterns and no assessment of this aspect was done.
In this systematic review and meta-analysis, we have
shown that endemic health-care-associated infection
represents a major burden and safety issue for patients in
the developing world, with an even greater epidemiological
relevance than in developed countries. Compared with
average prevalence of health-care-associated infection in
Europe (reported as 7·1 per 100 patients by the European
Centre for Disease Prevention and Control)172 and estimated
incidence in the USA (4·5 per 100 patients in 2002),173
pooled prevalence of health-care-associated infection in
resource-limited settings is substantially higher, particularly
in high-quality studies (15·5 per 100 patients).
The difference between developing and developed
countries is even more striking when considering incidence
of ICU-acquired infection (pooled density 47·9 per
1000 patient-days in developing countries), which is
estimated to be 13·6 per 1000 patient-days in the USA.173
Although invasive devices represent an unavoidable
infection risk for the critically ill patient, this risk goes well
beyond an acceptable level in the developing world,
especially for incidence of ventilator-associated pneumonia
and catheter-related bloodstream infections in both adult
and paediatric patients. In our review, pooled densities of
device-associated infection in critically ill adult patients
from comparable studies were two to eight times higher
than those reported by the US NNIS/NHSN98,99 and the
German hospital infection surveillance system (table 2).100,101
Pooled data from some low-income and middle-income
countries even showed densities up to 19 and 16 times
higher for catheter-related bloodstream infections and
ventilator-associated pneumonia, respectively. Our findings
also indicated that ventilator-associated pneumonia is the
most frequent type of health-care-associated infection in
this population of patients (figure 4D).9
Zaidi and colleagues8 reported neonatal infection rates
three to 20 times higher in resource-limited countries
than in industrialised nations. Our analysis confirms

234 www.thelancet.com Vol 377 January 15, 2011


these data, with the finding that the density of overall
health-care-associated infections in neonatal ICUs in
some countries (eg, Brazil)109–112 is up to nine times higher
than in the USA (6·9 infections per 1000 patient-days vs
15·2–62·0 infections per 1000 patient-days in our
review).173 Importantly, very high rates
health-care-associated infection in neonatal and paediatric
populations were noted not only in ICUs but also in
some paediatric wards and children’s hospitals.103,106,107,174
Our findings indicate that surgical-site infection is both
the most frequently studied and the leading
health-care-associated infection hospital-wide in the
developing world. The alarming global burden of
avoidable complications resulting from unsafe surgery
has been highlighted by WHO.175,176 The frequency of
surgical procedures complicated by surgical-site infection
was significantly higher in our study of developing
nations compared with those recorded in high-income
countries (pooled cumulative incidence 5·6 per
100 surgical procedures in our study). For example, in a
nationwide study undertaken in the USA,177 the
cumulative incidence of surgical-site infection was
2·6 per 100 surgical procedures; similarly, it was 2·9 per
100 surgical procedures in different European countries,178
and 1·6 per 100 procedures in Germany.100 Frequencies of
surgical-site infection according to wound class were very
high in all categories when compared with data reported
in the USA.179
Assessment of microbiological patterns of health-care-
associated infection was based on only a few isolates.
Therefore, we should be cautious about attributing a role
to some microorganisms as causative pathogens of
specific health-care-associated infections. Limitations in
microbiological assessment are highlighted by the paucity
of information on antimicrobial resistance.180 Apart from
the high level of meticillin resistance seen in S aureus
isolates, we could not provide information on other
resistance patterns in our present review.
What are the important determinants of a high burden
of health-care-associated infection in developing
countries? With available evidence, this question is
difficult to answer, particularly since information on risk
factors is scanty (data not shown). However, potential
determinants include:8,181,182 inadequate environmental
hygienic conditions; poor infrastructure; insufficient
equipment; understaffing; overcrowding; paucity of
knowledge and application of basic infection-control
measures; prolonged and inappropriate use of invasive
devices and antibiotics; and scarcity of local and national
guidelines and policies. Although judged the most
important measure for prevention of microbial
transmission during patient care, hand hygiene is very
often neglected by health-care workers in settings with
limited resources, as shown repeatedly by adherence of
less than 20% in a growing number of reports.157,183–188
Another widespread unsafe practice in developing
countries is reuse of equipment (needles, gloves) because
www.thelancet.com Vol 377 January 15, 2011
Articles
resources are scarce. In 2000, WHO estimated that
39·3% of injections in developing countries were done
with reused equipment.189 The main outcome of
contaminated injections was an estimated 21 million
hepatitis B infections, 2 million hepatitis C infections,
of and 260 000 HIV infections. Sharing of syringes caused a
large-scale nosocomial outbreak of HIV affecting
39 patients at two renal dialysis centres in Egypt.190
Although these types of infection are not the topic of our
report, bacterial pathogens can possibly be transmitted
through the same route.
While mapping the endemic situation of
health-care-associated infection in developing countries,
we noted a paucity of available data and a fragmented
picture, with some regions and many countries poorly
represented (figure 2). National or multicentre
surveillance reports were available from only a few low-
income and middle-income countries, whereas
43 national and 50 multicentre studies undertaken in the
developed world were published, according to the same
search criteria (data not shown). The paucity of national
reports accords with findings of a survey done by WHO,
in which only 23 of 147 developing countries (16%)
reported a functioning national surveillance system.191
Furthermore, according to the European Centre for
Disease Prevention and Control, only four of 26 (15%)
countries of low and middle income in Europe have
implemented surveillance protocols for health-care-
associated infection at national level.172
The emerging picture clearly indicates that major
difficulties exist for implementation of surveillance for
health-care-associated infection in developing countries.
The main reasons can be traced to an absence of expertise
and dedicated human and financial resources and to the
existence of other important health-care priorities
(panel 2). Use of standardised definitions is limited by
the scarcity and frequent unreliability of microbiological
data and other diagnostic procedures, inaccuracy of
information from patients’ records, and a paucity of
electronic records and software or databases for
surveillance of health-care-associated infection.
Furthermore, expertise in data interpretation—and a
leadership commitment to use data for raising awareness
and intervention—is sometimes absent.
About half of studies in our review were of overall low
quality, mainly indicated by use of non-standardised
definitions and suboptimum surveillance methods. For
this reason, comparison of data from different studies
proved to be challenging. Furthermore, about two-thirds
of studies were undertaken at single hospitals or on one
ward, and findings from these cannot be deemed
representative of the endemic situation of
health-care-associated infection in specific countries.
Similarly, half of all studies were done in teaching
hospitals, in which rates of health-care-associated infection
are usually higher. Thus, generalisability of these data to
all settings is questionable. These technical constraints,
235
 Articles
Panel 2: Surveillance constraints and perspectives for improvement and research of
health-care-associated infection in developing countries
Appropriate surveillance constraints
• Paucity of dedicated human resources and funds
• Scarcity of expertise in epidemiology and infection control
• Difficulties in application of standard definitions:
• limited expertise to distinguish between infection, colonisation, and
contamination
• shortage of reliable microbiological and other diagnostic methods
• poor-quality information from patients’ records
• need to evaluate clinical evidence
• Absence of skills for data interpretation and use
• Sparse or insufficient microbiological laboratory capacity
• Existence of different payer sources
Perspectives for improvement and research
• Improve reporting of information in clinical records
• Ensure minimum requirements in terms of facilities and resources available for
surveillance
• Improve capacity-building for clinical microbiological laboratories
• Ensure that core components for infection control are in place
• Promote staff education on infection control and surveillance of
health-care-associated infection
• Undertake research to adapt and validate definitions of health-care-associated
infection and protocols for its surveillance on the basis of the reality of developing
countries
• Undertake research on patients’ and relatives’ education and involvement in
detection and reporting of health-care-associated infection
and variations in settings, account at least partly for the
reported heterogeneity in all study categories.
Despite our broad selection criteria and extensive
search of several databases, only a fairly limited number
of articles were retrieved by our literature search. Studies
might have been done but not published or published in
abstract form only. Moreover, although endemic rates of
health-care-associated infection reported in intervention
studies were included in this Article, further data could
be available from non-population-based randomised
clinical trials not retrieved by our search.
Overall health-care-associated infection has a great effect
on health-care facilities, national health-care systems, and
patients. Unfortunately, in studies retrieved by our search,
findings related to increased length of stay and attributable
mortality and costs associated with health-care-associated
infection (data not shown) were fragmentary, differed
strikingly between studies, and methods to calculate
variables were seldom reported. For these reasons, we did
not include information on this topic. Reliable and
systematic data—specific to country and setting—about
the effect of health-care-associated infection are needed
urgently, including investigation of the relation between
rates of health-care-associated infection and a country’s
gross domestic product. This area of research should be
developed to inform policy makers about the most efficient
use of available resources.
236
Our data have the potential to alert policy makers and
decision makers to the fact that health-care-associated
infection represents a hidden and serious burden for
systems and patients alike. Since 2005, 88 UN member
states of 147 developing countries (60%) have committed
to reduce health-care-associated infection by signing the
pledge of WHO’s First Global Patient Safety Challenge,
together with 36 governments from 46 developed
countries (78%).3,192 Action is now required, and
investment of human and financial resources is
necessary; perspectives for improvement and research
are proposed (panel 2). Setting up the core components
for infection control identified by WHO193 could represent
an important starting point to reduce the burden of
endemic health-care-associated infection and guarantee
better preparedness. In many cases, measures to prevent
health-care pathogen transmission are low-cost, such as
hand hygiene.4,184,194,195 Staff education is a key element,
needing fairly limited efforts, and basic principles of
infection control should be included in curricula of
doctors, nurses, and other health-care professions.196
Relevant efforts are being made by international networks
(eg, African Partnership for Patient Safety, Infection
Prevention and Control African Network, International
Federation of Infection Control, International Nosocomial
Infection Control Consortium, Réseau International
pour la Planification et l’Amélioration de la Qualité et de
la Sécurité dans les Systèmes de Santé en Afrique) to
build infection surveillance and control skills in
developing countries, but apart from the International
Federation of Infection Control and International
Nosocomial Infection Control Consortium, most are at
an early stage. The European Centre for Disease
Prevention and Control is also currently coordinating
surveillance and infection-control activities in Europe,
including some countries of low and middle income.
A finding of our meta-analysis was that reported
incidence densities of health-care-associated infection,
catheter-related bloodstream infection, and catheter-related
urinary-tract infection in the ICU have fallen substantially
over recent years. In most papers that reported these
findings, regular surveillance data had been gathered by
coordination of the International Nosocomial Infection
Control Consortium.65,66,68,72,73,78,81,86,91 Therefore, the recorded
decrease probably represents mostly the effect of
surveillance per se and the effect of interventions
implemented by this network.91,197–199 We also noted that
most papers (162/220) retrieved through our review were
published from 2003 onwards, thus indicating that
surveillance activities have increased over the past 6 years.
An improvement in surveillance of health-care-associated
infection is essential to record the size of this infection
burden and the effect of interventions. Moreover, by itself,
surveillance can lead to reduction in health-care-associated
infection.100,200 Further research to investigate adaptation
and validation of standardised protocols and definitions
affordable in developing countries is very much needed.
www.thelancet.com Vol 377 January 15, 2011

Criteria for definition of health-care-associated infection,
mostly on the basis of clinical elements, should be
identified and their predictive values assessed by
comparison with the most frequently used international
definitions.11 In view of the important role of relatives and
patients in health-care provision in developing countries,
and to offset the effect of understaffing, affected
individuals and their family members could be instructed
to recognise and report signs of infection.201 For instance,
this approach could help with detection of surgical-site
infections, both during hospital stay and after discharge.
An additional option is to prioritise process control,202
which is easy to undertake and could provide information
on adherence to practices and the effect of interventions,
thus potentially improving patients’ safety. As a result of
improved surveillance of health-care-associated infection
worldwide, and with the objective to raise awareness
among policy makers and health-care workers, now could
be the time to investigate epidemiological models that
allow inclusion of health-care-associated infection in the
list of major diseases causing morbidity, mortality, and
disability, which are regularly reported by WHO and other
institutions within global estimates of burden of disease.6
Contributors
BA and DP had the idea for the project. SBN undertook searches of
published work and did data extraction. BA reviewed data by
independently reading the full articles. Statistical analysis and
elaboration of figures was done by CC, WG, and HA. BA wrote the paper
with important contributions from DP and input from SBN, CC, and
HA. SLD provided valuable comments on the report. All authors had full
access to all data in the study and read and approved the final version.
Conflicts of interest
We declare that we have no conflicts of interest.
Acknowledgments
We thank Stephan Harbarth (University of Geneva Hospitals and Faculty of
Medicine, Geneva, Switzerland) and Edward Kelley and Colin Mathers
(Evidence and Information and Research Cluster, WHO Headquarters,
Geneva, Switzerland) for useful comments on the report; Rosemary Sudan
(University of Geneva Hospitals and Faculty of Medicine, Geneva,
Switzerland) for her substantial editing contribution to the manuscript;
Elizabeth Mathai (Evidence and Information and Research Cluster, WHO
Headquarters, Geneva, Switzerland) for her support in assessment of
microbiological data; Petra Gastmeier (Charité-University Medicine, Berlin,
Germany) for advice on data comparison with the German Krankenhaus
Infektions Surveillance System; and the Public Health Information and
Geographic Information Systems team at the Evidence and Information and
Research Cluster (WHO Headquarters, Geneva, Switzerland), for
preparation of figure 2. A part of these data was presented at the
50th Interscience Conference on Antimicrobial Agents and Chemotherapy,
Boston, MA, USA, September 12–15, 2010 (posters K-254 and K-1721). This
work was funded by WHO. WHO takes no responsibility for the
information provided or the views expressed in this report. ©World Health
Organization, 2010.
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