Clinical Management of Bacterial Pneumonia

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Contents
Author biographies vii
Abbreviations ix
Preface xi

1 Introduction to pneumonia 1
Introduction 1
Overview of bacterial pneumonia 1
References 4

2 Epidemiology, etiology, and risk factors of bacterial 7

pneumonia
Epidemiology 7
Microbial etiology 11
Antibiotic resistance 15
Risk factors 19
Summary points 23
References 23

3 Pathology and clinical features of pneumonia 29

Pathophysiology of pneumonia 29
Pathogenesis of pneumonia 34
Signs and symptoms of pneumonia 34
Prognosis of pneumonia 35
Summary points 36
References 36

4 Diagnosis and classification of pneumonia 39

Diagnosis and classification of hospital-acquired and 39
ventilator-associated pneumonia
Diagnosis of community-acquired pneumonia 40

v
vi • CO NTE NTS

Summary points 54
References 54

5 Methods for preventing pneumonia 57

Guidelines for the prevention of pneumonia 57
Preventative strategies to reduce the risk of community-acquired 58
pneumonia in adults
Nonpharmacological prevention of hospital-acquired 61
and ventilator-associated pneumonia
Vaccination 63
New vaccines 68
Summary points 68
References 69

6 Management of pneumonia 75
Guidelines for management and treatment of pneumonia 75
Medical management of pneumonia 77
Guidelines for the antimicrobial treatment of community-acquired 80
pneumonia
Guidelines for the antimicrobial treatment of hospital-acquired/ 81
ventilator-associated pneumonia
Emerging therapies for the treatment of community-acquired 84
pneumonia
Emerging therapies for the treatment of hospital-acquired/ 88
ventilator-associated pneumonia
Management of pneumonia in special populations 89
Summary points 94
References 94
Author biographies
Antoni Torres, MD, is a Professor of Medicine at the University of
Barcelona. Born in Barcelona in 1954, he is Full Professor of Medicine
at the University of Barcelona and Head of the Respiratory Intensive
Care Unit at Hospital Clínic Barcelona. He is considered a physician of
reference both nationally and internationally in lung infections, including
pneumonia, chronic obstructive pulmonary disease, bronchiectasis,
immunocompromised patients, ventilation weaning, noninvasive
ventilation, and acute respiratory distress syndrome. He leads the
research group on Applied Research in Respiratory Diseases of the Institut
d’Investigacions Biomèdiques August Pi i Sunyer (IDIBAPS), from where
he facilitates translational research studies. He also coordinates a CIBER
group on respiratory diseases (Ciberes) and takes part in several European
projects. He is co-author of more than 300 scientific publications, has
supervised 24 PhD theses, and his H-Index is 97.
Professor Torres has been the recipient of several awards, including
the Edward Shanoff award (1988), the Josep Trueta Award (2001), the
Fundación de Ciencias de la Salud (2001) award for the 10 best biomedi-
cal researchers in the last 4 years, the Lilly Foundation Award (2007)
and the Award EUROPE ASPIRE (2011). He was awarded to “the profes-
sional excellence in Investigation” of the COMB (College of Physicians),
2013 and received the “ICREA Academia” award from the University
of Barcelona (2013). He also holds a Fellowship of the ERS (European
Respiratory Society) for the contribution to research in the respiratory
field (2014). He is also member of several societies and is the President of
the area of tuberculosis and respiratory infections of the Spanish Society
of Pneumology and Thoracic Surgery (SEPAR) and President of the area of
respiratory infections of the Latin American Thorax Association (ALAT).

vii
VIII • AUTHOR BIOGRAPHIES

Catia Cillóniz Campos, PhD, is a Doctor in Medicine at the University

of Barcelona. She holds a degree in Biology from the San Luis Gonzaga
National University in Peru and has a Masters in Advanced Microbiology
and Masters in SIDA from University of Barcelona. She is a researcher
within the Applied Research in Respiratory Diseases team, where she
coordinates the research line of community-acquired pneumonia (CAP).
Her research and clinical interests are in the microbial etiology of CAP,
determining the direct or indirect relationship of the different microor-
ganisms with the severity and course of the infection, or describing the
course of the different etiologic agents, the type of presentation observed
in hospitals and associated comorbidities. She also works on hospital-
acquired pneumonia, where she records and monitors the epidemiol-
ogy, clinical presentation, etiology, and outcome factors of disease. Her
research goal is to determine the etiology of CAP, its clinical presenta-
tion, severity, resistance, and to contribute to evolving diagnostic tests
to identify the etiologic agents with greater accuracy.
Dr. Cillóniz has been awarded with the University of Barcelona
Extraordinary Doctorate Prize for the academic year 2011/2012. This
award recognizes the quality of some of the theses developed and approved
at the University of Barcelona which have obtained the Excellent Cum
Laude qualification. She has published over 40 articles on CAP in peer-
review journals since 2007 and is a member of the European Society
of Clinical Microbiology and Infectious Diseases (ESCMID), Spanish
Society of Pneumology and Thoracic Surgery (SEPAR), and the European
Respiratory Society (ERS).
Abbreviations
ARDS Acute respiratory distress syndrome
ATS American Thoracic Society
BAL Bronchoalveolar lavage
BAS Bronchial aspirate
BLI β-lactamase inhibitor
Bpm Beats per minute
br Breaths
BTS British Thoracic Society
CABP Community-acquired bacterial pneumonia
CA-MRSA Community-acquired methicillin-resistant
Staphylococcus aureus
CAP Community-acquired pneumonia
CFU Colony-forming units
COPD Chronic obstructive pulmonary disease
CRM197 Cross-reactive material197
CRP C-reactive protein
CT Computerized tomography
CXR Chest X-ray
DRSP Drug resistant Streptococcus pneumoniae
Erm(B) Erythromycin ribosome methylation
ERS European Respiratory Society
ESBL Extended spectrum β-lactamases
ESCMID European Society of Clinical Microbiology and
Infectious Diseases
FiO2 Fraction of inspired oxygen
HAP Hospital-acquired pneumonia
HIV Human immunodeficiency virus
ICU Intensive care unit
IDSA Infectious Diseases Society of America
IgM Immunoglobulin M
IPD Invasive pneumococcal disease
IRVS Intensive respiratory or vasopressor support
ix
x • ABBREVIATIONS

IV Intravenous
MDR Multidrug-resistant
MIC Mean inhibitory concentration
mprF Multipeptide resistance factor
MRSA Methicillin-resistant Staphylococcus aureus
MRSE Methicillin-resistant Staphylococcus epidermidis
MSSA Methicillin-sensitive Staphylococcus aureus
MSSE Methicillin-sensitive Staphylococcus epidermidis
MV Mechanical ventilation
NBP Nosocomial bacterial pneumonia
NP Nosocomial pneumonia
NV-ICUAP Nonventilated ICU-acquired pneumonia
OR Odds ratio
PaO2 Partial arterial oxygen pressure
PBPs Penicillin-binding proteins
PcpA Pneumococcal choline-binding protein A
PCV Pneumococcal conjugate vaccine
PhtD Pneumococcal histidine triad protein D
PLT Platelets
PORT Pneumonia Patient Outcomes Research Team
PPSV Pneumococcal polysaccharide vaccine
PSB Protected specimen brushing
PSI Pneumonia Severity Index
PTC Protected telescoping catheter
PVL Panton-Valentine leukocidin
QRDR Quinolone resistance determinant region
RR Respiratory rate
VAP Ventilator-associated pneumonia
VE-VAP Very early-onset ventilator-associated pneumonia
VISA Vancomycin intermediate Staphylococcus aureus
VRSA Vancomycin-resistant Staphylococcus aureus
WBC White blood cell
yo Years old
Preface
Despite many advances in antibiotic therapies, diagnostic tools and
strategies for prevention, pneumonia is still the primary cause of death
from infectious disease worldwide. The key factor for the increased
mortality is the effect of pneumonia on comorbidities and underlying
diseases, along with the rising age of the population and the virulence
of the pathogens. The increasing number of antibiotic-resistant bacteria
is a matter of concern for clinicians when choosing antibiotic treatment
in patients with pneumonia. In general, the management of pneumonia
presents a major challenge for the clinicians. The optimum outcome
for pneumonia can be achieved by careful risk stratification, accurate
assessment of severity, and appropriate antibiotic therapy.
In the last decade several international and national societies have
released guidelines for the management of pneumonia (community- and
hosptial-acquired pneumonia), including recommendations for initial
antibiotic treatment, microbiological testing, decision to hospitalize and
admit to the intensive care unit, and management of non-responding
patients. Recent studies show that implementation of guidelines for the
management of pneumonia is followed by improvement in outcomes,
including mortality.
This handbook summarizes important features and management
issues of bacterial pneumonia, including the latest information on micro-
biological etiology, clinical course, diagnostic testing, and antimicrobial
treatment and prevention.

xi
 Chapter 1

Introduction to pneumonia
Introduction
Pneumonia is an infection that involves a complex set of steps, beginning
with initial contact with a pathogenic microorganism and culminating in
the invasion of the lower respiratory tract. This infection can be acquired
in the community or within the hospital setting, and can be transmitted
by aspirated or inhaled microorganisms.
Pneumonia is a severe health problem and a significant cause of mor-
tality and morbidity worldwide. In 2013, pneumonia was the eighth most
common cause of death in the United States [1]. In the US alone it is respon-
sible for approximately 1.1 million hospital admissions, 50,000 deaths,
and close to 14,000 hospital readmissions per year [1,2]. Pneumonia can
be bacterial, viral, or fungal (but most commonly bacterial). It is impor-
tant to understand the role of the different pathogens in the microbial
etiology of pneumonia to effectively manage and guide appropriate
antibiotic therapy. This handbook will focus on bacterial pneumonia and
will cover the most clinically relevant information, including important
features of pneumonia, microbial etiology, clinical course, diagnostic
testing, management issues, and antimicrobial treatment and prevention.

Overview of bacterial pneumonia

Hospital-acquired pneumonia
Hospital-acquired (nosocomial) pneumonia (HAP) is defined as pneu-
monia that develops 48 hours or more after admission, which was

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A. Torres and C. Cillóniz, Clinical Management of Bacterial Pneumonia,
DOI 10.1007/978-3-319-22062-8_1
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not incubating at the time of admission, or pneumonia that occurs

in intubated patients (Box 1.1) [3]. HAP is the second most frequent
nosocomial infection worldwide, affecting 0.5 to 1.7% of hospitalized
patients (although this number may be higher in a hospital ward or in the
intensive care unit [ICU] where cases of HAP are more severe), and is the
leading cause of mortality among all hospital nosocomial infections [4].
HAP accounts for 50% of all antibiotics administered in the hospital
setting and has significant impact on health care costs [5–8]. HAP is a
dynamic disease with a changing natural history, multiple etiologies,
and numerous risk factors.
Ventilator-associated pneumonia (VAP) is defined as pneumonia
that arises more than 48 to 72 hours after endotracheal intubation
(Box 1.1) [9–11]. VAP is the most frequent nosocomial infection in the
ICU setting, representing approximately 70 to 80% of HAP cases in the
ICU (Box 1.1). Pneumonia accounts for approximately a quarter of all
infections in the ICU, and a third to half of all nosocomial pneumonia
deaths are directly attributable to the pneumonia itself [12,13].
HAP is divided into two groups:
1. Early-onset — usually occurs within the first 4 days of
hospitalization and is most frequently caused by ‘community’
pathogens such as Streptococcus pneumoniae, Haemophilus
influenzae, and anaerobes;
2. Late-onset — usually occurs after the fifth day of hospitalization
and is mainly caused by methicillin-resistant Staphylococcus aureus
(MRSA), enteric Gram-negative bacilli, Pseudomonas aeruginosa,
nonfermenting bacteria (eg, Acinetobacter baumanii and
Stenotrophomonas maltophilia), and polymicrobial infections [3].
Early-onset HAP tends to carry a better prognosis than late-onset HAP because
of the association of the latter with multidrug-resistant (MDR) organisms.
The mortality rate of HAP ranges from 30 to 70% and is associated
with a poor outcome when treatment is delayed or when inadequate
antibiotic therapy is used. Despite antimicrobial therapy and advances
in supportive care, the mortality rate increases if the infection is caused
by MDR pathogens [3,5,14].
 I N T R O D U C T I O N TO P N EU M O N I A • 3

Hospital-acquired pneumonia (HAP) Alveolar infection that was neither present nor
incubating at the time of hospital admission
and that develops after 48 hours or more after
hospital admission
Ventilator-associated pneumonia (VAP) Pneumonia occurring after 48 hours of
endotracheal intubation and starting
mechanical ventilation
Early-onset nosocomial pneumonia Pneumonia developing usually within the first
4 days of hospitalization
Late-onset nosocomial pneumonia Pneumonia occurring usually after the fifth
day after hospital admission

Box 1.1 Definitions in nosocomial pneumonia.

Community-acquired pneumonia
Community-acquired pneumonia (CAP) is a serious health problem
associated with high morbidity and mortality in all age groups world-
wide [15]. CAP is the sixth leading cause of death worldwide and is a major
burden on health care resources [15]. In the United States pneumonia
and influenza together caused 50,000 deaths in 2010 — the ninth leading
cause of death in this territory [16]. In Europe the mortality rates of CAP
vary widely from country to country, ranging between <1% and 48% [17].
In a comprehensive literature review, Torres et al [18] found the overall
annual incidence of CAP in Europe to be between 1.07 to 1.2 per 1000
person-years and 1.54 to 1.7 per 1000 population. In the same review it
was found that the incidence of CAP increased with age to 14 per 1000
person-years in adults aged ≥65 years, and the incidence of CAP was
significantly higher in men than in women [18]. The incidence of CAP
has also been found to increase with comorbid disease [17].
An increase of 34% in hospital admissions due to CAP has been
described over the last decade [19], especially in the elderly [20]. Among
hospitalized patients, approximately 10% required admission to the ICU.
Mortality rates in the outpatient setting are low (<3%), but are higher
(8 to 20%) among patients admitted to a medical ward, and are highest
(up to 50%) in patients admitted to the ICU [21].
Presentation of CAP may vary in severity from a mild disease,
managed with outpatient care (50 to 80% of CAP cases), to a very severe
illness requiring hospital (20 to 50% of CAP cases) or ICU admission
4 • CL INI C A L MA N AG E M E NT O F B AC T E RIA L P N E U M O N IA

(approximately 10% of CAP cases) [22–24]. Severity tools [25,26] in

conjunction with clinical assessment are recommended by all guidelines
for the management of adults with CAP [15,27]. Clinical diagnosis of
CAP is based on the presence of select clinical features and supported by
imaging of the lung and physical examination to complement the diagnosis.
Microbiological investigations may support the diagnosis of pneumonia,
with bacteria being the most common causative microorganisms (notably
S. pneumoniae). However, defining an etiologic agent is challenging and
the etiology of CAP remains unknown in up to 50% of the cases when
routine tests are performed. Even though early empirical therapy is often
necessary, it is still important to identify the etiologic agent to effectively
guide appropriate antibiotic management and reduce unnecessary anti-
biotic therapy use.
The appropriate diagnosis and management of pneumonia is made
more challenging by increases in average life expectancy across the
globe and an accompanying increase in the number of patients who
have age-related comorbidities, who are institutionalized, or who are
immunocompromised. Further complexity is brought about by the wide
diversity of pathogens that cause pneumonia, especially those that are
antibiotic resistant.

References
1 Kochanek KD, Murphy SL, Xu J, Arias E. Mortality in the United States, 2013. NCHS Data Brief.
2014;178:1–8.
2 Elixhauser A, Steiner C. Readmissions to U.S. Hospitals by Diagnosis, 2010: Statistical Brief
#153. 2013 Apr. In: Healthcare Cost and Utilization Project (HCUP) Statistical Briefs [Internet].
Rockville (MD): Agency for Health Care Policy and Research (US); 2006 Feb-. Available from:
http://www.ncbi.nlm.nih.gov/books/NBK154385/
3 American Thoracic Society, Infectious Diseases Society of America. Guidelines for the
management of adults with hospital-acquired, ventilator-associated, and healthcare-
associated pneumonia. Am J Respir Crit Care Med. 2005;171:388–416.
4 Nair GB, Niederman MS. Nosocomial pneumonia: lessons learned. Crit Care Clin. 2013;29:521–546.
5 Chastre J, Fagon JY. Ventilator-associated pneumonia. Am J Respir Crit Care Med.
2002;165:867–903.
6 Kollef MH, Hamilton CW, Ernst FR. Economic impact of ventilator-associated pneumonia in a
large matched cohort. Infect Control Hosp Epidemiol. 2012;33:250–256.
7 Restrepo MI, Anzueto A, Arroliga AC, et al. Economic burden of ventilator-associated
pneumonia based on total resource utilization. Infect Control Hosp Epidemiol. 2010;31:509–515.
8 Rello J, Ollendorf DA, Oster G, et al. Epidemiology and outcomes of ventilator-associated
pneumonia in a large US database. Chest. 2002;122:2115–2121.
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9 Richards MJ, Edwards JR, Culver DH, Gaynes RP. Nosocomial infections in combined
medical-surgical intensive care units in the United States. Infect Control Hosp Epidemiol.
2000;21:510–515.
10 Esperatti M, Ferrer M, Theessen A, et al. Nosocomial pneumonia in the intensive care unit
acquired during mechanical ventilation or not. Am J Respir Crit Care Med. 2010;182:1533–1539.
11 Vincent JL, Rello J, Marshall J, et al. International study of the prevalence and outcomes of
infection in intensive care units. JAMA. 2009;302:2323–2329.
12 Flanders SA, Collard HR, Saint S. Nosocomial pneumonia: state of the science. Am J Infect
Control. 2006;34:84–93.
13 Torres A, Ewig S, Lode H, Carlet J. Defining, treating and preventing hospital acquired
pneumonia: European perspective. Intensive Care Med. 2009;35:9–29.
14 Uvizl R, Hanulik V, Husickova V, Sedlakova MH, Adamus M, Kolar M. Hospital-acquired
pneumonia in ICU patients. Biomed Pap Med Fac Univ Palacky Olomouc Czech Repub.
2011;155:373–378.
15 Mandell LA, Wunderink RG, Anzueto A, et al. Infectious Diseases Society of America/
American Thoracic Society consensus guidelines on the management of community-
acquired pneumonia in adults. Clin Infect Dis. 2007;44 (Suppl 2):S27–S72.
16 Murphy SL, Xu JQ, Kochanek KD. Deaths: Preliminary data for 2010. National vital statistics
reports. 2012;60.
17 Welte T, Torres A, Nathwani D. Clinical and economic burden of community-acquired
pneumonia among adults in Europe. Thorax. 2012;67:71–79.
18 Torres A, Peetermans WE, Viegi G, Blasi F. Risk factors for community-acquired pneumonia in
adults in Europe: a literature review. Thorax. 2013;68:1057–1065.
19 Trotter CL, Stuart JM, George R, Miller E. Increasing hospital admissions for pneumonia,
England. Emerg Infect Dis. 2008;14:727–733.
20 Fry AM, Shay DK, Holman RC, Curns AT, Anderson LJ. Trends in hospitalizations for
pneumonia among persons aged 65 years or older in the United States, 1988-2002. JAMA.
2005;294:2712–2719.
21 Restrepo MI, Mortensen EM, Velez JA, Frei C, Anzueto A. A comparative study of community-
acquired pneumonia patients admitted to the ward and the ICU. Chest. 2008;133:610–617.
22 Minogue MF, Coley CM, Fine MJ, Marrie TJ, Kapoor WN, Singer DE. Patients hospitalized
after initial outpatient treatment for community-acquired pneumonia. Ann Emerg Med.
1998;31:376–380.
23 Niederman MS, Bass JB Jr, Campbell GD, et al. Guidelines for the initial management of
adults with community-acquired pneumonia: diagnosis, assessment of severity, and initial
antimicrobial therapy. American Thoracic Society. Medical Section of the American Lung
Association. Am Rev Respir Dis. 1993;148:1418–1426.
24 Dwyer R, Hedlund J, Darenberg J, et al. Improvement of CRB-65 as a prognostic scoring
system in adult patients with bacteraemic pneumococcal pneumonia. Scand J Infect Dis.
2011;43:448–455.
25 Fine MJ, Auble TE, Yealy DM, et al. A prediction rule to identify low-risk patients with
community-acquired pneumonia. N Engl J Med. 1997;336:243–250.
26 Lim WS, van der Eerden MM, Laing R, et al. Defining community acquired pneumonia
severity on presentation to hospital: an international derivation and validation study.
Thorax. 2003;58:377–382.
27 Lim WS, Baudouin SV, George RC, et al. BTS guidelines for the management of community
acquired pneumonia in adults: update 2009. Thorax. 2009;64 (Suppl 3):iii1–55.
 Chapter 2

Epidemiology, etiology, and risk

factors of bacterial pneumonia
Epidemiology

Hospital-acquired pneumonia
Hospital-acquired pneumonia (HAP) is the second most common noso-
comial infection after urinary tract infections. The incidence of HAP
ranges from 5 to 15 cases per 1000 hospital admissions, and is a frequent
problem in general wards (incidence ranging from 1.6 to 3.67 cases per
1000 admissions) [1–3]. In the case of patients admitted to an intensive
care unit (ICU), HAP occurs in up to 25% of patients [4], with approxi-
mately 70 to 80% of episodes occurring during mechanical ventilation
(MV) [5] (Figure 2.1).

Incidence of HAP
5 to 15 cases per 1000 hospital admissions

ICU HAP occurs in up to 25% of all

admitted patients

Approximately 70 to 80% of episodes Approximately 20 to 30% of episodes of

of HAP occur during MV HAP occur in nonventilated ICU patients

Figure 2.1 Distribution of hospital-acquired pneumonia [1–5]. HAP, hospital-acquired

pneumonia; ICU, intensive care unit; MV, mechanical ventilation.

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The incidence of HAP in the ICU varies by geographic area (Table 2.1). In
the United States, the National Nosocomial Infection Surveillance data
found that 31% of all nosocomial infections in combined medical–surgical
ICUs were due to pneumonia, with 83% of cases being ventilator-associ-
ated pneumonia (VAP) [6]. In Europe, a large Italian study in 125 ICUs
(which included 34,472 patients) reported that 9.1% of all admitted
patients developed nosocomial infections, and pneumonia (specifically
VAP) was the most prevalent (48.7%) ICU-acquired infection [7]. In a
prevalence study of 254 ICUs in Mexico, 23.2% of patients had an ICU-
acquired infection, and VAP was the most prevalent infection (41.2%) [8].
According to a study in Asian hospitals, the proportion of ICU-acquired
respiratory infections ranges from 9 to 23% [9].
Most of the currently available studies on HAP have focused on
ventilated patients; there are few studies on HAP in nonventilated ICU-
acquired pneumonia (NV-ICUAP). One study that compared VAP and
NV-ICUAP in a population of 315 patients with ICU-acquired pneumonia,
found that 52% of patients had VAP and 48% had NV-ICUAP [5].
With all the data available relating to HAP in the ICU we can say that
HAP represents one of the most common nosocomial infections world-
wide and VAP is the most common nosocomial infection diagnosed in
the ICU. The true incidence of NV-ICUAP remains uncertain.

Community-acquired pneumonia
Since community-acquired pneumonia (CAP) is not a reportable disease,
its true incidence remains uncertain. Only 20 to 50% of patients with
CAP require hospitalization. The overall annual incidence of CAP in
adults in Europe ranges between 1.07 and 1.20 per 1000 person-years
and 1.54 and 1.70 per 1000 population and increases with age (14 per
1000 person-years in adults aged ≥65 years) [22] (Table 2.2). CAP most
frequently affects individuals at extremes of age and those with any type
of coexisting illness [22–24]. The study by Torres et al [22] reported an
increased risk of CAP in men (compared with women) and in patients
≥65 years of age.
Based on data from a systematic literature review, Said et al [28]
estimated that the proportion of pneumococcal pneumonia that is
 Study Country/Year of publication Study period Population Incidence
Torres et al [10] Spain/1991 April 1987 to May 1988 VAP 78 (24%) per 322 cases
Rello et al [11] Spain/1991 January 1988 to November 1989 VAP 58 (21.9%) per 264 cases
Joseph et al [12] India/2009 October 2006 to December 2007 VAP 22.94 per 1000 ventilator days
Blot et al [13] Belgium, France, Germany, The period of data collection was VAP 14.6% in patients 45 to 64 years of age
Greece, Italy, Ireland, Portugal, 6 months 17.0% in patients 65 to 74 years of age
Spain, and Turkey/2014 12.8% in patients ≥75 years of age
Suka et al [14] Japan/2007 July 2002 and June 2004 VAP 53.4%
6.5 cases per 1000 patient-days
Sopena et al [15] Spain/2014 January 2006 and April 2008 Non-ICU 2.45 cases per 1000 hospital admissions
HAP (95% CI, 2.04–2.92)
Barreiro-Lopez et al [16] Spain/2005 November 1997 to January 1999 Non-ICU 3.35 cases per 1000 hospital admissions
HAP
Franzetti et al [17] Italy/2006 January 1988 and December NBP (HIV) 24 cases per 1000 inpatient/year
2002
Weber et al [18] USA/2007 2000 to 2003 HAP/VAP 0.37 cases per 1000 hospital admissions
Diouf et al [19] France/2006 January to December 2002 VAP 7.16 per 100 admitted patients and 50 per 100
ventilated patients
Koulenti et al [20] Belgium, France, Germany, HAP/VAP 75.9% NP
Greece, Italy, Ireland, Portugal, 20.5% HAP
Spain, and Turkey/2009 42.7% VAP
12.7% VE-VAP
Japoni et al [21] Iran/2011 June 2008 and March 2009 HAP/VAP 6.9% NP, of which 72% were VAP

Table 2.1 Incidence of hospital-acquired pneumonia. HAP, hospital-acquired pneumonia; HIV, human immunodeficiency virus; ICU, intensive care unit; NBP,
nosocomial bacterial pneumonia; NP, nosocomial pneumonia; VAP, ventilator-associated pneumonia; VE- VAP, very early-onset ventilator-associated pneumonia. Data
E P I D E M I O LO G Y, E T I O LO G Y, A N D R I S K FAC TO R S O F B AC T E R I A L P N EU M O N I A • 9

extracted from [10–21].