Bacterial Pneumonia in Hospitalized

Patients With HIV Infection*

The Pulmonary Complications, ICU Support, and
Prognostic Factors of Hospitalized Patients With
HIV (PIP) Study
Bekele Afessa, MD, FCCP; and Bethany Green, DO

Study objectives: To describe the causative organisms and factors associated with bacterial
pneumonia and to assess its impact on the outcome of hospitalized patients with HIV.
Design: Prospective, observational.
Setting: A university-affiliated medical center.
Methods: We included 1,225 consecutive hospital admissions, from April 1995 through March
1998, of 599 adults with HIV. We collected data on APACHE II (acute physiology and chronic
health evaluation II) score, leukocyte and CD4ⴙ lymphocyte counts, length of hospital stay, ICU
admission rate, and case-fatality rate. Chest radiographs and laboratory results were reviewed.
The presence of bacterial pneumonia was noted.
Results: Bacterial pneumonia was diagnosed in 111 hospitalizations (9%): 80 (72%) were
community-acquired infections. The CD4ⴙ lymphocyte count was lower (median, 38 vs 66/␮L,
p ⴝ 0.0027), APACHE II score higher (17 vs 13, p < 0.0001), length of hospital stay longer
(median, 6 vs 4), and ICU admission (28% vs 9%) and case-fatality rates (21% vs 4%) higher in
patients with bacterial pneumonia compared with those without bacterial pneumonia. The most
common pathogen was Pseudomonas aeruginosa (32 admissions), followed by Streptococcus
pneumoniae (22 admissions), Staphylococcus aureus (16 admissions), and Haemophilus influenzae
(11 admissions). Thirty-three (30%) of the pneumonias were bacteremic. Bacteremia was more
common in pneumococcal than in pseudomonal pneumonia (95% vs 9%, p < 0.0001). Compared
with patients with pneumococcal pneumonia, patients with pseudomonal pneumonia had lower
leukocyte and CD4ⴙ lymphocyte counts, longer hospital stay, and similar case-fatality rate.
Conclusions: P aeruginosa is becoming a common cause of both community-acquired and
nosocomial bacterial pneumonia in hospitalized patients with HIV, especially in those with low
leukocyte and CD4ⴙ lymphocyte counts. (CHEST 2000; 117:1017–1022)

Key words: AIDS; bacterial pneumonia; HIV; ICU admission; mortality; Pseudomonas aeruginosa infection; Strepto-
coccus pneumoniae infection

Abbreviation: APACHE II ⫽ acute physiology and chronic health evaluation II

S ince the beginning of the AIDS epidemic, the

lungs have continued to be a frequent site of
organ complication. Traditionally, pulmonary infec-
tions in patients with HIV have been classified into
opportunistic and nonopportunistic. Opportunistic
infections are caused by organisms that do not cause
*From the Department of Internal Medicine, Division of Pulmo-
nary and Critical Care, University of Florida Health Science
Center, Jacksonville, FL.
Manuscript received May 11, 1999; revision accepted September
9, 1999.
Correspondence to: Bekele Afessa, MD, FCCP, Division of Pul-
monary and Critical Care Medicine, Department of Medicine,
University of Tennessee, Memphis, 956 Court Ave, Rm H314,
Memphis, TN 38163; e-mail: Bafessa@UTMEM1.UTMEM.EDU
disease in immunocompetent individuals. However,
any human pathogenic organism can cause disease in
patients with HIV, blurring this classic classification.
The type of pulmonary infection occurring in an
HIV-infected patient depends on the stage of the
HIV infection, the individual history of prior infec-
tion, the virulence of the infecting organism, and
other host-related factors, such as the disease expo-
sure category and geographic location. Various de-
fects in immunity have been described early in the
disease process of patients with HIV infection, be-
fore we see a decline in the CD4⫹ lymphocyte
count. In addition to the low CD4⫹ lymphocyte
count, humoral immune dysfunction, depressed
IgA2 and IgG2 levels, and decreased CD4⫹ T-

CHEST / 117 / 4 / APRIL, 2000 1017

lymphocyte cell-mediated antibody-dependent cel- Table 1—Demographic Characteristics, Exposure
lular cytotoxicity are also present in HIV-infected Categories, CD4ⴙ Lymphocyte Count, and APACHE II
Scores of 1,225 Hospital Admissions of 599 Patients
patients, predisposing them to bacterial infections.1–3 With HIV*
Bacterial infections are the most common respiratory
complications in patients with HIV infection.4 These Characteristics No. (%)
infections occur at all levels of CD4⫹ lymphocyte Sex
count but become more frequent as the CD4⫹ Male 754 (62)
lymphocyte count declines.5,6 The purpose of this Female 471 (38)
study was to describe the incidence and types of Race
African American 1,026 (84)
bacterial pneumonia in hospitalized patients with White 190 (16)
HIV infection and to determine the factors associ- Hispanic 9 (1)
ated with it and its impact on patient outcome. Exposure category
Injection drug use 333 (27)
Heterosexual contact 194 (16)
Homosexuality 138 (11)
Materials and Methods Commercial sex work and injection 32 (3)
drug use
This prospective, observational study included 1,225 consecu- Homosexuality and injection drug use 30 (2)
tive hospital admissions of 599 adults with HIV infection treated Commercial sex work 29 (2)
at the University Medical Center, Jacksonville, FL, from April Blood transfusion 22 (2)
1995 through March 1998. All adults with HIV infection who Needle stick 1
were admitted to the hospital were included in the study. The Unidentified 446 (36)
University Medical Center is a 528-bed, teaching inner-city CD4⫹ lymphocyte count/␮L (median) 159 ⫾ 223 (60)
hospital affiliated with the University of Florida. The need for APACHE II score (median) 15 ⫾ 7 (14)
informed consent was waived by the Institutional Review Board
of the hospital. *Age of patients (mean ⫾ SD) was 38.2 ⫾ 8.9 years.
Bacterial pneumonia was defined by the presence of new or
worsening infiltrate on chest radiograph, temperature ⬎ 100.4°F
or ⬍ 96.8°F, leukocyte count ⬎ 12,000/mm3 or ⬍ 4,000/mm3 or
bandemia ⬎ 10%, and sputum Gram’s stain or culture showing a episodes of bacterial pneumonia occurred in 94
bacterial organism in a purulent sputum or quantitative culture of patients: one episode in 82 patients, two episodes in
BAL showing bacteria ⱖ 104/mL or the isolation of a likely
pathogen from blood, or pleural fluid or urine positive for
10 patients, three episodes in 1 patient, and six
Legionella pneumophila antigen. Purulent sputum was identified episodes in 1 patient. The causative organisms are
by the presence of ⬎ 25 WBCs and ⬍ 10 epithelial cells per listed in Table 2. Among the 12 patients with two or
microscopic low-power field of a sputum sample. Nosocomial more episodes of bacterial pneumonia, 4 had re-
pneumonia was defined as pneumonia that developed after 48 h peated episodes caused by Pseudomonas aeruginosa,
of hospitalization or within 14 days of previous hospitalization. All
chest radiographs were reviewed by one of the investigators
and 8 had repeated episodes caused by different
(B.A.), a pulmonologist. We collected data on age, sex, race, organisms, none by the same organism. Pneumocys-
exposure category for HIV infection, place of acquisition, WBC tis carinii pneumonia was present in 14 of the 111
count, CD4⫹ lymphocyte count, APACHE II (acute physiology patient-admissions with bacterial pneumonia (13%).
and chronic health evaluation II) score, chest radiograph find- Fiberoptic bronchoscopy, performed in 69 patient-
ings, the presence of bacteremia, ICU admission status, length of
hospital stay, and in-hospital mortality. For the purpose of this
admissions, was diagnostic of bacterial pneumonia in
study, each admission was considered as one patient and termed 3, all from P aeruginosa. Fifty-seven of the organisms
a patient-admission. were Gram-negative and 43 were Gram-positive.
StatView 5.0 computer software (SAS Institute Inc.; Cary, NC) Although the sputum Gram’s stain showed organ-
was used for statistical analysis. Results are expressed as mean isms, the cultures were negative in 11 patients. All
⫾ SD. Comparisons between groups were made using Student’s
t test, Mann-Whitney U test, ␹2, Fisher’s Exact Test, and logistic
BAL specimens were examined for the presence of
regression analysis. Probability values ⬍ 0.05 were considered Mycoplasma pneumoniae and L pneumophila infec-
significant. tion. However, no atypical bacterial pneumonia was
diagnosed by bronchoscopy. There was one case of L
pneumophila pneumonia detected by direct fluores-
Results cence antibody for urine antigen.
There were no significant differences in age, sex,
The demographic characteristics, exposure catego- and risk factors for HIV infection between patients
ries, CD4⫹ lymphocyte count, and APACHE II with or without bacterial pneumonia (Table 3).
scores of the patients are listed in Table 1. Bacterial pneumonia was more common in Hispan-
One hundred eleven of the 1,225 patient-admis- ics compared with African Americans and whites
sions (9%) had bacterial pneumonia: 80 (72%) com- (Table 3). The CD4⫹ lymphocyte count was lower
munity-acquired and 31 (28%) nosocomial. The 111 and the APACHE II score higher in patients with

1018 Clinical Investigations

Table 2—Bacterial Pathogens Isolated in 111 Episodes dence of pleural effusions and multilobar infiltrate
of Pneumonia in Patients With HIV on chest radiograph, ICU admission rate, length of
Community-acquired Nosocomial hospital stay, and in-hospital mortality between pa-
Pathogen (n ⫽ 80) (n ⫽ 31) tients with pseudomonal and pneumococcal pneu-
Gram-negative 40 17
monia are listed in Table 5.
Pseudomonas aeruginosa 20 12
Haemophilus influenza 10 1
Klebsiella pneumoniae 3 0
Escherichia coli 1 2
Discussion
Serratia marcescens 1 0
Serratia liquefaciens 0 1
This study describes 111 cases of bacterial pneu-
Proteus mirabilis 0 1 monia among 1,225 hospital admissions of 599 pa-
Haemophilus parainfluenza 1 0 tients with HIV infection. P aeruginosa and S pneu-
Enterobacter aerogenes 1 0 moniae were the two most common causative
Acinetobacter baumanii 1 0 pathogens.
Bordetella bronchiseptica 1 0
Legionella pneumophila 1 0
Early in the HIV epidemic, researchers noted that
Gram-positive 31 12 bacterial pneumonia was a common cause of mor-
Streptococcus pneumoniae 20 2 bidity.7–9 Decreasing CD4⫹ lymphocyte count, in-
Staphylococcus aureus 8 8 jection drug use, prior sinusitis, and prior lower
Streptococcus viridans 2 1 respiratory tract bacterial infection are risk factors
Enterococcus species 0 1
Group C streptococcus 1 0
for bacterial pneumonia in patients with HIV infec-
No organism isolated 9 2 tion.5,10 –12 A recent multicenter study showed the
incidence of bacterial pneumonia to be 5.5 per 100
person-years among HIV seropositive individuals10;
this incidence was higher than that of P carinii
bacterial pneumonia compared with those without pneumonia.10 An autopsy study from two medical
bacterial pneumonia (Table 3). Of the 111 bacterial centers has confirmed bacterial pneumonia to be the
pneumonias, 33 (30%) were bacteremic: Streptococ- most common pulmonary complication in patients
cus pneumoniae (21), P aeruginosa (3), Streptococcus with HIV.13 The cumulative incidence of bacterial
viridans (3), Staphylococcus aureus (2), Escherichia pneumonia in hospitalized patients with HIV infec-
coli (1), Haemophilus influenza (1), Enterococcus tion may be as high as 12.5 per 100 person-years.11
spp (1), and Group C streptococcus (1). Twenty In our study, the incidence of bacterial pneumonia
(91%) of the pneumococcal isolates were fully sen- was 9 per 100 inpatients. However, this number
sitive to penicillin, and 2 (9%) were intermediately underestimates the actual incidence, because we did
sensitive. not include the cases that were empirically treated
The differences in the length of hospital stay, ICU for presumed pneumonia without obtaining respira-
admission rate, and in-hospital mortality between tory specimens to confirm the diagnosis. Unlike
patients with or without bacterial pneumonia are previous studies, we did not find a significant rela-
listed in Table 4. The in-hospital mortality rate of tionship between injection drug use and bacterial
patients with bacterial pneumonia was 21% (23 of pneumonia. Although the incidence of bacterial
111). Multiple logistic regression analysis showed pneumonia was higher in Hispanics in our study, we
that there was a significant difference only in cannot make any reasonable conclusion because only
APACHE II score (15 vs 25, p ⫽ 0.0003) not in nine patients were of Hispanic origin.
CD4⫹ lymphocyte count (50 vs 18/␮L, p ⫽ 0.6431) The annual incidence of pneumococcal bactere-
or in incidence of bacteremia (28% vs 35%, mia is estimated to be as high as 940 per 100,000
p ⫽ 0.7128) between survivors and nonsurvivors patients with AIDS.14 In certain regions, the ma-
with bacterial pneumonia. jority of adults with pneumococcal infection and
P aeruginosa and S pneumoniae were the two most ⬍ 40 years of age are HIV seropositive.15,16 Previ-
common causes of bacterial pneumonia. There were ous studies have shown S pneumoniae to be the
no significant differences in age, sex, race, and most common cause of bacterial pneumonia.5,8,11
exposure category between patients with pseudo- In our study, S pneumoniae was not the most
monal or pneumococcal pneumonia. Twenty of the common pathogen causing bacterial pneumonia. S
22 pneumococcal pneumonias (91%) were commu- pneumoniae is isolated in blood cultures of 60% of
nity-acquired compared with 20 of the 32 pseudo- HIV-infected patients with pneumococcal pneu-
monal pneumonias (63%; p ⫽ 0.0269). The differ- monia and 15 to 30% of patients without HIV
ences in APACHE II score, WBC count, CD4⫹ infection.1 In the multicenter study by the Pulmo-
lymphocyte count, incidence of bacteremia, inci- nary Complications of HIV Infection Study Group,

CHEST / 117 / 4 / APRIL, 2000 1019

 Table 3—Differences in Age, Sex, Race, Exposure Category, CD4ⴙ Lymphocyte Count, and APACHE II Scores
Between Patients With or Without Bacterial Pneumonia

Bacterial Pneumonia No Bacterial Pneumonia

(n ⫽ 111) (n ⫽ 1114) p Value

Age (mean ⫾ SD), yr 37.5 ⫾ 8.2 38.2 ⫾ 9.0 0.4399

Sex, No. (%) 0.3766
Male 64 (8.5) 690 (91.5)
Female 47 (10.0) 424 (90.0)
Race, No. (%) 0.0009
African American 92 (9.0) 934 (91.0)
White 15 (7.9) 175 (92.1)
Hispanic 4 (44.4) 5 (55.6)
Exposure category, No. (%) 0.8919
Injection drug use 25 (7.5) 308 (92.5)
Heterosexual contact 22 (11.3) 172 (88.7)
Homosexuality 12 (8.7) 126 (91.3)
Commercial sex work and injection drug use 3 (9.4) 29 (90.6)
Homosexuality and injection drug use 2 (6.7) 28 (93.3)
Commercial sex work 2 (6.9) 27 (93.1)
Blood transfusion 1 (4.5) 21 (95.5)
Needle stick 0 1 (100%)
Unidentified 44 (9.9) 402 (90.1)
CD4⫹ lymphocyte count/␮L (median) 107 ⫾ 172 (38) 165 ⫾ 227 (66) 0.0027
APACHE II score (median) 18.5 ⫾ 8.4 (17) 14.3 ⫾ 6.6 (13) ⬍0.0001

Table 4 —Differences in Length of Hospital Stay, ICU
Admission Rate, and In-Hospital Mortality Between
Patients With or Without Bacterial Pneumonia
Bacterial Pneumonia
Yes No
Variable (N ⫽ 111) (N ⫽ 1,1114)
Length of hospital stay, 9.1 ⫾ 9.4 (6) 5.9 ⫾ 6.2 (4)
days (median)
ICU admission, No. (%) 31 (28) 102 (9)
In-hospital mortality, No. 23 (21) 44 (4)
(%)
11 of the 36 pneumococcal pneumonias (31%)
were bacteremic.5 In our study, 95% of the pneu-
mococcal pneumonias were bacteremic, suggest-
ing underdiagnosis of nonbacteremic pneumococ-
cal pneumonia. Because our study was purely
observational, we did not have any control on the
management plan of the individual patients. The
common medical practice in our emergency de-
partment included giving at least one IV dose each
of trimethoprim/sulfamethoxazole and a third-gen-
eration cephalosporin to ill-looking HIV-infected
patients with suspected pneumonia before obtain-
ing respiratory specimens. This practice may have
led to a falsely decreased incidence of pneumo-
coccal pneumonia in our study.
Penicillin remains the drug of choice for patients
infected with a susceptible strain of S pneumoniae.
In the United States, 7% of S pneumoniae are
penicillin-resistant compared with 44% in Spain.17 In
a study from France of HIV-infected inpatients with
bacterial pneumonia, 75% of the pneumococci had
decreased susceptibility to penicillin.11 In our study,
only 9% of the pneumococci had decreased suscep-
p Value tibility to penicillin.
Bacteremic and nonbacteremic P aeruginosa
⬍0.0001
infections are becoming more common in patients
⬍0.0001 with HIV.18 An effective defense against P aerugi-
⬍0.0001 nosa depends on functions of the epithelial cell
barrier, antibodies, complement system, phago-
cytic cells, and lymphocytes.19 Traditionally, P
aeruginosa infection has been associated with
neutropenia, hospitalization, central venous cath-
eters, burn wounds, bronchiectasis, and cystic
fibrosis.19 The development of bronchiectasis and
defects in granulocytes, chemotaxis, phagocytosis,
and bacterial killing have been described in HIV-
infected patients and have predisposed them to
infection with P aeruginosa.2,3,20,21 In a prospec-
tive study of HIV-infected inpatients from France,
6 of the 33 identified pathogens causing bacterial
pneumonia (18%) were P aeruginosa.11 In the
multicenter study by the Pulmonary Complica-
tions of HIV Infection Study Group, P aeruginosa
accounted for 6 of the 89 organisms identified as
causing bacterial pneumonia (7%).5 Other studies
have highlighted the importance of P aeruginosa
pneumonia in patients with HIV infection, includ-
ing a rise in its incidence more recently.22–26 Most
of these infections are community-acquired.22–26
The incidence of P aeruginosa infection in hospi-

1020 Clinical Investigations

 Table 5—Differences in APACHE II Score, Leukocyte Count, CD4ⴙ Lymphocyte Count, Incidence of Bacteremia,
Incidences of Pleural Effusion and Multilobar Infiltrate on Chest Radiograph, ICU Admission Rate, Length of
Hospital Stay, and In-Hospital Mortality Between Patients With Pseudomonal and Pneumococcal Pneumonia
P aeruginosa
Variable (n ⫽ 32)
APACHE II (median) 18.5
Leukocyte count/mm3 (median) 5.0
CD4⫹ lymphocyte count/␮L (median) 19
Bacteremia, No. (%) 3 (9)
Chest radiograph, No. (%)
Pleural effusion 4 (13)
Multilobar infiltrate 17 (53)
ICU admission 11 (34)
Length of hospital stay (median), d 9 4
Mortality, No. (%) 6 (19)
talized patients with HIV is estimated to be 5.8%
and on the rise.26 In our study, the incidence of
pneumonia from P aeruginosa in hospitalized pa-
tients with HIV infection was 2.6%. Unlike previ-
ous studies, we found P aeruginosa, not S pneu-
moniae, to be the most common pathogen causing
bacterial pneumonia in our patients. The underdi-
agnosis of pneumococcal pneumonia in our study,
caused by technical difficulties in culturing S
pneumoniae and empiric antibiotic use before
obtaining adequate respiratory samples, may
partly explain this unexpected finding. The low
CD4⫹ lymphocyte count in our patients with
pseudomonal pneumonia was similar to the find-
ings in other studies.22,25
Atypical bacterial pneumonia was diagnosed in
only one patient in our study. The Pulmonary Com-
plications of HIV Infection Study Group reported
only one case of L pneumophila among 237 episodes
of bacterial pneumonia in HIV-positive patients.5
There are case reports of pneumonia caused by
Bordetella bronchiseptica in patients with HIV infec-
tion.27,28 B bronchiseptica was the only unusual
bacterial pathogen found to cause pneumonia in our
study.
Recent trends among persons dying of HIV infec-
tion in the United States show an increase in the
percentage of deaths associated with bacterial pneu-
monia.29 An Italian study of 350 episodes of bacterial
pneumonia reported a case-fatality rate of 27%.12
The case-fatality rate was 21% in our study. Com-
pared with patients without bacterial pneumonia,
patients with bacterial pneumonia had longer length
of hospital stay and higher ICU admission and
case-fatality rates in our study. This indicates the
adverse impact of bacterial pneumonia on the mor-
bidity and mortality of hospitalized patients with
HIV infection.
Our study has several limitations. The diagnostic
S pneumoniae
(n ⫽ 22) p Value
16 0.0962
12.4 0.0054
106 0.0001
21 (95) ⬍0.0001
7 (32) 0.0996
9 (41) 0.3774
5 (23) 0.3570
0.0023
3 (14) 0.7230
and therapeutic approaches varied according to
each patient’s primary physician. The initiation of
empiric antibiotic therapy before obtaining respi-
ratory specimen samples may have led to the
underdiagnosis of bacterial pneumonia, pneumo-
coccal in particular. Although there were patients
whose clinical presentation and response to ther-
apy were consistent with bacterial pneumonia,
they were not considered as having bacterial pneu-
monia unless they had microbiologic evidence of
bacterial pneumonia. This may have led to under-
estimation of the incidence of bacterial pneumo-
nia. Because we were unable to document the
patients’ antiretroviral treatment and trimetho-
prim/sulfamethoxazole use before hospitalization,
we could not determine their effect on the inci-
dence and type of the bacterial pneumonia.
In summary, we have described the incidence and
types of bacterial pneumonia in hospitalized patients
with HIV infection. Pseudomonal pneumonia is be-
coming a common pulmonary complication, espe-
cially in patients with low leukocyte and CD4⫹
lymphocyte counts. Compared with pneumococcal
pneumonia, pseudomonal pneumonia is associated
with a lower incidence of bacteremia and a longer
hospital stay. Despite the low CD4⫹ lymphocyte
and leukocyte counts associated with pseudomonal
pneumonia, the mortality rate is only 19%. We need
to closely monitor the changes in disease patterns,
including the pathogens causing pneumonia, in dif-
ferent institutions and regions. Our observations
suggest that pseudomonal pneumonia should be
included in the differential diagnosis of both com-
munity-acquired and nosocomial pneumonia in pa-
tients with HIV infection.
ACKNOWLEDGMENT: We thank Dr. David L. Armbruster
for editing our manuscript.
CHEST / 117 / 4 / APRIL, 2000 1021
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