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Journal of Clinical Microbiology, October 2001, p. 3495-3498, Vol. 39, No. 10
Microbiology Unit, Canterbury Health
Laboratories,1 and Christchurch School
of Medicine, University of Otago,3 Christchurch,
and Waikato Hospital, Hamilton,4 New
Zealand, and Clinical Microbiology Laboratory, Duke
University Medical Center, Durham, North Carolina
277102
Received 21 March 2001/Returned for modification 9 July
2001/Accepted 26 July 2001
Streptococcus pneumoniae is the most common cause of
community-acquired pneumonia but is undoubtedly underdiagnosed.
Isolation of S. pneumoniae from blood is specific but
lacks sensitivity, while isolation of S. pneumoniae from
sputum may represent colonization. We evaluated a new
immunochromatographic test (NOW S. pneumoniae urinary
antigen test; Binax, Portland, Maine) that is simple to perform and
that can detect S. pneumoniae antigen in urine within 15 min. Urine samples from 420 adults with community-acquired pneumonia
and 169 control patients who did not have pneumonia were tested. Urine
from 315 (75%) of the pneumonia patients and all controls was tested
both before and after 25-fold concentration, while the remaining 105 samples were only tested without concentration. S.
pneumoniae urinary antigen tests were positive for 120 (29%) patients with pneumonia and for none of the controls. Of the urine samples tested with and without concentration, 96 were positive, of
which 6 were positive only after concentration. S.
pneumoniae antigen was detected in the urine from 16 of the 20 (80%) patients with blood cultures positive for S.
pneumoniae and from 28 of the 54 (52%) patients with
sputum cultures positive for S. pneumoniae. The absence
of S. pneumoniae antigen in the urine from controls suggests that the specificity is high. Concentration of urine prior to
testing resulted in a small increase in yield. The NOW S.
pneumoniae urinary antigen test should be a useful adjunct to
culture for determining the etiology of community-acquired pneumonia in adults.
Streptococcus pneumoniae
has consistently been shown to be the most common cause of
community-acquired pneumonia (CAP) in both adults and children.
S. pneumoniae accounts for about two-thirds of cases where
an etiologic diagnosis is made (12) and is likely to be
the leading cause of pneumonia of otherwise unknown etiology (19). Despite being the single most important pathogen
causing CAP, S. pneumoniae is undoubtedly underdiagnosed due
to limitations of conventional diagnostic tests. Isolation of S. pneumoniae from blood lacks sensitivity, isolation of S. pneumoniae from sputum may represent colonization, and lung
aspirates are rarely performed. In an effort to improve the diagnostic
yield for patients with suspected pneumonia, there has been a
considerable interest in alternative techniques, such as PCR and
antigen detection.
Detection of S. pneumoniae antigens in the urine of patients
with pneumonia was first described in 1917 (8). Over the
intervening years the detection of S. pneumoniae antigens
(usually capsular polysaccharides) in urine has been extensively
studied using a variety of techniques, including
counterimmunoelectrophoresis, latex agglutination, coagglutination, and
enzyme-linked immunosorbent assay (1, 2, 5, 6, 14, 23). To
date, the performance of these tests has been variable, such that they
have never received general acceptance.
Recently, an immunochromatographic test, the NOW S. pneumoniae urinary antigen test (Binax, Inc., Portland, Maine),
has been developed; the test is simple to perform, detects the C
polysaccharide cell wall antigen common to all S. pneumoniae
strains (21), and provides results within 15 min.
We evaluated this test using concentrated and unconcentrated urine
samples from adults admitted to hospital with and without pneumonia.
(This work was presented at the 101st General Meeting of the American
Society for Microbiology, Orlando, Fla., 20 to 24 May 2001 [abstract
C-112].)
Urine samples from 420 adults (age range, 18 to 95 years; median
age, 68 years; 51% male) admitted to hospital with CAP were tested for
pneumococcal antigen using the NOW S. pneumoniae urinary antigen test. The patients were recruited as part of a prospective study of all adult CAP admissions to two large tertiary hospitals (Christchurch Hospital, Christchurch, New Zealand, and Waikato Hospital, Hamilton, New Zealand) over a 1-year period. All patients had
an acute illness with clinical features of pneumonia and radiographic pulmonary shadowing that was at least segmental or present in one lobe
and was neither preexisting nor due to some other known cause. Patients
were excluded when pneumonia was not the principal reason for admission
or was an expected terminal event or when the pneumonia was associated
with bronchial obstruction, bronchiectasis, or known tuberculosis. We
also tested urine samples from 169 hospitalized patients who did not
have pneumonia (age range, 20 to 91 years; median age, 69 years; 53%
male) to serve as controls. These patients had been admitted to one of
the study hospitals (Christchurch Hospital) at the same time as the
patients with CAP, with whom they were matched for age and sex. Control
patients were excluded if their presenting problem was a respiratory or
infectious disease, although 6 of the 169 were identified as having an
infection by the time of discharge (3 with cellulitis, 1 with
diverticulitis, 1 with a foot abscess, and 1 with cholecystitis). The
urine samples were collected soon after admission from both patients
with pneumonia and controls.
Blood cultures were collected at the time of admission from the
patients with pneumonia and processed using the BacT/Alert microbial
detection system (Organon Teknika, Durham, N.C.). Sputum samples were
examined by Gram stain microscopy for the presence of bacteria and the
quantities of squamous epithelial cells and polymorphonuclear
leukocytes and were cultured on sheep blood agar and chocolate agar.
Most antigen testing was performed at Duke University Medical Center
after urine samples had been rapidly transported from New Zealand. On
arrival in North Carolina, all samples remained in a completely or
mostly frozen state. Urine samples were stored between The NOW S. pneumoniae urinary antigen test consists of a
hinged, book-shaped test device containing a nitrocellulose membrane on
which the rabbit anti-S. pneumoniae antibody is adsorbed
(the sample line). Goat anti-rabbit immunoglobulin G (IgG) is adsorbed onto the same membrane as a second stripe (control line). Rabbit anti-S. pneumoniae antibodies are conjugated to visualizing
particles, which are dried onto an inert fibrous support. The test was
performed according to the manufacturer's instructions. A swab was
dipped into the urine sample and then inserted into the test device. A
buffer solution was added, and the device was closed, bringing the
sample into contact with the test strip. Pneumococcal antigen present
in the urine sample binds to the anti-S.
pneumoniae-conjugated antibodies, and the resulting
antigen-antibody complexes are captured by immobilized anti-S.
pneumoniae antibodies, forming the sample line. Immobilized goat
anti-rabbit IgG captures excess visualizing conjugate, forming the
control line. The test was read at 15 min and was interpreted by noting
the presence or absence of visually detectable pink-to-purple lines. A
positive test result was indicated by the detection of both sample and
control lines. A negative test result was indicated by the detection of
a control line only.
The Mann-Whitney U test was used to compare urine sample collection
times from patients with positive and negative urinary antigen test results.
S. pneumoniae urinary antigen tests were positive for
120 (29%) patients with pneumonia and for none of the controls. None of the tests were read as invalid due to the absence of a control band.
Of the 484 urine samples tested with and without concentration, 96 were
positive, of which 6 were positive only after concentration.
Of the 420 patients with pneumonia, 396 (94%) had blood cultures and
296 (70%) had sputum collected. Coincidentally, 9 of the 169 control
patients had blood cultures collected, and all were negative. S. pneumoniae antigen was detected in the urine from 16 of the 20 patients with blood cultures positive for S. pneumoniae.
Details of the patients with pneumococcal pneumonia and bacteremia are
shown in Table 1. S. pneumoniae antigen was detected in the urine from 28 of the 54 patients with sputum cultures positive for S. pneumoniae. Of
the 15 patients with pneumonia who had received a pneumococcal vaccine,
5 had positive S. pneumoniae urinary antigen tests. None of
these patients had the vaccine administered within 5 days of testing;
the manufacturer recommends that testing for S. pneumoniae
urinary antigen not be performed within 5 days of receiving the
pneumococcal vaccine because of the risk of false-positive results
(product instructions, NOW S. pneumoniae urinary antigen
test; Binax, Inc.).
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.10.3495-3498.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Evaluation of a Rapid Immunochromatographic Test
for Detection of Streptococcus pneumoniae Antigen in
Urine Samples from Adults with Community-Acquired
Pneumonia
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
MATERIALS AND METHODS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
80 and
70°C in both New Zealand and North Carolina and were thawed
immediately prior to testing. Samples from 315 pneumonia patients and
all control patients were tested both before and after 25-fold
concentration using Minicon-B15 concentrators (Millipore, Bedford,
Mass.). An additional 105 samples were tested only without concentration. Testing was performed in a blinded fashion, without knowing whether samples were from cases or controls.
RESULTS
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
TABLE 1.
Characteristics of the pneumonia patients with
pneumococcal bacteremia
Urine samples were collected a median of less than 1 day after admission (range, 0 to 3 days) from the patients with pneumonia and a median of 1 day after admission (range, 0 to 4 days) from controls. The median time from onset of symptoms to collection of urine was 5 days both for patients who had positive (range, 1 to 29 days; interquartile range, 3 to 7 days) and negative (range, 0 to 61 days; interquartile range, 3 to 9 days) S. pneumoniae urinary antigen test results (P value for the difference between distributions, 0.71). Of the patients with pneumonia, 76% were taking antibiotics at the time the urine samples were collected (79% of those with positive urinary antigen tests). Of the 120 patients with positive S. pneumoniae urinary antigen tests, 65 had no other etiological diagnoses, 33 had S. pneumoniae isolated from blood or sputum and had no evidence of infection with another pathogen, 14 had evidence of infection with only non-S. pneumoniae pathogens (Haemophilus influenzae, 3; respiratory syncytial virus, 3; Legionella spp., 2; Chlamydia pneumoniae, 2; parainfluenza virus, 2; Staphylococcus aureus, 1; influenza B virus, 1), and 8 had mixed infections with S. pneumoniae and other pathogens (H. influenzae, 3; respiratory syncytial virus, Legionella spp., influenza A virus, Moraxella catarrhalis, and Mycoplasma pneumoniae, 1 each).
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
|
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The NOW S. pneumoniae urinary antigen test is easy to perform, provides results within a few minutes, and detects an antigen common to all S. pneumoniae strains (21). The manufacturer's own study confirmed that the test was able to detect 44 different strains of S. pneumoniae, representing the 23 serotypes responsible for at least 90% of pneumococcal infections (product instructions, NOW S. pneumoniae urinary antigen test; Binax, Inc.). Our findings indicate that the sensitivity of the test is 80% when positive blood cultures are used as the "gold standard." The absence of S. pneumoniae antigen in the urine from controls suggests that the specificity is high.
These findings are similar to those of other investigators who have used the NOW S. pneumoniae urinary antigen test. Domínguez et al. (9) tested urine samples from patients with pneumococcal pneumonia, and detected S. pneumoniae antigen in 23 of 28 bacteremic patients (82%) and in 18 of 23 nonbacteremic patients (78%). The specificity was 97%, based on two positive results among 71 patients with documented infections caused by microorganisms other than S. pneumoniae. Yu et al. detected S. pneumoniae antigen in the urine from 86% of bacteremic patients (V. L. Yu, J. A. Kellog, J. F. Plouff, J. A. Coladonato, J. Manzella, W. Alves Dos Santos, R. B. Kohler, A. Torres, T. M. File, and J. D. Rihs, Abstr. 38th IDSA Annu. Meet., abstr. 262, 2000). In another study, S. pneumoniae antigen was detected in urine from 24 of 45 patients with CAP and the diagnostic yield for pneumococcal pneumonia was increased by 60% (15).
In contrast, the performance of other methods for detection of S. pneumoniae antigen in urine has been inconsistent, with sensitivities ranging from 0 to >80%, usually <50% (2, 3, 6, 7, 14, 16, 18, 20). The improved sensitivity of the NOW S. pneumoniae urinary antigen test may be due, in part, to the detection of the cell wall C polysaccharide common to all S. pneumoniae strains, rather than type-specific capsular polysaccharides. This has been demonstrated in at least one comparative study using latex agglutination assays, where the C polysaccharide was detected in the urine of 23 of 33 patients with pneumococcal bacteremia, while type-specific polysaccharides were detected in only 17 of these patients (3).
The NOW S. pneumoniae urinary antigen test may be less useful for detecting pneumococcal pneumonia in children because of the high false-positive rate due to nasopharyngeal colonization with S. pneumoniae. In one series, the test was no more likely to be positive among 88 children with pneumonia than among 198 control subjects but was significantly more likely to be positive among children who were nasopharyngeal carriers of S. pneumoniae (10). While we did not test for nasopharyngeal carriage in the present study, the absence of positive results in our control group suggests this may not be an issue in adults. These findings may reflect the lower rates of pneumococcal colonization in adults than in children.
It is unclear why S. pneumoniae antigen was not detected in urine from four patients with pneumococcal bacteremia. Although two of these patients had urine collected many days after the onset of symptoms, S. pneumoniae was isolated from blood cultures within 2 days of urine collection in both cases, suggesting recent or concurrent antigenemia. Three of the 4 bacteremic patients with negative urinary antigen tests were taking antibiotics at the time of urine collection, compared with 6 of the 16 with positive tests. However, the numbers are too small to determine whether this trend is a true association. It is possible that the relative dilutions of the urine samples may affect test results and that pneumococcal antigen was present in very low concentrations in the four negative samples. Unfortunately, we were unable to test concentrated urine from two of the four patients because of insufficient volume. The relatively low urinary antigen positivity rate among patients with sputum cultures positive for S. pneumoniae may partly reflect the inherent problems of interpreting sputum cultures. It is difficult to be certain that S. pneumoniae isolated from sputum represents infection rather than colonization, and, although we cytologically screened all samples, it is likely that some of our positive samples were due to contamination with oropharyngeal flora.
Concentrating urine samples before antigen testing is widely practiced, but few studies have determined the increase in yield by testing samples both before and after concentration. Twentyfold concentration of urine resulted in a 1.6-fold increase in yield of positive S. pneumoniae antigen results (from 14 to 22%) using counterimmunoelectrophoresis (13). Using the NOW S. pneumoniae urinary antigen test, Marcos et al. noted a 1.4-fold increase in yield following concentration of urine (from 38 to 53%) (15), which is at variance with the small increase in sensitivity that we documented (from 29 to 30%). They did not record the method they used for concentrating urine, but it is unlikely that using a concentrator with a lower-molecular-mass cutoff would increase sensitivity. The molecular mass of the C polysaccharide is 20 to 30 kDa (22), whereas the Minicon-B15 concentrator has a molecular mass cutoff of 15 kDa (product instructions, Minicon and Miniplus clinical sample concentrators; Millipore). While the identification of these additional cases may be important, the small increase in yield in our study would not justify routine concentration of samples by diagnostic laboratories, especially given the substantial increase in costs that this would entail.
Although new tests for diagnosing pneumococcal disease have traditionally been compared with blood cultures, bacteremia was documented in only 20 to 30% of patients with pneumococcal pneumonia (4, 11, 17). In the present study, of the pneumonia patients with positive urinary antigen tests who had blood cultures collected, only 18% were bacteremic. The NOW S. pneumoniae urinary antigen test will be especially useful for identifying the large number of patients with nonbacteremic pneumococcal pneumonia and for rapidly identifying a group of patients in whom narrow-spectrum antibiotics may be used.
We conclude that the NOW S. pneumoniae urinary antigen test is a useful adjunct to culture for determining the etiology of CAP in adults. Further research should focus on the time course of urinary antigen positivity and the use of this test in settings other than adult pneumonia.
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ACKNOWLEDGMENTS |
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This work was supported by the Health Research Council of New Zealand, Canterbury Respiratory Research Trust, and Canterbury Health Limited.
We thank other members of the Christchurch-Waikato Community-Acquired Pneumonia Study research team and Binax, Inc., for donating the antigen detection kits.
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FOOTNOTES |
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* Corresponding author. Mailing address: Microbiology Unit, Canterbury Health Laboratories, P.O. Box 151, Christchurch, New Zealand. Phone: 64 3 364 1530. Fax: 64 3 364 0238. E-mail: david.murdoch{at}cdhb.govt.nz.
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Journal of Clinical Microbiology, October 2001, p. 3495-3498, Vol. 39, No. 10
0095-1137/01/$04.00+0 DOI: 10.1128/JCM.39.10.3495-3498.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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