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Previous Article | Next Article 
Journal of Clinical Microbiology, March 1998, p. 820-823, Vol. 36, No. 3
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
Simplified Technique for Detection of Significant
Bacteriuria by Microscopic Examination of Urine
Celso Luíz
Cardoso,1,*
Carla Barbosa
Muraro,2
Vera Lúcia Dias
Siqueira,1 and
Márcio
Guilhermetti1
Laboratory of Microbiology, Department of
Clinical Analyses,1 and
Department of
Medicine,2 State University of
Maringá, 87020-900 Maringá, Paraná, Brazil
Received 7 May 1997/Returned for modification 10 July 1997/Accepted 25 November 1997
 |
ABSTRACT |
A comparative study of microscopic examination of 10 µl
(simplified loop technique) and 50 µl (traditional drop technique) of
uncentrifuged Gram-stained urine specimens for detection of significant
bacteriuria was carried out. The results demonstrated that the 10-µl
loop technique can be used as an alternative to the 50-µl drop
technique for presumptive diagnosis of urinary-tract infection in
bacteriological practice, with the advantages of greater rapidity and
ease of performance.
| |
TEXT |
Urinary-tract infections, including
cystitis, pyelonephritis, asymptomatic bacteriuria, and acute urethral
syndrome, constitute one of the most frequent causes of illness in
humans (17, 18). Most such infections are caused by a few
genera of bacteria, and the presence of these microorganisms in the
urine is known as bacteriuria (6, 24). Quantitative urine
culture is considered the standard procedure for adequate diagnosis of
urinary-tract infections (25). Urine cultures represent 40 to 70% of the specimens sent for examination to clinical-microbiology
laboratories (7, 14). Although the prevalence of urinary
infections may vary in different patient populations, approximately
80% of urine cultures are negative (7, 14, 33). In an
attempt to reduce the cost and time expended in examining these
negative cultures, several rapid methods have been developed for
characterizing bacteriuria, including microscopic examination, chemical
tests, and automated systems (6, 7, 17).
Microscopic examination of an uncentrifuged Gram-stained urine drop
constitutes one of the best diagnostic methods for detecting significant bacteriuria, i.e., the presence of 100,000 or more microorganisms per ml of urine (4, 6, 11, 26). Observation of one or more bacteria per oil immersion field correlates with 90% of
cases of significant bacteriuria, thus indicating active urinary-tract
infection (4, 20, 26, 30).
In Brazil, this method is not used in bacteriological practice,
possibly because it is not widely known, because it is not standardized, or because of the prolonged drying time (probably due to
the high concentration of salts and urea), about 3 to 4 h, of the
urine drop, which is deposited, without spreading, on the slide. Use of
a smaller volume of urine, leading to more rapid drying, might
facilitate the use of this technique. However, no information regarding
this subject was found in the literature, particularly in relation to
the possibility of compromising the sensitivity or specificity of the
method by using urine volumes less than 1 drop (50 µl).
In order to better investigate this matter, we performed a comparative
study of microscopic examination of an amount of urine applied with a
calibrated loop (10 µl) and a drop (50 µl) of uncentrifuged Gram-stained urine, for detection of significant bacteriuria in patients with suspected urinary infections treated at the Maringá Regional University Hospital. As a reference method, we performed parallel counts of bacterial colonies cultured from the 500 urine samples analyzed in the present study.
Samples.
From October 1994 through July 1996, 500 urine
samples were analyzed from patients treated at the Maringá
Regional University Hospital of the State University of Maringá,
in the city of Maringá, state of Paraná. Basic hygienic and
aseptic precautions were taken in obtaining all urine specimens
(4, 6). The time between collection and culture never
exceeded 2 h. Urine samples not cultured immediately following
collection were refrigerated at 4°C until processing (6).
Drop method.
After homogenization of the urine sample, a
hanging drop of approximately 50 µl of the urine was deposited, by
means of a 1- to 2-ml sterilized pipette, on the surface of a 25- by
75-mm microscope slide and was allowed to dry, without spreading, at ambient temperature (30).
Loop method.
A 10-µl volume of homogenized urine sample was
applied, by means of a nickel-chrome loop calibrated to 10 µl, to the
surface of a 25- by 75-mm microscope slide and was allowed to dry,
without spreading, at ambient temperature.
Gram staining.
After air drying, the smears were fixed by
passing the slides two or three times through the flame of a Bunsen
burner, and then they were stained by the Gram method (5).
Microscopic examination.
A preliminary inspection of the
smears was performed by using a low-magnification (10× to 20×) dry
objective in order to locate the material on the slide. Next, with a
100× oil immersion objective, 50 fields were examined, and the shapes
and number of microorganisms and cells per field were recorded. The
microscopic reading was done systematically, beginning at the edge of
the central region of the smear and continuing across its diameter. A
positive microscopic examination was defined as the presence of 
2
microorganisms uniformly distributed per oil immersion field, after
observation of at least 20 fields, according to the criteria of
Washington et al. (30).
Semiquantitative urine culture.
Semiquantitative urine culture
using the calibrated loop technique (6) and inoculation on
cystine-lactose-electrolyte-deficient agar (Difco Laboratories,
Detroit, Mich.) was employed as the reference method. Samples were
considered positive if they contained 105, or
104 to <105, CFU of the urinary pathogen/ml of
pure culture. Also considered to indicate a urinary infection was
isolation of two potentially pathogenic bacterial species, when the
individual counts for the two species were >105 and
>105, >105 and >104, or
>104 and >104 CFU/ml, or when the count for
one organism was >104 CFU/ml and it was clearly
predominant, i.e., at least 10-fold more than the other (6).
Urine specimens containing 105 or <105
CFU of nonpathogenic bacteria (lactobacilli, diphtheroids,
Staphylococcus epidermidis, or non-group-D
Streptococcus spp.)/ml or multiple (three or more) species
of gram-negative bacteria, obtained from patients without clinical
evidence of urinary infection, were considered contaminated and were
excluded from the study. Isolated microorganisms were identified by
standard biochemical procedures (4).
Statistical analysis.
Sensitivity, specificity, and positive
and negative predictive values were calculated by the method of
Ransohoff and Feinstein (27), according to the following
formulae: (i) sensitivity = TP/(TP + FN), the probability
that the microscopic examination will be positive in patients with
urinary infections (positive culture), (ii) specificity = TN/(TN + FP), the probability that the microscopic examination
will be negative in patients without urinary infections (negative
culture), (iii) positive predictive value = TP/(TP + FP), the
probability that a urinary infection is present when the microscopic
examination is positive, and (iv) negative predictive value = TN/(TN + FN), the probability that a urinary infection is not
present when the microscopic examination is negative, where TP stands
for true positive (microscopy and cultures both positive), FP for false
positive (positive microscopy and negative culture), TN for true
negative (microscopy and culture both negative), and FN for false
negative (microscopy negative and culture positive). Comparison of the
mean numbers of bacteria found in 10, 20, 30, 40, and 50 oil immersion
fields of the microscopic Gram-stained preparations made with 10 µl
(loop technique) and 50 µl (drop technique) of positive urine
specimens (>104 to 105 CFU/ml) was performed
by using Student's t test for independent samples at a 5%
significance level, with the program STATISTICA for Windows,
release 4.3 (1993; StatSoft, Inc., Tulsa, Okla.).
Four hundred fifty-six of the 500 urine samples analyzed were collected
by spontaneous urination (clean catch midstream), and 44 were collected
with a plastic collecting bag. Most (80.42%) were from outpatients;
the remainder were from inpatients. The ages of the patients ranged
from 2 days to 87 years (mean, 32 years).
The incidence of positive cultures was 24.8% (124 of 500). The
following groups of urinary pathogens (with the number of samples infected with each species in parentheses) were identified: (i) gram-negative bacilli, including Escherichia coli (74),
Klebsiella pneumoniae (9), Pseudomonas aeruginosa
(8), Klebsiella ozaenae (6), Enterobacter
aerogenes (2), Citrobacter diversus (2),
Proteus mirabilis (2), Enterobacter agglomerans
(1), Enterobacter sp. (1), and Morganella
morganii (1); (ii) gram-positive cocci, including Staphylococcus saprophyticus (5), Enterococcus
faecalis (3), S. epidermidis (3), Staphylococcus
aureus (2), group-D Streptococcus sp. (2), and
Enterococcus sp. (1); and (iii) fungi, i.e., yeast (1). In
approximately 95% of the positive cultures (118 of 124), the
etiological infective agent was isolated in pure culture, at a
concentration of 105 CFU/ml.
The results of the two microscopy techniques showed 100% correlation.
This was not at all surprising, considering that the 10- and 50-µl
methods used the same urine with the same concentration of bacteria.
The mean diameters of the smears made with the calibrated loop (10 µl) and the drop (50 µl) of urine were 6 and 11 mm, respectively. With regard to drying time, the smears made with the loop appeared dry
in 10 to 15 min, as opposed to 3 to 5 h for those prepared with a
urine drop.
Table 1 shows the correlation of the
microscopic examinations with the cultures of the 500 urine specimens
studied. Disagreement was observed in eight samples, with five
false-negative results (negative microscopy and positive culture) and
three false-positive results (positive microscopy and negative
culture). In the latter there were pleomorphic, weakly stained
gram-negative bacilli, suggestive of anaerobic bacteria. The
microscopic examination, however, showed high sensitivity (96.0%) and
specificity (99.2%) as a diagnostic method for significant
bacteriuria (Table 1).
No statistically significant differences (P > 0.05)
were found in relation to the mean numbers of bacteria observed in 10, 20, 30, 40, and 50 oil immersion fields of the stained microscopic preparations made with 10 µl (loop technique) and 50 µl (drop technique) of the positive urine samples.
In the positive microscopic urine examinations (122 of 500), the mean
number of bacteria found in the 50 microscopic fields was 66.30 bacteria for the drop technique and 48.47 for the loop technique. On
the other hand, in the 378 negative microscopic examinations, means of
0.16 and 0.18 bacteria, respectively, were found for the loop (10-µl)
and drop (50-µl) techniques.
Microscopic examination of urine for detection of significant
bacteriuria can be performed in bacteriological practice by four basic
procedures: (i) examination of uncentrifuged fresh urine with a 40×
dry objective, (ii) observation of fresh urinary centrifuged sediment
with a 40× dry objective, (iii) examination with an oil immersion
objective (100×) of a Gram-stained smear of uncentrifuged urine, and
(iv) observation of a Gram-stained smear of centrifuged urine with an
oil immersion objective (11). In the present investigation,
we chose to use microscopic examination of uncentrifuged Gram-stained
urine, because this is considered the most easily performed, the least
expensive, and probably the most sensitive and reliable diagnostic
method for identifying urine specimens containing more than
105 CFU/ml (4).
Although microscopic examination of an uncentrifuged
Gram-stained urine drop is recognized as the conventional
microscopic method for diagnosing urine specimens with counts of
105 CFU/ml, being recommended as the routine procedure in
bacteriological practice by several authors (4, 6, 7, 10, 11, 16, 17, 20, 25, 26, 30), no standardized technique exists for
performing this procedure in the microbiological laboratory (11).
This lack of standardization is evidenced, for example, in 14 studies
recorded in the literature, involving microscopic examination of
approximately 46,200 urine specimens, in which the sensitivity of the
method for detection of significant bacteriuria varied between 69 and
99%. In relation to the volume of urine used, in six of these studies
(3, 7, 8, 15, 30, 31) the use of the drop (50-µl)
technique was described, and in eight (1, 9, 10, 12, 19, 23, 29,
32) the calibrated loop technique was used, with urine volumes
varying from 5 to 10 µl. The number of microscopic fields examined
per urine sample was 5 (23, 31, 32), 10 (7-9),
20 (3, 30), or 50 (1, 29). Some authors used an
observation parameter of 30 s (15), and others used an
observation parameter of 3 min (9, 19). The different
criteria for positivity for the microscopy included the presence of 1
(1, 12, 15, 23, 29, 32), 2 (3, 30, 31), 5
(8), or even any number of microorganisms per oil immersion
field (7, 9, 10, 19).
The choice of criteria of positivity of the microscopic examination
used in our investigation was based on a representative study in which
the authors analyzed 32,076 urine specimens and obtained 94%
sensitivity and 90% specificity in the detection of significant
bacteriuria (30). In our study all the positive microscopic
examinations (122 of 500) showed more than two bacteria per field, and
in the 378 negative examinations we always observed fewer than two
microorganisms per field. Nevertheless, it is worth mentioning that we
found a mean of 1 to 1.5 bacteria per 20 fields in five negative urine
specimens, which would give false-positive results if we were to employ
a criterion of 1 microorganism per field.
Weinberg and Gan (31), on the basis of a study of
microscopic examination of 1,019 urine specimens to diagnose urinary
infection, emphasized that changing the criterion of positivity from
1 to 2 bacteria per oil immersion field improved the efficacy of
the method, maintaining practically unchanged the 97.6% sensitivity but increasing the specificity from 87% to 94%. Our results were consistent with this observation.
Detection of significant bacteriuria by microscopic examination of 10 µl of uncentrifuged Gram-stained urine (loop technique) is described
in three studies (1, 29, 32) in which the authors, using
procedures similar to that employed in our investigation, found
sensitivities of 94.1, 96.2, and 92.9%, respectively. These values
were similar to the 96.0% sensitivity described in the present study.
Perhaps the lower sensitivity obtained in one of the studies
(32) was due to the criterion for positivity represented by
the finding of 1 gram-negative bacillus in 5 fields examined, excluding the presence of gram-positive bacteria, which, in our investigation, for example, represented 8.1% (10 of 124) of the isolates. In two of these studies (1, 29) a procedure
slightly different from ours was used, in which the urine smear was
spread with the 10-µl loop soon after application, over a 30-mm area of the slide. The authors used as a criterion of positivity the presence of 1 microorganism in 50 fields examined.
It is worth pointing out that in our study, spontaneous drying of the
10 µl of urine applied on the slide led to accumulation of bacteria
at the edge of the drop in all the positive urine specimens,
facilitating the reading of the microscopic examination (Fig.
1). This was not observed in the negative
urine samples.
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FIG. 1.
Microscopic field (oil immersion objective) showing the
accumulation of E. coli at the edge of the urine drop (to
the left) with the Gram-stained preparation of 10 µl of a positive
urine specimen (105 CFU/ml). A DIAPLAN microscope (Leitz,
Wetzlar, Germany) and Tri-X pan ISO 400/27 film (Eastman Kodak Company,
Rochester, N.Y.) were used.
|
|
The chief advantage of performing microscopic examination of
uncentrifuged Gram-stained urine as part of the bacteriological routine of urine cultures is the presumptive rapid diagnosis of urinary infection and guidance for initial patient treatment based on
the form and staining properties of the probable etiological infective
agent; these can be made available while the clinic awaits the results
of the urine culture and antibiotic sensitivity tests, which are
generally available within 24 to 48 h (6, 11). Other
advantages of this method include low cost and high specificity and
sensitivity for detection of significant bacteriuria in urine specimens
containing 105 CFU/ml (4, 6, 11, 25, 28-30).
On the other hand, in the opinions of some authors (2, 6,
17), microscopic examination of stained urine preparations, besides being a lengthy, tedious process because of the large number of
negative urine cultures, has some limitations. There are the
possibilities of false-negative results due to loss of bacteria in the
case of inadequate fixation of the material on the slide and of
false-positive results as a result of the presence of artifacts or the
use of contaminated staining solutions (2). The low
specificity and sensitivity of this method for detecting bacteriuria in
urine specimens containing <105 CFU/ml, which may be
significant at the 104-CFU/ml level or in symptomatic
patients with 102 to 104 CFU/ml, are well
recognized (6, 26, 32).
Based on these considerations, a probable explanation for the
false-negative results of the microscopic examination obtained in our
study (5 of 124), is loss of the urine smear from the slide during the
staining process because of inadequate fixation of the material. In
relation to the false-positive results (3 of 376), the evidence
indicates possible infections of the urinary tract caused by fastidious
or anaerobic bacteria. In all three cases, there was a positive smear
and the specimens failed to grow on aerobic culture. These patients
were not being treated with antibiotics.
The major limitation of the microscopic method reported in this study
is its decreased sensitivity for detecting bacteriuria in urine
specimens containing <105 CFU/ml, a level that may be
present in the acute dysuric syndrome in women, in infection in
children, in infection in adult males, and in patients with urinary
catheters (13, 21, 22, 26, 32). In addition, many clinical
laboratories use 104 CFU/ml as a reportably and clinically
significant result. This number is below the sensitivity of the
microscopic method reported here. On the other hand, in urine specimens
containing 105 CFU/ml, usually associated with
asymptomatic patients, patients with acute pyelonephritis, and patients
with acute cystitis, a Gram-stained smear may be used as an accurate
and inexpensive screening method (4, 6, 20-22, 26).
As evidenced in our study, microscopic examination of 10 µl of
uncentrifuged Gram-stained urine showed no difference in the indices of
efficiency for detection of significant bacteriuria compared to the
conventional method of microscopic examination of a urine drop (50 µl). The rapid drying time of the 10-µl volume facilitates the use
of this technique in bacteriological practice. Nevertheless, it is
important to point out that for defining a positive microscopic
examination, the microorganisms must be uniformly distributed over at
least 10 oil immersion fields examined. The presence of many epithelial
cells from desquamation, sometimes associated with the presence of
different morphological and staining types of bacteria, indicates
probable contamination of the urine specimen.
In summation, the results obtained in the present investigation
demonstrated that the loop technique (10 µl) can be utilized as an
alternative to the conventional drop technique (50 µl) for detecting
significant bacteriuria, with the advantage of greater rapidity and
simplicity of execution. As criteria for a positive microscopic
examination, we recommend the reading of 10 oil immersion fields, with
the presence of at least two microorganisms per field.
| |
ACKNOWLEDGMENTS |
We gratefully acknowledge the staff of the Maringá Regional
University Hospital for collecting and storing the urine specimens and
Yoshiaki Fukushigue for statistical analysis of the data. Janet W. Reid
translated the manuscript into English.
The investigation was carried out with financial support from the
National Council of Scientific and Technological Development (CNPq
Proc. 520118/95-2).
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Laboratory of
Microbiology, Department of Clinical Analyses, State University of
Maringá, 5790 Colombo Ave., 87020-900 Maringá,
Paraná, Brazil. Phone: 55 44 261-4429. Fax: 55 44 263-5116. E-mail: deres{at}cybertelecom.com.br.
| |
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Journal of Clinical Microbiology, March 1998, p. 820-823, Vol. 36, No. 3
0095-1137/98/$04.00+0
Copyright © 1998, American Society for Microbiology. All rights reserved.
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