Visual and Clinical Analysis of Bac-T-Screen Urine Screen Results

Transcription

1 JOURNAL OF CLINICAL MICROBIOLOGY, Nov. 1988, p /88/ $02.00/0 Copyright C 1988, American Society for Microbiology Vol. 26, No. 11 Visual and Clinical Analysis of Bac-T-Screen Urine Screen Results ELLEN JO BARON,1,2t* MARY B. TYBURSKI,1 RENEE ALMON,3 AND MARJORIE BERMAN' North Shore University Hospital, Manhasset, New York ; Cornell University Medical College, New York, New York ; and Brookdale Hospital Medical Center, Brooklyn, New York Received 14 March 1988/Accepted 9 August 1988 Of 337 urine specimens evaluated, 75 of the 113 that showed positive readings on the Bac-T-Screen urine-screening instrument were found by subsequent semiquantitative culture to yield either less than 10,000 CFU of mixed bacteria per ml or no growth (less than 100 CFU/ml by our criteria). We tried to determine what factors contributed to the positive Bac-T-Screen results by examining the 75 Bac-T-Screen-positive urine specimens with three visual methods: Gram staining, hemacytometer chamber counting, and filtering through a 5.0-,um-pore-size nitrocellulose filter with subsequent microscopic examination of the stained filter. Somatic cells and other particles present in those urine specimens that yielded positive readings by the Bac-T-Screen included epithelial cells in 43%, crystals and amorphous material in 33%, and leukocytes in 17% of the specimens. There was no relationship between the numbers of particles seen in urine and the magnitude of the relative absorbance reading obtained with the Bac-T-Screen. A retrospective chart review was conducted for patients with positive Bac-T-Screen results and negative cultures. Of the 75 patients, 6 were thought to have urinary tract infections on the basis of clinical criteria; the majority of the remaining 69 patients had clinical histories revealing systemic or urogenital conditions consistent with shedding of particles in the urine. A positive reading by the Bac-T-Screen system seemed to be related to the presence of somatic cells and other particles in urine; bacteriuria was not always detectable in these cases. A number of screening methods have been advocated in the continuing effort to streamline microbiological laboratory procedures to provide more rapid results to physicians and to decrease unnecessary specimen processing (5, 21). With the availability of automated methods such as nephelometry, bioluminescence, and colorimetric particle analysis, screening of urine specimens has gained widespread acceptance (3, 4, 6, 12-16). Urine specimens represent a large proportion of the specimens received by many laboratories, and the number of cultures yielding negative or clinically insignificant results is usually high (18). For these reasons, the ability to rapidly report a negative result and preempt further processing of a urine specimen is an attractive alternative to routine culturing. The Bac-T-Screen (BTS; currently marketed by Vitek Systems, McDonnell Douglas Corp., Hazelwood, Mo.) is used by approximately 300 laboratories throughout the United States for initial screening of urine specimens. It has been shown in several studies that positive BTS results are an accurate predictor of urinary tract infection (UTI), with a sensitivity of 85 to >90% when 105 bacteria per ml of urine is considered a positive culture result (12, 16, 17, 22). Many studies however, have found a consistent incidence of falsepositive results, even when criteria for positive cultures include those urine specimens with bacterial or yeast colony counts less than 104 CFU/ml. We sought to determine what factor(s) might be responsible for such positive BTS results from urine specimens that subsequently failed to yield culture results that fell within our definition of positive (>10,000 CFU of three or fewer species per ml). Additionally, we sought to determine whether patients whose urine specimens fell into this category might be evaluated clinically as having true UTIs despite the bacteriologically insignificant culture * Corresponding author. t Present address: Clinical Anaerobic Bacteriology Research Laboratory, Wadsworth Veterans Administration Medical Center, Wilshire and Sawtelle Boulevards, West Los Angeles, CA results. Urine specimens were tested on the BTS and cultured semiquantitatively with a 0.01-ml calibrated loop. In addition, the specimens were examined visually by three different methods: (i) hemacytometer particle counting, (ii) Gram staining, and (iii) filtration through a 5.0-ptm-pore-size nitrocellulose filter and staining of the material remaining on the filter surface. Because the BTS system is based on the colorimetric detection of stained particles remaining on the surface of a filter through which the urine specimens have been passed, we reasoned that we could detect the particles responsible for false-positive results with at least one of the three visualization methods. MATERIALS AND METHODS Specimens. Three hundred thirty-seven urine specimens received for routine culture were evaluated. No catheterized, surgically obtained, or bladder urine specimens were included in the study, since such specimens are not processed by BTS in our laboratory. The majority of specimens were received in sterile screw-cap cups within 2 h of collection and were refrigerated at 4 C until processed. BTS assay. Urine specimens were processed according to the instructions of the manufacturer by passing 1.0 ml of urine through the filter of a BTS (Model 402, Vitek). Relative absorbance (RA) values were determined by placing the reacted filter card into a card reader, whiçh is supplied with the BTS instrument. All specimens with RA values greater than or equal to 4 U above the reagent blank and those that failed to pass through the filter were considered positive. Specimens yielding RA values less than 4 or greater than 30 U above the negative control blank were cultured but were not evaluated by any of the particle visualization methods. Culture. Urine specimens were mixed thoroughly, and 0.01 ml was inoculated onto MacConkey, Trypticase soy- 5% sheep blood, and Columbia base colistin-nalidixic acidagar plates (BBL Microbiology Systems, Cockeysville, Md.) via a vertically inserted calibrated platinum loop. Cultures were incubated overnight at 35 C in air. All cultures were

2 VOL. 26, 1988 POSITIVE URINE SCREEN RESULTS 2383 TABLE 1. Semiquantitative grading system for enumerating particulate urinary components retained on nitrocellulose filter No. (density) of particles per microscopic field for rank of: Negative Occasional i Erythrocytes or epithelial cells 0 < >30 (Less than packed) Packed field Leukocytes 0 < >30 (Less than packed) Packed field Crystals or amorphous material 0 < >30 Bacterial or yeast cells 0 < >30 (Less than packed) Packed field a Urine (1 ml) was passed through the filter, which was stained with 0.03% methylene blue and examined at a magnification of x400. reincubated and examined for a second time after an additional overnight incubation before being discarded. Bacteria were identified by using conventional procedures, and yeasts were identified by colonial and microscopic morphology. Estimated CFUs were determined. Hemacytometer assay. A drop of well-mixed, undiluted urine was placed on two sides of a standard hemacytometer and covered with a weighted cover slip. The slide was examined at a magnification of x400 and the numbers of bacteria, yeast cells, epithelial cells, leukocytes, erythrocytes, and other particles present within the etched counting areas on both grids of the hemacytometer were counted. Specimens were considered positive for a specific cell or particle type if more than 6 particles per mm3 were counted, which corresponded to 6,000 particles per ml of urine (8). Gram stain. A modification of the procedure outlined by Washington et al. was used (21). Briefly, a measured, 0.01-ml heaped drop of urine was air dried and stained and at least 20 microscopic fields were examined at a magnification of x 1,000 (oil immersion). The presence of one or more bacteria, yeast cells, or other cells or particles per field was considered positive. Filter assay. The same amount of urine as was used in the BTS assay (1 ml) was drawn into a 3-ml disposable plastic syringe. The syringe was attached to a filter holder containing a 5.0-,um-pore-size, 25-mm-diameter nitrocellulose filter (Millipore Corp., Bedford, Mass.), and the urine was forced through the filter. The filter was carefully removed from the filter holder and allowed to air dry. The filter was placed on a large glass slide, flooded with 0.03% methylene blue stain for 1 min, and allowed to air dry again. For microscopic evaluation, the stained filter was placed on the surface of a large glass slide, flooded with xylene (which cleared the nitrocellulose), covered with a large cover slip, and examined at a magnification of x400., including epithelial cells, leukocytes, erythrocytes, crystals, and amorphous material, could be visualized. Numbers of somatic cells, bacteria, and crystals were graded semiquantitatively according to a modification of the scale recommended for evaluation of urine sediment by Henry (8) (Table 1). Scores of 2+ or higher were considered positive. The surface area of the filter was 491 mm2, and there are 625 microscopic fields per filter when visualized at a magnification of x400. Assuming a fairly even distribution of the 1.0-ml drop of urine over the entire surface, 10 cells per field would correspond to approximately 6,250 cells per ml of urine. Clinical history review. Charts of patients whose urine specimens yielded <10,000 CFU/ml despite RA values between 4 and 30 were retrospectively reviewed by using criteria similar to those employed by Murray et al. (12). The following data were recorded: results of urinalysis performed on the same specimen as that received for culture; presence of fever, dysuria, frequency or urgency, flank or abdominal pain, foul-smelling urine, or urethral discharge; previous antimicrobial therapy or institution of new therapy based on urine culture or urinalysis results; relevant medical history; and clinical impression. For instances in which clinical impression could not be divined from the chart, a physician familiar with the patient was consulted. Patients were judged as having a UTI if they were placed on new antimicrobial therapy as a result of urinary signs or symptoms or if the physicians' notes stated the diagnosis or clinical impression of UTI. We judged patients as not having UTI when there were no notes in the chart or changes in management attributable to the results of urine studies. Additionally, we consulted verbally with physicians on all equivocal patient histories. RESULTS BTS assay. The RA of the negative control blank was arbitrarily set at zero for each day's testing, and all RA values greater than that of the negative control were adjusted accordingly. Thirty-five urine specimens showed positive BTS results (RA values >4) and yielded >10,000 CFU of bacteria or yeast cells (three or fewer total different species types) per ml. Three urine specimens obtained from females visiting the outpatient gynecologic clinic had RA values >30 and yielded pure cultures of Escherichia coli in numbers ranging from 102 to 104 CFU/ml. These 38 results were considered by the authors to be true positives and were not evaluated further. An additional 208 urine specimens with negative BTS results (RA values <4) yielded no growth or <10,000 CFU of mixed organisms, including staphylococci, diphtheroids, lactobacilli, and streptococci, per ml and were considered to be true negatives by our criteria. Thus, 61.7% of all urine specimens tested would have been accurately screened as negative by BTS, preempting further processing. There were 16 false-negative results (4.8%) for which the BTS RA was <4 but for which cultures yielded (per milliliter) >10,000 CFU of microorganisms determined to be bacteriologically significant. These cultures grew enterococci (five specimens), group B beta-hemolytic streptococci (three specimens), E. coli and enterococci mixed (two specimens), E. coli alone (one specimen), Morganella morganii and enterococci mixed (one specimen), Enterobacter aerogenes and enterococci mixed (one specimen), coagulasenegative staphylococci (one specimen), Candida albicans and mixed gram-positive cocci (one specimen), and yeast species alone (one specimen). The remaining 75 specimens showed BTS RA values between 4 and 30 and yielded <10,000 CFU/ml or no growth (<100 CFU/ml by our criteria) on culture. These 75 specimens were included in the study and evaluated by the visual assays described above. RA values recorded for the 75 specimens whose positive BTS results failed to predict bacteriologically significant urine cultures (>104 CFU/ml) were arbitrarily divided into three categories: low (4 to 12 RA units), medium (13 to 21 RA units), and high (22 to 30 RA units). Culture. Of the 75 urine specimens included in the study, 37 (49%) yielded no growth. Of the 38 urine specimens

3 2384 BARON ET AL. TABLE 2. Comparison of three visual methods for the detection of particulate urinary components No. (%) of 75 tested urine specimens considered positive for each particle as determined by: Hemacytometer Stained filter Gram stain Epithelial cells 23 (31) 32 (43) 20 (27) Erythrocytes 10 (13) 3 (4) 4 (5) Leukocytes 13 (17) 11 (15) 8 (11) Bacteria or yeasts 13 (17) 12 (16) 19 (25) Crystals or amorphous 23 (31) 25 (33) 14 (19) material showing microbial growth, cultures yielded mixed cultures of lactobacilli, coliforms, Corynebacterium species, staphylococci, or streptococci and were not considered to be indicative of an infectious process (9, 10). Low numbers (102 to 104) of pure cultures of a member of the family Enterobacteriaceae or Staphylococcus aureus were not encountered among this limited sample. Visual assays. Numbers and percentages of urine specimens showing cells and particles by each visual assay are listed in Table 2. For leukocytes, microorganisms, and crystals and amorphous material, the hemacytometer and filter assays revealed similar numbers and types of particles (Table 2). The filter assay failed to detect intact erythrocytes. Since the BTS detects pigment as one component of a positive RA and lysed erythrocytes are known to contribute some pigment, the influence of erythrocytes on BTS results could be inferred from hemacytometer results only (15). The Gram stain was less sensitive for the detection of RBCs, crystals, and amorphous material than were the other methods, although the Gram stain was able to detect bacteria or yeast cells in all but one specimen in which they were detected by any method. Of 25 Gram-stain-negative urine specimens, 13 contained amorphous material or crystals or both, 9 contained epithelial cells, 3 contained leukocytes, and 1 contained yeast cells and pseudohyphae, as visualized by at least one other assay. There were no screen-positive specimens in which the presence of bacteria or yeast cells alone was detected without additional other particles, when results from all methods were compared. Results obtained by testing urine by the filter and stain assays were compared with the corresponding BTS RA values (Table 3). The relative number or presence of particles detected in a specimen did not correlate quantitatively with its RA value. Clinical history review. Relevant patient findings included only six patients (8%) thought by their physicians to have UTI despite nonsignificant culture results; three were patients whose urine specimens yielded no growth. Numerous conditions that might contribute to the presence of particles in their urine were documented in the patients evaluated (Table 4). Additionally, 47 (63%) patients were on antimicrobial therapy when cultures were obtained, indicative of a preceding infectious process. DISCUSSION False-positive BTS results seemed to be due to cells and other particles being trapped and stained in the filter. Seventeen percent of the urine specimens studied contained leukocytes by at least one visual assay method. More than 10 leukocytes per mm3 has been shown by some workers to TABLE 3. Urinary RA values obtained with BTS compared with particles seen on stained filters No. of specimens positive for a given particle by the stained filter assay with the following BTS RA values: Low Medium High (4-12) (13-21) (22-30) Leukocytesb Epithelial cells 18 il 3C Crystals or amorphous material 8 9 8d a Urine specimens were considered positive if a given particle had a score of 2+ or higher (see Table 1). b Of 11 urine specimens with leukocytes, 3 (27%) also showed bacteria or yeasts. c Of three urine specimens with high RA values and positive epithelial cell scores, two (67%) also contained leukocytes or erythrocytes. d Of eight urine specimens with high RA values and crystals, only two (25%) contained other particles (epithelial cells in both cases). correlate well with a leukocyte excretion rate of >400,000/h, which is indicative of an infectious process, and Fairley and Barraclough found more than 8 leukocytes to be abnormal pyuria (4, 7). We considered >6 leukocytes per mm3 to be positive in our hemacytometer counts to conform more closely to the filter assay, skewing the data slightly in favor of the patient. Pfaller et al. found >10 leukocytes per mm3 by hemacytometer count in 68 of 240 patients judged not to have urinary tract infection by clinical and bacteriologic grounds, for a false-positive rate of 28% as determined by hemacytometer assay (17). This value is higher than our finding that 17 and 15% of specimens without significant bacterial growth contained leukocytes by hemacytometer assay and by filter and stain, respectively. Our hemacytometer assay, however, was only used as an additional visual method for determining the nature of particles that might be trapped on the BTS filter and was not meant to yield the same data as a true urine cell count. Our criteria for positivity are not the same as those used for quantitative assays for pyuria. The delay between urine collection time and our visual examination, as well as the refrigeration of our samples, both of which are factors known to result in lysis of leukocytes, could account for the lower numbers of leukocytes that we were able to visualize. In addition, 63% of our patient population were receiving antimicrobial therapy before cultures were obtained, and an additional 33% TABLE 4. Clinical parameters for patients whose urine specimens yielded positive BTS results but failed to yield significant bacteriological culture results Patient characteristic No. (%) of patients with cultures yielding: No < 10,000 growth CFU/mlb Receiving antimicrobial therapy 25 (68) 22 (58) Diagnosis of cancer 9 (24) 7 (18) Postoperative 6 (16) 3 (8) Foley catheter in place 6 (16) 4 (11) Previous UTI this admission 2 (5) 4 (11) Postpartum 2 (5) 2 (5) Renal failure 0 2 (5) Clinical diagnosis of UTI 3 (8) 3 (8) " Thirty-seven patients. b Thirty-eight patients. J. CLIN. MICROBIOL.

4 VOL. 26, 1988 had predisposing conditions (surgery or cancer) whose symptoms may have mimicked those of UTI. Our use of the hemacytometer was not meant to aid in diagnosis of UTI, since the urine specimens were not usually evaluated within the time recommended for validity of such assays; Stamm et al. used 1 h as the maximum allowable time after collection during which leukocytes could be counted (20). Urine specimens from the six patients in our series that were judged clinically to have UTI all showed leukocytes by at least one method, however; one of these specimens also contained casts, as seen with the hemacytometer. The Gram stain was the least reliable method for detecting erythrocytes and crystals. However, our procedure did not include methanol fixation. The addition of this step should significantly enhance the sensitivity of the Gram stain at least for somatic cells, whose physiology would be preserved. Approximately 43% of urine specimens yielding screen results that failed to predict significant bacteriuria contained more than 6,000 epithelial cells per ml. Although better specimen collection practices may decrease the numbers of specimens with large numbers of epithelial cells, our results indicate that poor collection alone does not account for many of our false-positive urine results. The nitrocellulose filter assay was assumed to most closely simulate the BTS filtering, washing, staining, and colorimetric reading system. Only the nuclei of epithelial cells trapped in the nitrocellulose filter stained blue; it would thus seem to require a very large number of such cells lying on top of each other to affect the colorimeter. Two of eight specimens with high RA values ostensibly due to crystals also revealed other particles, which were epithelial cells in both cases. Overall, 33% of the false-positive urine specimens showed crystals or amorphous material. Only 3 of the 11 urine specimens (27%) with leukocytes also contained bacteria as visualized microscopically, and none contained yeast cells. The bacteria may have failed to grow in culture because of previous antibiotic therapy, because they were anaerobic, or because they required nutritional supplements not present in our routine media (such as Haemophilus species, reported to be urinary tract pathogens under some circumstances) (2). All three of these urine specimens were from patients judged on clinical grounds to have UTI. It is thus probable that these three specimens represent true positives that were detected by BTS but missed by culture. The remaining eight specimens with >2+ leukocytes (including the additional three specimens from patients judged by physicians to have UTI) may have harbored Mycoplasma species, viruses, Chlamydia species, or bacteria in numbers below the limits of our detection system, or may have been the result of a noninfectious condition (11, 19, 20). On the basis of the low numbers of patients in our study with leukocytes and the fact that patients on antibiotics were being treated for a condition other than UTI in most cases, we feel that our false-positive BTS results, other than those described above, are true false-positives in the sense that the majority of the patients being tested did not have a current UTI. Murray et al. reported 174 positive BTS results from patients judged clinically to have no infection among 500 urine specimens tested, for a true false-positive rate of 34.8% (12). Two-thirds (63%) of the false-positive BTS results reported by Murray et al. came from urine specimens with pyuria or colony counts between 104 and 105 CFU/mI, whereas only 17% of our false-positives had evidence of pyuria. With detailed clinical analysis, those authors found POSITIVE URINE SCREEN RESULTS 2385 good correlation between BTS-positive results and the presence of infection as determined clinically using criteria similar to ours. Our study differed from that of Murray et al. by excluding all catheterized urine specimens, which are more likely to contain sloughed cellular material and thus to test falsely positive by BTS (Murray et al. included 38.2% catheterized specimens), and by excluding those specimens that yielded organisms in amounts >10,000 CFU/ml, which we considered positive bacteriologically and did not evaluate further. Inclusion of the latte& group of urine specimens in our study would have enhanced the relative sensitivity of the BTS by including more true positives in the data base. Our findings agree with those of Murray, et al. in that increasing the RA value considered to be positive to decrease the number of'urine specimens plated would decrease the sensitivity of tbé screen system (12). With the BTS, Murray et al. could eliminate further processing of approximately half of all urine specimens submitted for culture, only slightly less than the 62% true negative results that we report here. Using the culture criterion of >104 CFU/ml as positive, Bixler-Forell et al. found 22.3% false-positive results with the BTS (3). Wright and others found only 15% false-positive urine specimens when >105 CFU/ml was used as the definition of a positive urine culture (22). These workers used a ml calibrated loop, in contrast to the other studies and our own, in which a 0.01-ml loop was used. The small loop accounts for a greater number of errors in sampling, as documented by Albers and Fletcher (1). This may account, in part, for the lower false-positive rate reported by Wright et al. It is also possible that urine specimens submitted to Wright's group were collected more carefully than those evaluated by other workers. As is apparent from the data cited above, epithelial cells are a contributory factor to false-positive BTS results. The same cellular and particulate elements that contribute to false-positive BTS results, however, may aid in detecting urine specimens from patients with UTI and numbers of bacteria or yeast cells of <105 CFU/ml. As suggested by Wright and co-workers, the impact of microbial virulence factors on epithelial adherence and the sloughing of leukocytes and other particulate matter may contribute to the ability of BTS to reliably detect urine specimens likely to yield clinically relevant culture results, despite the absence of traditionally positive culture results of >105 CFU/ml (12, 22). For the same reason, such particles present in nonbacteriuric urine are likely to increase the number of potentially false-positive urine specimens detected by the BTS screening system. Judging from clinical data collected on patients in this study, the presence of a positive BTS result should serve to alert health care providers of the possible presence of an abnormal clinical condition or urogenital disorder which may not always be detected by routine bacteriological culture. LITERATURE CITED 1. Albers, A. C., and R. D. Fletcher Accuracy of calibratedloop transfer. J. Clin. Microbiol. 18: Albritton, W. L., G. W. Hammond, and A. R. Ronald Bacteria Haemophilus influenza genitourinary tract infection in adults. Arch. Intern. Med. 138: Bixler-Forell, E., M. A. Bertram, and D. A. Bruckner Clinical evaluation of three rapid methods for the detection of significant bacteriuria. J. Clin. Microbiol. 22: Clarridge, J. E., M. T. Pezzlo, and K. L. Vosti Cumitech 2A, Laboratory diagnosis of urinary tract infections. Coordinating ed., A. S. Weissfeld. American Society for Microbiology, Washington, D.C.

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