Urinary Tract Infections: Role of the Clinical Microbiology Laboratory

Mark Smyth John E. Moore Colin E. Goldsmith

rinary tract infections Urinary tract infections (UTIs) are common infectious diseases in all (UTIs) are common both ages of humans, from the neonate through to the elderly, with certain in the community and ages having an increasesed occurrence of specific bacterial etiolo- hospital and involve the gies. Clinical microbiology forms an important cornerstone in the sci- Uinteraction between clinician and entific workup of (a) detecting a causal agent responsible for the UTI, clinical microbiologist. To many, (b) phenotypic and increasingly genotypic identification of causal the role of the clinical microbiolo- agents of UTIs, and (c) characterization of identified agents of UTIs, gy laboratory remains a “black including antibiotic susceptibility testing and virulence testing. For box,” which generates microbiol- most clinicians, the workings of clinical microbiology remain a “black ogy laboratory reports that may box;” hence, the main objective of this review is to present scientif- aid in patient management. ic insight into how clinical microbiology handles the laboratory Several authoritative reviews on the management of UTIs have workup of urine specimens, and the pearls and pitfalls of urine micro- been published recently (Dulczak biology that may cause delay and frustration in the feedback of & Kirk, 2005). Therefore, the aim microbiology data to the patient’s clinician. of this review is to discuss the role of the microbiology laboratory to those clinical disciplines inter- nificant proportion of the work- lower and upper urinary tracts. ested in learning about updates load in most clinical microbiolo- Infections can be further classi- in diagnostic methodologies in gy laboratories. A UTI is normal- fied as uncomplicated and com- microbiologic urology. ly diagnosed based on medical plicated depending on the extent UTIs are among the most history and a physical examina- and duration of the infection. prevalent bacterial infections tion. Confirmation of a urinary In an uncomplicated UTI, the affecting both genders and all age tract infection requires a labora- most common site of infection is groups. They also represent a sig- tory examination of a urinary usually the urinary bladder. The sample, using a combination of most common route of access for microscopy and bacterial cul- pathogenic micro-organisms is Mark Smyth, MSc, BSc, is a ture. Bacterial isolates will then an ascending infection from Biomedical Scientist, Northern Ireland undergo antimicrobial sensitivity neighboring sites, in particular, Public Health Laboratory, Belfast City testing to provide the clinician from the urethra and perianal Hospital, Northern Ireland, United with antibiotic choices, if regions. A less-common route is Kingdom. required for the patient. spread from the cardiovascular system, which is typical in infec- John E. Moore, PhD, BSc, is a Overview of Urinary Tract tions caused by Salmonella spp. Clinical Scientist, Northern Ireland Infections Public Health Laboratory, Belfast City and Mycobacterium tuberculosis Hospital, Northern Ireland, United The urinary tract above the (Hawkey & Lewis, 2003). Kingdom. level of the distal urethra is nor- Cystitis is the term used to mally sterile but infection can describe uncomplicated lower Colin E. Goldsmith, MB, BCh, BAO, occur at any site from the kidney urinary tract infection of the BSc, MRCPath, is a Consultant in to the urethra. Urinary tract bladder. Signs and symptoms Medical Microbilogy, Northern Ireland infections may involve just the include a combination of factors Public Health Laboratory, Belfast City lower urinary tract, or the infec- including dysuria, urgency, fre- Hospital, Northern Ireland, United tion may encompass both the quency, hematuria, and suprapu- Kingdom.

198 UROLOGIC NURSING / June 2006 / Volume 26 Number 3 bic pain. Upper urinary tract infection is commonly described Once adulthood is reached, the prevalence of as pyelonephritis and is often steadily increases in the female associated with the symptoms of cystitis combined with flank population. pain and abdominal tenderness. Cystitis and pyelonephritis often present as acute diseases, but recurrent or chronic infections abnormalities. Patients with of the female population will may also occur (Jawetz, Melnick, renal abnormalities are more experience a symptomatic uri- & Adelberg, 1995). likely to suffer from true mixed nary tract infection at some time The risk of suffering from a infections. Frequently, the infect- in their life, with a prevalence of UTI is dependent on age, underly- ing bacteria may be antibiotic- between 1% to 3% among non- ing renal impairments, and most resistant due to repeated antimi- pregnant woman. Sexual activity importantly gender (Hawkey & crobial therapy (Murray, 1998). and use of spermicides also Lewis, 2003). Bacteriuria is signif- With nosocomial or hospital- increase the risk for UTIs in icantly more prevalent in the acquired infections, the actual young women (Sanford, 1975). In female population, and it increas- hospital environment is an adult men, the prevalence rates es with age in both sexes until the important determinant of the are low at around 0.1% until the gender ratio of infection becomes nature of the infecting organisms. later years in life, when it steadi- nearly equal in the elderly. Proteus, Klebsiella, Enterobacter, ly increases. Bacteriuria among Pseudomonas, staphylococci, adult men, as in childhood, is Epidemiology of Infecting and enterococci are more often frequently associated with uri- Organisms isolated from inpatients, as com- nary anatomic abnormalities There are differences between pared to the preponderance of E. (Kaye, 1972). the infecting bacterial species in a coli in an outpatient population In the elderly patient, the patient suffering from an initial (Turck & Stamm, 1970). female/male UTI ratio becomes acute episode of urinary tract The incidence of UTI spans less significant. For patients of infection as compared to those all age groups starting with both genders over the age of 65, with frequent recurring infec- neonates. In infants up to 6 the prevalence increases substan- tions. Escherichia coli are by far months, the infection rate is tially; at least 10% of men and the most frequent infecting bacte- about 2 cases per 1,000 live 20% of women over 65 will suf- ria in acute UTIs. E. coli causes births and is more prevalent in fer from a UTI (Kaye, 1980). 80% to 90% of acute uncompli- boys (Boineau & Lewy, 1975). There are several factors that cated bacterial UTIs in young During the preschool years, the increase the prevalence of UTIs women (Hawkey & Lewis, 2003). incidence of UTI becomes more in the elderly. This includes Other enteric bacteria and prevalent in females. In a study obstructive uropathy from the Staphylococcus saprophyticus of this age group, the prevalence prostate and the weakening of cause most of the other culture- was 4.5% for girls and less than the bactericidal activity of prosta- positive infections in this patient 0.5% for boys. The infections tic secretions in men. In women, group. Some young women with that occur in preschool boys are the increases can be partially acute dysuria, suggesting cystitis, often associated with congenital attributed to soiling of the per- have negative urine cultures for renal abnormalities (Boineau & ineum from fecal incontinence bacteria. In these patients, selec- Lewy, 1975; Randolph & and poor bladder emptying due tive cultures for more difficult-to- Greenield, 1964). to prolapse (Romano & Kaye, culture organisms, such as In a study of children of 1981). Catheterization also dra- Neisseria gonorrhoea and school age, bacteriuria was com- matically increases the risks of Chlamydia trachomatis, and mon, frequently asymptomatic, developing an upper UTI in the evaluation for herpes simplex and commonly recurred in the elderly. Even with optimal care viral infection should be investi- female population. The preva- and closed drainage systems, gated (Jawetz et al., 1995). lence for girls was reported as 50% of catheterized patients will In recurrent or chronic UTIs, 1.2%, with 5% experiencing a become infected after 4 to 5 days, the frequency of infection caused UTI during their time at school. 75% after 7 to 9 days, and 100% by Proteus spp., Pseudomonas Among boys, bacteriuria was after 2 weeks (Hawkey & Lewis, spp., Klebsiella spp., Enterobacter reported as being very low, at 2003). spp., and by enterococci and approximately 0.03% in the staphylococci is significant. group studied (Kunin, 1970; Role of the Clinical Chronic and recurrent UTIs are 1976). Laboratory generally due to the presence of Once adulthood is reached, The aim of clinical laborato- structural abnormalities such as the prevalence of bacteriuria ry diagnostic procedures should obstructive uropathy, neurogenic steadily increases in the female be the detection of the abnormal bladder, and congenital renal population. At least 10% to 20% presence of bacteria within the

UROLOGIC NURSING / June 2006 / Volume 26 Number 3 199 urinary tract together with evi- from around the urethra. The Urine Microscopy dence of inflammation. The mid-stream section of the urine Microscopy can be a useful detection and identification of should then be collected. tool in the diagnosis of bacteri- bacteria is normally carried out Reliability of a positive result uria and is often the first step in using routine culture methods, from a clean voided MSU in laboratory diagnosis of a UTI. and evidence of inflammation females is 80% after one sample, Microscopy is used to identify can be ascertained by standard 90% from two samples, and the presence of leucocytes (white light microscopy. For accurate 100% from three consecutive blood cells), erythrocytes (red diagnosis, it is essential that the samples. Only one sample is blood cells), urinary casts, criteria for specimen collection required in males, as urethral epithelial cells, bacteria, and and transport are adhered. contamination is much less like- other cellular components in Incorrectly taken specimens can ly (Hawkey & Lewis, 2003). The urine. Microscopy of urine may lead to bacterial contamination, second type of collection is a be carried out in two methods. and delays in transport can result catheter specimen of urine and The first method is by using in bacterial multiplication, this may be required from the unspun urine. The second which in turn can lead to poten- elderly and patients with neuro- method is by performing a cen- tial misdiagnosis (Hindman, genic bladders, who may have trifugation step first and then Tronic, & Bartlett, 1976). poor control over bladder empty- performing microscopy on the Laboratory examination of ing. Finally, to resolve diagnostic sediment. There are significant the urine is normally requested problems, urine can be aspirated advantages in using uncen- when signs or symptoms point to directly from the full bladder by trifuged urine because it allows a UTI, renal insufficiency, or means of a suprapubic aspirate. for direct quantification of cellu- hypertension. It is recommended This is the best sample to be col- lar components and bacteria. for patients with suspected sys- lected from babies and young There is also the difficulty in temic infection or those present- children. standardizing centrifugation ing with pyrexia of unknown ori- techniques to allow for quantifi- gin. It is also suggested for Specimen Transport cation. The centrifugation step women in the first trimester of Once a suitable urine sample can also make a routine urine pregnancy (Jawetz et al., 1995). has been collected, it is impor- microscopy a very time-consum- The ability of a clinical microbi- tant that there is a minimal delay ing procedure. Despite this, cen- ology laboratory to confirm a sus- between voiding and bacterial trifugation is continued in some pected UTI depends on a number analysis in the laboratory. Delay laboratories to help with the of factors including specimen in transportation and storage at detection of urinary casts whose collection and transport, use of room temperature may result in presence may indicate renal dys- bacterial preservatives, and after the multiplication of many bacte- function (Hawkey & Lewis, arrival in the laboratory, depend- ria present in the sample and this 2003). ing on microscopy and culture. will not reflect a true clinical pic- Significant pyuria has been ture. Wheldon and Slack (1977) defined as 5 to 10 leukocytes per Specimen Collection attempted to define the maxi- high power field, which is the Rapid transport and culture mum time of lapse before a cul- equivalent of 50 to 100 cells per of the sample are essential for ture would give false positive ml (Brumfitt, 1965). Microscopic reliable laboratory diagnosis. In results due to multiplication of findings should be interpreted the collection of urine, the main contaminant bacteria. Their find- with caution as leukocytes will problem is contamination of the ings indicated that a delay of up be present in all forms of inflam- sample by commensal flora from to 4 hours is likely to give a true mation. In females, leukocytes the vagina or perineum, coming indication of the presence or may in fact have originated from into contact with the urethra. absence of infection. Delays inflammation in the vagina. The main problem with com- greater than 4 hours caused the Differences in urine flow can mensal contamination is that interpretation of a heavy growth affect cell numbers. Leukocytes they can be the same organisms of bacteria to become progres- can disintegrate in alkaline urine, that cause ordinary UTIs. sively more unreliable, even in thus infections caused by Proteus There are three main meth- pure culture. sp. combined with a delay in ods of collecting a urine sample Where delay is unavoidable, transportation can result in no that are used in routine bacterio- refrigeration at 39.2o F (4o C) is a apparent pyuria. Significant logic testing. First, the mid- satisfactory means of maintain- pyuria can continue to be present stream urine (MSU) is the most ing urinary bacterial preservation several days after successful appropriate sample for most rou- for culture. Analysis of bacterial antibiotic treatment. tine laboratory testing. In the col- colony counts before and after It should be emphasized that lection of a MSU specimen, as overnight refrigeration indicated although the finding of pyuria is the name suggests, the first pas- satisfactory results in quantita- nonspecific, using the stricter sage of urine is not collected. tive bacteriologic evaluation definition of >10 leukocytes per This should remove commensals (Lewis & Alexander, 1980). ml (by counting chamber), the

200 UROLOGIC NURSING / June 2006 / Volume 26 Number 3 vast majority of patients with An even simpler visual agar pour plate techniques (Kaye, either symptomatic or asympto- method has been used to predict 1972). Although accurate, both of matic bacteriuria will have UTIs. The visual inspection of these methods are time consum- pyuria (Boscia, Abrutyn, Levi- urines and their division into cat- ing and therefore not best suited son, Pitsakis, & Kaye, 1989). egories of clear and cloudy has a for routine work in a busy clini- Other cellular components high negative predictive value of cal laboratory environment. present in urine may also be of 97.3%. Although calling urine Other quantitative methods diagnostic value. Microscopic “clear” on visual inspection can- include the streak plate method and occasionally gross hematuria not completely eliminate the which necessitates the use of will be present in patients with a possibility of infection, the find- standardized bacteriologic loops. UTI. However, the microscopic ing of clear urine should be con- Calibrated loops serve as a sim- presence of red blood cells may sidered a reasonable and relative- ple and inexpensive method of be indicative of renal abnormali- ly effective bedside screen for the delivering a fixed volume of ties, such as calculi, tumor, vas- presence of a UTI (Bulloch, urine to an . After incu- culitis, glomerulonephritis, or 2000). bation, the total number of organ- renal tuberculosis. The presence isms can be calculated by multi- of large numbers of epithelial Culture for Urinary plying colony count by the vol- cells may be indicative of ure- Pathogens ume of urine used. The tech- thral contamination. The pres- The next step in the laborato- nique can be further refined by ence of white cell casts with and ry analysis is to recover or the use of deferential media to without infection presents strong exclude likely uropathogens allow rapid identification of evidence for pyelonephritis. from a urinary sample in a time- organisms and to help identifica- The microscopic examina- ly manner. To achieve this, tion of mixed cultures. tion of urine for bacteria is one of appropriate media, incubation The filter paper method is a the most significant tests for the times, and conditions must be semi-quantitative culture method presumptive diagnosis of a UTI. adhered. Even the most carefully ideal for screening large numbers Smaller numbers of bacteria can collected urine specimens may of urine samples. This technique be detected in a Gram-stained suffer from some form of urethral involves the absorption of a given specimen and the sensitivity can contamination. Ideally, a urine volume of urine onto a piece of be increased by a centrifugation sample will benefit from being sterile filter paper, which is then step. Presence of at least one bac- cultured by a quantitative streaked across an agar plate. The terium per oil-immersion field in method. This is to allow the clin- use of filter paper of standardized a mid-stream, clean-catch, Gram- ical laboratory to distinguish porosity allows each strip to stained, uncentrifuged urine cor- between a legitimate UTI and deliver the same quantity of urine. relates with 105 bacteria/ml. As contamination. After overnight incubation, more this corresponds to what is Kass (1957) helped to define than 25 colonies on the plate is regarded as significant bacteri- the criteria for significant bacteri- equivalent to more than 105 bacte- uria, it represents a relatively uria. It was suggested that a ria per ml of urine (Leigh & reliable method of detecting sig- count of 100,000 colony-forming Williams, 1964). nificant numbers of organisms units (cfu’s) per ml or greater of a It is important that the cho- (Murray, 1998). single species of micro-organism sen solid media (agar plates) In larger clinical laboratories, in an MSU was almost invariably used for urinary culture are able the centrifugation of all urine indicative of bladder bacteriuria. to support the growth of all samples for microscopy may be This was realized by comparing known urinary pathogens and considered too time consuming. colony counts of E. coli in cul- also that of contaminating com- The microscopic examination of tures of bladder urine collected mensal bacteria. Ideally, the unspun urine for significant by catheter with those of MSUs identification of lactose fermen- pyuria and bacteriuria can be from the same woman. However, tation should also be demonstra- performed using a disposable some studies have suggested that ble by a color change in the agar; slide with counting chambers. too strong an emphasis should more importantly Proteus spp. The counting chamber method not be placed on these criteria. should be inhibited from produc- can detect significant bacteriuria Indeed, in one study some symp- ing the swarming cell type. (sensitivity 94%; specificity tomatic women with counts of A standard blood-containing 88%), and when combined with 10,000 (104) cfu/ml, and some- agar and MacConkey agar can be significant pyuria can have both times less, had clinical bladder used successfully in combina- a sensitivity and negative predic- infection (Stamm et al., 1982). tion. The blood agar allows the tive value as high as 97%. The Despite this, bacteriuria is usual- growth of all urinary pathogens counting chamber represents a ly characterized by counts well and commensals of the genital simple, sensitive, and cost-effec- in excess of 1,000,000 (106) tract but suffers from a lack of tive method for the diagnosis of a cfu/ml. differentiation between lactose UTI by microscopy (Hiraoka et The most accurate methods fermenters and non-fermenters, al., 1993). to quantify urinary bacteria and no inhibition of swarming include the serial tube and the

UROLOGIC NURSING / June 2006 / Volume 26 Number 3 201 The presence of particular species is Antimicrobial Sensitivity Testing important for hospital infection control The testing of antimicrobial and should be monitored. activity in vitro is primarily per- formed to ascertain the sensitivi- ty of an infecting organism to Proteus spp. MacConkey medi- Full identification may be neces- known concentrations of antimi- um is a selective agar allowing sary for infection control at the crobial agents. In most clinical for differentiation of lactose fer- ward level. It can also help in laboratories, the method of menters and prevents swarming establishing whether repeated choice is the disk diffusion by Proteus spp., but is inhibitory infections are due to relapse, re- method. An antibiotic-impregnat- to many Gram-positive organ- infection, or cross-infection. The ed filter paper disk containing isms. presence of particular species is measured quantities of a particular A medium which fulfills all important for hospital infection antimicrobial agent is placed on a of the above requirements for control and should be monitored. solid medium, generally an appro- urine culture in a single medium Of particular importance are priate sensitivity testing agar that is CLED (Cysteine Lactose multi-antibiotic resistant organ- has been heavily seeded with the Electrolyte-Deficient) agar. It is isms, such as methicillin resistant organism. After overnight incuba- widely used in many clinical lab- Staphylococcus aureus (MRSA), tion, the diameter of the clear oratories as the standard urinary vancomycin resistant enterococci zone of inhibition surrounding agar. The indicator used (VRE), and Gram-negative ex- the diffused disk equates to the in CLED agar is bromothymol tended spectrum-lactamase pro- inhibitory power of the test agent blue which will indicate lactose ducers (ESBLs). against the particular organism. fermentation. Laboratories can identify uri- This method is subject to many Additionally, there are now nary isolates into broad groups by chemical and physical factors; several chromogenic agars avail- using simple identification proce- nevertheless, standardization of able for urinary culture. The aim dures. These groups can be conditions permits a quantitative of chromogenic agar is to aid in broadly defined such as coliforms assay of the sensitivity of an the primary identification of uri- (Gram-negative, oxidase-nega- organism, when used in conjunc- nary pathogens through color tive, lactose fermenters) and tion with established reference changes. In a recent study, the Pseudomonas spp. (Gram-nega- standards and procedures. performance of a chromogenic tive, oxidase positive, non-lactose The practice of performing agar (oxoid chromogenic urinary fermenters). Candida spp. can be direct antimicrobial susceptibili- tract infection medium; CUTI) identified by Gram-stain or wet ty testing (DST) of urine speci- was evaluated against CLED agar, preparation viewing. Staphylo- mens possesses many advantages in terms of isolation rates and cocci can be broadly grouped into including next-day reporting of presumptive identification of iso- S. aureus and -negative antimicrobial sensitivities. The lates when compared with com- staphylococci (CNS) based on the method still remains controver- mercial identification systems. coagulase reaction. However, it is sial due to concerns regarding its The CUTI medium improved the necessary to differentiate Staphy- accuracy. In a study by Oakes, detection of mixed cultures, lococcus saprophyticus from Badger, and Grove (1994), the DST thereby increasing the reliability other CNS, by means of novo- method was compared with a stan- in the reporting of significant iso- biocin-testing, as S. saprophyti- dardized . After lates, when compared with CLED cus is a frequent cause of lower 1,106 urine samples containing 105 agar. If supplemented with sim- urinary tract infection, particular- organisms in pure culture were ple bench tests, it was capable of ly in females of child-bearing age. compared using ampicillin, co- successfully speciating 86.8% of Significant streptococcal and amoxyclav, cephalothin, gentam- Gram-negative isolates (Fallon et enterococcal isolates can be iden- icin, norfloxacin, and trimetho- al., 2002). tified by means of a commercial prim, there was 94.3% agreement Lancefield Grouping kit and on the between the two methods. Identifying Urinary basis of their bile aesculin reaction. Another study compared DST Pathogens After demonstration of signif- against standardized disk diffu- Ideally all significant cultures icant urinary infection and iden- sion susceptibility testing using should be fully identified to the tification of the cause, the next 25 traditional and contemporary species level, but this can be role of the laboratory is to provide antimicrobial agents. Of the impractical or considered unnec- antimicrobial sensitivity patterns. 2,983 individual comparisons essary in a busy diagnostic micro- This information is important for between the two methods, there biology laboratory. Some labora- the clinician as sensitivity pat- was 95.5% agreement (Johnson, tories may deem it necessary to terns of isolates will identify the Tiu, & Stamm, 1995). identify all organisms, subsec- antibiotics needed to clinically tions of organisms, or species treat the infection. Conclusions from specific patients or wards. Urinary tract infections con-

202 UROLOGIC NURSING / June 2006 / Volume 26 Number 3 tinue to remain a major cause of Jawetz, E., Melnick, J.L., & Adelberg, E.A. infection, both in the community (1995). (20th ed.). London: Prentice Hall and hospital, with an associated International. high degree of morbidity. The clin- Johnson, J.R., Tiu, F.S., & Stamm, W.E. ical microbiology laboratory plays (1995). Direct antimicrobial suscep- a major role in the laboratory diag- tibility testing for acute urinary tract nosis of the numbers of infecting infections in women. Journal of Clinical Microbiology, 33, 2316- pathogens, the identification and 2323. characterization of these organ- Kass, E.H. (1957). Bacteriuria and the isms, as well as helping to deter- diagnosis of infections of the urinary mine the antibiotic sensitivity of tract; with observations on the use of methionine as a urinary antiseptic. these pathogens to a range of American Medical Association antibiotics presently used in the Archives of Internal Medicine, 100, management of such infections. 709-714. Current technological develop- Kaye, D. (Ed.). (1972). Diagnosis of uri- ments in automation, imaging, nary tract infection by culture. In Urinary tract infections and its man- and molecular methods will allow agement (pp. 28-42). St. Louis: microbiology results to be Mosby. obtained more quickly, thus allow- Kaye, D. (1980). Urinary tract infection in ing improved management of the elderly. Bulletin of the New York Academy of Medicine, 56, 209-220. patients with such infections. • Kunin, C.M. (1970). The natural history of recurrent bacteriuria in school girls. References New England Journal of Medicine, Boineau, F.G., & Lewy, J.E. (1975). 282, 1443-1448. Urinary tract infection in children: Kunin, C.M. (1976). Urinary tract infec- An overview. Pediatric Annals, 4, tions in children. Hospital 515-526. Practitioner, 11, 91-98. Boscia, J.A., Abrutyn, E., Levison, M.E., Leigh, D.A., & Williams, J.D. (1964). Pitsakis, P.G., & Kaye, D. (1989). Method for the detection of signifi- Correlation of pyuria and bacteriuria cant bacteriuria in large groups of in elderly ambulatory women. patients. Journal of Clinical Annals of Internal Medicine, 110, Pathology, 17, 498-503. 404-405. Lewis, J.F., & Alexander, J.J. (1980). Brumfitt, W. (1965). Urinary cell counts Overnight refrigeration of urine and their value. Journal of Clinical specimens for culture. Southern Pathology, 18, 550-555. Medical Journal, 73, 351-352. Bulloch, B. (2000). Can urine clarity Murray, P.R. (Ed.). (1998). Urinary tract exclude the diagnosis of urinary infections. In Manual of clinical tract infection? Pediatrics, 106, E60. microbiology (7th ed.) (pp. 581-611). Dulczak, S., & Kirk, J. (2005). Overview of Washington, DC: ASM Press. the evaluation, diagnosis, and man- Oakes, A.R., Badger, R., & Grove, D.I. agement of urinary tract infections (1994). Comparison of direct and in infants and children. Urologic standardized testing of infecting Nursing, 25, 185-191. urine for antimicrobial susceptibili- Fallon, D., Andrews, N., Frodsham, D., ties by disk diffusion. Journal of Gee, B., Howe, S., Iliffe, A., et al. Clinical Microbiology, 32, 40-45. (2002). A comparison of the perfor- Randolph, M.F., & Greenfield, M. (1964). mance of cysteine lactose electrolyte The incidence of asymptomatic bac- deficient (CLED) agar with oxoid teriuria and pyuria in infancy. chromogenic urinary tract infection Journal of Pediatrics, 65, 57-66. (CUTI) medium for the isolation and Romano, J.M., & Kaye, D. (1981). UTI in presumptive identification of organ- the elderly: Common yet atypical. isms from urine. Journal of Clinical Geriatrics, 36, 113-115. Pathology, 55, 524-529. Sanford, J.P. (1975). Urinary tract symp- Hawkey, P., & Lewis, D.A. (Eds.). (2003). toms and infection. Annual Reviews Bacteriology of urine. In Medical in Medicine, 26, 485-98. bacteriology. A practical approach Stamm, W.E., Counts, G.W., Running, (2nd ed.) (pp. 1-19). London: Oxford K.R., Fihn, S., Turck, M., & Holmes, University Press. K.K. (1982). Diagnosis of coliform Hindman, R., Tronic, B., & Bartlett, R. infection in acutely dysuric women. (1976). Effect of delay on culture of New England Journal of Medicine, urine. Journal of Clinical 307, 463-468. Microbiology, 4, 102-103. Turck, M., & Stamm, W.E. (1970). Hiraoka, M., Hida, Y., Tuchida, S., Nosocomial infection of the urinary Tsukahara, H., Yamashita, M., tract. American Journal of Medicine, Kuroda, M., & Sudo, M. (1993). 70, 651-654. Diagnosis of urinary tract infection by Wheldon, D., & Slack, M. (1977). urine microscopy using a disposable Multiplication of contaminant bacte- counting chamber. Scandinavian ria in urine and interpretation of Journal of Clinical Laboratory delayed culture. Journal of Clinical Investigation, 53, 705-709. Pathology, 30, 615-619.

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