HOSPITAL-ACQUIRED URINARY TRACT INFECTIONS ASSOCIATED WITH THE INDWELLING CATHETER

INFECTIONS IN UROLOGY

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HOSPITAL-ACQUIRED URINARY TRACT INFECTIONS ASSOCIATED WITH THE INDWELLING CATHETER John Sedor, MS and S. Grant Mulholland, MD

The indwelling urethral urinary catheter is used in as many as 25% of patients admitted to hospitals in the United States.23These catheters are commonly placed in association with surgical procedures and anesthesia for accurate measurements of urinary output, to relieve urinary retention or incontinence, to improve nursing care, to protect against skin problems in incontinent patients, to facilitate urinary flow in neurologic patients who are not candidates for other forms of drainage, and for irrigation of the bladder or instillation of drugs. Fortunately, these catheters are usually left indwelling for a short period of time. The urethral catheter is the most prevalent cause of nosocomial infections and gram-negative bacteremia. The duration of catheterization is directly related to the development of bacteriuria.33 The urinary tract accounts for more than 40% of the total number of nosocomial infections affecting an estimated 800,000 patients per year.h,22, 44, 45 Most nosocomial infections associated with the urinary tract follow instrumentation, usually with the catheter. Many techniques have been used in an attempt to reduce the incidence of infection. The most important factor in the reduction of urinary tract infections and sepsis is a reduction in use of the catheter. The clinician must be certain that the catheter inserted is abso-

lutely necessary and should attempt to have the catheter removed as soon as possible. The infections that arise with catheterization are caused by bacteria from the patient’s body or colonic flora and by bacteria found in the hospital setting. Bacteria can easily invade the lower urinary tract along the external surface of the catheter or by ascending through the urine in the lumen of the catheter. THE BATTLE WITH THE INDWELLING CATHETER

”Catheter fever” was first described in the literature in the late 1800s’ and has been referred to in case studies for decades. Contemporary interest in urinary catheter infection was greatly stimulated by Beeson in 1958.’ Prior to this report, there was limited interest in reducing infection and subsequent morbidity by using better sterile technique and closed systems. Study of the mechanisms of bacterial entry into the bladder began, and more thorough epidemiologic data were obtained. It became apparent that if a catheter was absolutely necessary, short-term, sterile, closed drainage systems were ideal. A discussion of premodern solutions to the problem is beyond the scope of this article, but closed

From the Department of Urology, Jefferson Medical College of Thomas Jefferson University, Philadelphia, Pennsylvania

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systems were described, with some clinicians advocating antibacterial irrigation. Rigid glass collecting bottles made closed systems cumbersome. The closed system was easily violated, and bacteria entered to flourish and ascend to the bladder. The closed system was perfected with the advent of plastic receptacles, tubing, and valves. Innovative design resulted in new systems throughout the 1960s, 1970s, and 1980~.'~, 33 Because further improvements in closed system technologies seem elusive, current research efforts have been directed at attacking or preventing bacterial entry or discouraging their colonization of the urinary tract. Antibiotic and antiseptic irrigation, meatal cleansing, and urethral antimicrobial application have not had a significant impact on reducing infection. The introduction of antimicrobial or antiadherent substances into or onto the catheter may have some influence in certain patients. A solution to the problem of infection is important not only because of morbidity but also economics.

teriuria per day should encourage the clinician to remove the catheter in 4 days or lessz3 All catheters should be introduced using impeccably sterile techniques. Closed systems are used extensively, and the systems should not be entered unless absolutely necessary. Risk factors other than the duration of catheterization include contamination of the drainage bag, diabetes mellitus, a female patient, antibiotic usage, the presence of a urinometer, frequent measurement of urinary output, a compromised status of renal function, and poor technique. Uropathogens in or around the urinary tract are more efficient at creating bacteriuria than are normal flora.19

PATHOGENESIS

Bacteriuria is a common consequence of indwelling urinary catheter usage. Because most catheter-related urinary tract infections are asymptomatic, bacteriuria is diagnostic of these infections. The duration of catheterization is the most important risk factor for the CATHETERIZATION-INCIDENCE OF development of bacteriuria in catheterized INFECTION AND EPIDEMIOLOGY patients.I8 Other important risk factors include microbial colonization of the periurThe leading risk factor for the development ethral area or the urine drainage bag, and the route of entry is ascending via the outside of an infection associated with an indwelling catheter is the duration of catheteri~ation.~~surface of the catheter or the luminal surface, 50 Differences in the route of respe~tively.'~, Numerous other factors are involved. The entry are apparently gender-related. In ferisk of infection with a single catheterization males, the majority of cases are caused by the is 1%to 2°/0.63A small number of organisms periurethral route with rectal flora; in males, may be introduced into the bladder that are efficiently eliminated by voiding. The risk of the predominant route is intraluminal, suggesting an exogenous source.8,6o In addition, infection is increased in patients who are in microorganisms that are present on the meurinary retention, in female patients, in paatus or distal urethra can be transferred ditients catheterized peripartum, in men with rectly into the bladder during the insertion of prostatic obstruction, and in diabetic, debilithe catheter. tated, and elderly patients.32 Unfortunately, Bacteriuria that occurs during short-term most patients do not receive a single cathetercatheterization is usually caused by a single ization in the hospital but have an indwelling organism, although it may be polymicrobial. catheter left in place for days. In patients with The most commonly isolated pathogen is an open drainage system, bacteriuria occurs Escherichia coli. Other organisms include enrapidly within 2 to 3 days. With closed drainterococci, Pseudomonas, Klebsiella, Enterobacter, age systems, one-half of patients will be bactStaphylococcus epidermidis, Staphylococcus eriuric within 10 days to 2 weeks; most paaureus, and S e r ~ a t i a66. ~Most ~ ~ of the infecting tients will be bacteriuric by the end of 30 organisms are part of the endogenous intestidays." nal flora, but contamination can also originate Most catheters placed in the hospital setfrom exogenous sources, such as other pating are used for short periods of time, and tients, hospital personnel, contaminated soluon removal of the catheter, the patient will tions, or nonsterile instruments. Bacterial isoefficiently clear bacteria from the urinary tract lates that might suggest an exogenous source or with relatively short courses of antimicroinclude staphylococci, Serratia marcescens, bial therapy. The 3% to 10% incidence of bac-

HOSPITAL-ACQUIRED URINARY TRACT INFECTIONS WITH THE INDWELLING CATHETER

Burkholderia (Pseudomonas) cepacia, and Stenotrophomonas rnalt~philia.~~, 5y, 61 Long-term catheterization (>30 days) is common in long-term residents of chronic care facilities. The incidence of bacteriuria in long-term catheterized patients is 8% to 10% per day, and the prevalence of bacteriuria is 67 Bacteriuria nearly 100°/~in this population.66* in these patients tends to be of a polymicrobh7 Common uropathogens include ial nature.32, E. coli, Pseudomonas aeruginosa, Proteus mirabilis, and less commonly, Providencia stuartii, Morganella morganii, and Acinetobacter bau~ n a n n i .37,~ 42, ~ , 50 Once established, many of these strains are persistent, which is a possible consequence of their tenacious adherence 66, b7 As is true for a to the catheter majority of nosocomial pathogens, many of these organisms possess multiple antibiotic resistances. These polymicrobial infections are difficult to treat as long as the catheter remains in place because, in addition to providing access to the bladder, the catheter becomes a reservoir for the pathogens.56 In the bacteriuric urinary tract, there are two populations of bacteria: (1) planktonic growth, those bacteria growing in suspension Current in the urine and (2) biofilm research has focused on the attachment and colonization of the catheter surface and relationships to catheter-related urinary tract infections. Scanning electron microscopy confirms layers of organisms, termed biofilms, on infected indwelling cathetersj6,52 Biofilm formation is a process that progresses in a welldefined sequence. Bacteria attach to the catheter surface, grow, and secrete an extracellular polysaccharide matrix of bacteria glycocalices. Host urinary protein and salts complex with this matrix, leading to encrustation of the catheter lumen. Microorganisms embedded in a biofilm are protected from antibiotics, antiseptics, and host defense mechanisms. Microbes in biofilms form a microenvironment that is favorable for the formation of encrustations on the inner surface of the catheter, which can lead to obstruction to urine flow.', 21, 27 Encrustation results from struvite (magnesium ammonium sulfate) and apatite (calcium phosphate) formation and deposition. Embedded colonies of urease-producing bacteria (Protease, Providencia, Morganella spp) provide the foci for crystal formation. Anionic polysaccharide matrix attracts Ca' + and Mg' from the urine. Bacterial urease increases urine pH by the conversion of urea to ammonia. Crystals precipitate and aggregate +

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with matrix glycoprotein and adhere to the catheter surface. This mechanism is also responsible for the formation of infection stones. In addition to obstruction, encrustations on the balloon tip can traumatize the bladder on catheter withdrawal. Virulence factors such as P fimbriae associated with community-acquired urinary tract infections do not seem to be prevalent in strains that cause bacteremic catheter-related urinary tract infection^?^, 30 and host defense factors, which are compromised, may be more important in their pathogenesis. Studies suggest an inherent difference in bacterial adhesion to uroepithelial cells in catheterized pat i e n t ~ Better .~ understanding of the complex interactions between uroepithelium and microbial pathogenesis may lead to novel approaches to the prevention of catheter-related urinary tract infections and subsequent systemic dissemination of the uropathogen.

MORBIDITY OF CATHETERIZATION Short-term catheterization usually results in bacteriuria that rapidly clears after removal of the catheter, especially with antibiotic treatment for short periods of time. Febrile episodes are more commonly associated with long-term catheterization, but the incidence b9 The most comof these episodes is low.68* mon cause of fever is pyelonephritis, but other causes are local complications associated with the urinary catheter, especially in the male. These complications include urethritis, prostatitis, and epididymitis. When fever develops in a catheterized patient, it is extremely important to rule out local sources. Discovering a local source may alter the course of treatment. With these types of infections, the clinician may want to remove the urethral catheter and initiate a suprapubic drainage system. Febrile episodes may progress or may resolve without treatment. The possible progression, especially in debilitated or high-risk patients, would be the development of bacteremia, sepsis, and death. Platt and co-workersS1demonstrated that patients with catheter-associated urinary tract infections had a fatality rate nearly three-fold higher than noninfected patients. The reason for this high risk was thought to be progression to bacteremia and sepsis. The importance of unrecognized bacteremia and septicemia in hospitalized patients with gram-negative rod bacteriuria and fever was studied by Van

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Deventer and colleagues.h5One-half of these patients were catheterized. Positive blood cultures and endotoxemia were usually found in patients who had clinically diagnosed sepsis. Of the patients with fever alone, 44% had positive blood cultures. Therefore unrecognized bacteremia and sepsis are prevalent with gram-negative rod bacteriuria. Understanding of even the simplest and most common sequelae of catheterization remains limited. The previous discussion implies that fever alone may be serious, and that occult systemic infection may not be uncommon. There are probably a large number of patients who have bacteriuria that is transient and asymptomatic. These patients who have a low incidence of sequelae and morbidity can clear the bacteriuria easily on removal of the catheter and are probably not actually infected. Other patients have infection yet are asymptomatic. This group would seem to be more likely to have a higher incidence of morbidity. Concern must be highest for the group with fever who must be treated aggressively because of the significant risk for serious morbidity. The characterization of patients into each group is not predictable, and clinicians should strive to identify these patients better before serious sequelae. Prevention of morbidity is extremely important. The obvious approach to this problem is to eliminate use of the catheter as much as possible and to place it, when necessary, for shorter periods of time. After the catheter has been inserted under ideal conditions, a common question that is asked is whether antimicrobial agents should be started to ”cover the catheter.” Two large categorizations of bacteriuria are associated with the catheter-symptomatic and asymptomatic. Current knowledge dictates that asymptomatic bacteriuria in both long- and shortterm catheterization need not be treated while the catheter is in place. The prophylactic use of antimicrobials beginning at the introduction of the catheter probably creates a more resistant flora within the hospital setting. Controversy continues regarding antimicrobial prophylaxis in patients undergoing transurethral surgery. The antimicrobial treatment of these patients during and after instrumentation will most likely reduce the morbidity of bacteriuria and the development of symptomatic urinary tract infection. Patients who are having protheses inserted clearly need antimicrobial protection. Other patients at high risk include those

who are immunosuppressed, recipients of organ transplants, or pregnant. Occasionally, pathogenic organisms will become a problem within the hospital, and catheter-related infections will become prevalent. In these instances, it may be necessary to protect patients from infection with these organisms, especially in a specific area of the hospital. Generally, after the catheter is removed, the urinary tract will clear bacteria spontaneously. To increase the rate of clearance and possibly reduce symptoms, a short course of antimicrobial therapy may be advisable. PREVENTION OF CATHETERRELATED URINARY TRACT INFECTION Because of the hazards associated with use of the indwelling urinary catheter, an obvious preventive measure is the avoidance of catheterization. The decision to place an indwelling urinary catheter should never be made arbitrarily. Indwelling catheters should never be used to collect timed urine specimens, for medical personnel convenience, or merely as a routine aspect of postoperative care if the patient can void spontane~usly.~~ Prudent infection control practices dictate limited use of urinary catheters to carefully selected patients, therefore minimizing the population at risk for nosocomial urinary tract infection. If it is not possible to avoid the use of the catheter, it is of utmost importance that the catheter be removed as promptly as possible. With a single catheterization, the infection rate is low, approximately l%.63 In patients with an indwelling catheter in place for less than 7 days, the rate of infection is 10% to 40%, whereas in long-term catheterization (>28 days), prevalence approaches 100%.lR, 27 Good Catheter Hygiene

Although not all catheter-related urinary tract infections can be prevented, the infection rate can be minimized by promoting good catheter hygiene.32,72 Good catheter care starts with the procedure of catheter insertion, taking steps to avoid the introduction of microorganisms into the bladder. Catheters should be inserted aseptically using sterile equipment. Gloves should be worn, the patient should be draped, and the meatal surface cleansed using an antiseptic solution. To min-

HOSPITAL-ACQUIRED URINARY TRACT INFECTIONS WITH THE INDWELLING CATHETER

imize urethral trauma, the tip should be lubricated, and the smallest possible catheter size should be used. After insertion, the distal end of the catheter should be secured to the thigh in females and to the abdomen in males to minimize catheter movement and subsequent urethral traction.I2 The most important hygienic measure in preventing patient-to-patient transmission of infection is handwashing by health care personnel before and after handling of the catheter.h2As many as 15% of nosocomial urinary tract infections occur in clusters, a direct result of cross-infection.4,s5 Outbreaks of catheter-related bacteriuria can be prevented by good catheter hygiene, including the use of gloves, handwashing, and segregation of catheterized patients, particularly those already infected.'" Although it seems logical that the prophylactic use of antibiotics would curtail the incidence of catheter-related urinary tract infection, this practice will only postpone the onset of bacteriuria and will not prevent it. In fact, the prophylactic use of antibiotics compounds the problem by leading to the emergence of 47 antibiotic-resistant strains.43* As an adjunct to diligent handwashing, good meatal care may prevent microbes from colonizing the periurethral surface and infecting the bladder. Most studies have shown that the application of an antiseptic to the urethral meatus has little or no effect on the infection rate, although one recent study found povidone-iodine cream to be effective in preventing urinary tract infection.2,5, 28, 38 Notwithstanding, meatal cleansing may decrease irritation and seems to be a reasonable practice. Closed Drainage Systems

A sterile continuous closed catheter system is a universally recommended catheter hygiene principle for infection control. Closed drainage, first introduced in 1928 by Sir Cuthbert Dukes, a pathologist at St. Mark's Hospital in London, did not become standard practice until the 1960s.", 3y For short-term catheterization, closed system drainage effectively reduces the infection rate from 100% to 28%.33 The basic components of a closed system include the catheter, a preconnected collecting tube with attached sampling port, and a vented drainage bag with a spigot for drain-

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ing. Characteristics of a good system are good flow properties, a drainage bag that can be easily emptied, and a minimum number of parts. Numerous modifications to the basic system have been developed, such as air vents, drip chambers, one-way valves, hydrophobic drainage vents, and a povidoneiodine release cartridge on the outlet tube. None of these alterations have proved to be effective, and they result in a needlessly complex system that can easily malfunction.", Ease of use is paramount for acceptance by health care personnel, and these accessories also drive up the cost. Several principal measures maintain the integrity of an aseptically closed The catheter/collecting tube junction should be disinfected when connected. All urine samples should be collected aseptically through the sampling port, wiping with disinfectant before and after sampling. The catheter should be disconnected from the drainage tube to clear blood clots. The entire system should be replaced in instances of obstruction, breaks in aseptic technique, poor flow, odor, disconnection, or leakage. The drainage bag should be kept below the level of the bladder and should be drained at regular intervals. Alternatives to Indwelling Catheters

Alternative methods of urinary drainage are available to the clinician that are useful in selected patient populations. These options apparently have a lower risk for the development of bacteriuria. Suprapubic catheters are used mainly in patients undergoing urologic or gynecologic procedures. These devices should be placed by specialists, limiting their widespread use. The anterior abdominal wall possesses a lower microbial load than the periurethral area, and several studies have shown no increased risk of infection.z5,2 6 , s8 Suprapubic catheters are more convenient for medical personnel and are more comfortable for the patient. Condom catheters are external drainage devices that are used in comatose, incontinent, or neurologically impaired males without outlet obstruction and with intact voiding reflex pathways. The urine in the catheter has a h g h number of bacteria, and the periurethral skin is colonized with uropathogens.lhP24, 41 Despite these factors, condom catheter use,

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which avoids instrumentation of the urethra, results in a lower risk of infection, and several studies suggest lower incidences of bacteriuria.", 49 These devices should be changed daily, accompanied by cleansing of the perineal and periurethral areas. Without meticulous care, complications can occur, including skin maceration, phimosis, and strangulation of the penis. Condom catheters can fall off as a result of erection and can be pulled off by agitated patients. Intermittent catheterization is the practice of insertion and removal of a sterile or clean catheter several times per day at regular intervals. It is useful for certain patients with bladder emptying dysfunction, including spinal cord-injured patients, children with neurogenic bladders, and postoperatively after renal t r a n ~ p l a n t . ~ ~ Modification of Catheter Composition

The clinical use of indwelling catheters is often hindered by the formation of biofilms and consequent encrustation. The thrust of current research and development regarding urinary catheters has been the design of biomedical materials that will prevent bacterial adherence or inhibit bacterial growth, delaying the onset of bacteriuria. Urinary catheters are composed of various materials, including latex, silicone, and latex/silicone combination. Some are manufactured with a hydrophilic coating designed to prevent bacterial adherence. Latex catheters are the least expensive, but irritation and allergic reaction may occur. Silicone catheters offer no advantage over latex, although they are more comfortable and might be a better choice for long-term (>4 days) use. Silicone catheters obstruct less often than latex, Teflon, or silicon-coated latex in patients prone to catheter en~rustation.~~ Strategies to achieve the goal of a bacteriostatic catheter involve coating or impregnation of the catheter material with various compounds. Catheters that are coated with silver oxide may delay bacteriuria during short-term use, but silver alloy-coated cathe35, 54, 57 The treatters seem more effe~tive.'~, ment of catheters with antimicrobial agents may be effective, but, eventually, the surfaces may be colonized with more resistant strains. In vitro studies of catheters impregnated with quinolones or chlorhexidine gluconate show 70 Electric current applied promising results.53*

to catheter surfaces has been effective in in vitro and animal models, but a practical clinical application of this technology awaits further Some of these measures seem effective for the prevention of early onset bacteriuria, but for long-term catheterizations, regularly scheduled catheter replacement is more efficacious and economical. SUMMARY

Indwelling urethral catheters are commonly used in patients admitted to acute care hospitals. Forty percent of nosocomial infections occur in the urinary tract, and greater than 80% of these infections are secondary to an indwelling urethral catheter. Fortunately, the majority of catheters are left indwelling for a short period of time. The duration of catheterization is directly related to the development of bacteriuria, nosocomial infection, and possible bacteremia with sepsis. A relatively low percentage of patients become infected during the first 3 to 5 days if sterile technique and proper maintenance of a closed system are performed. Bacteria may grow in the urine (planktonic) and ascend via the lumen, or bacteria in the biofilm around the outside of the catheter may infect the bladder. Most organisms are from the patient's intestinal flora, but exogenous sources on or near the patient may be involved. The major morbid events associated with the catheter are fever and the possible progression to bacteremia and sepsis. Early recognition of complications and arresting their progression, especially in the high-risk patient, are essential. Current research is directed at developing ways to reduce infection beyond the sterile closed system. References 1. Beeson PB The case against the catheter. Am J Med 24~1-3,1958 2. Britt MR, Burke JP, Miller WA, et al: The non-effectiveness of daily meatal care in the prevention of catheter-associated bacteriuria. In Proceedings of the 16th Interscience Conference on Antimicrobial Agents and Chemotherapy, 1976, p 141 3. Bruce AW, Sira SS, Clark AF, et al: The problem of catheter encrustation. Can Med Assoc J 111:238-241, 1974 4. Bukhari S, Sanderson P, Richardson D, et al: Endemic cross-infection in an acute medical ward. J Hosp Infect 24:261-271, 1993 5. Burke JP, Jacobsen JA, Garibaldi RA, et a 1 Evaluation

HOSPITAL-ACQUIRED URINARY TRACT INFECTIONS WITH THE INDWELLING CATHETER of meatal care with polyantibiotic ointment in prevention of urinary catheter associated bacteriuria. J Urol 129:331-334, 1983 6. Centers for Disease Control: National Nosocomial Infections Study Report. Atlanta, Centers for Disease Control, 1979, pp 2-14 7. Clark A. Remarks on catheter fever. Lancet 2:10751077, 1883 8. Daifuku R, Stamm W: Association of rectal and urethral colonization with urinary tract infection. JAMA 2522028-2030, 1984 9. Daifuku R, Stamm W: Bacterial adherence to uroepithelial cells in catheter-associated urinary tract infection. N Engl J Med 314:1208-1213, 1986 10. Davis C, Shirtliff M, Trieff N, et al: Quantification, qualification and microbial killing efficiencies of antimicrobial chlorine-based substances produced by iontophoresis. Antimicrob Agents Chemother 382768-2774, 1994 11. Davis CP, Shirtliff ME, Scimeca JM, et a 1 In vivo reduction of bacterial population in the urinary tract o f catheterized sheep by iontophoresis. J Urol 154:1948-1953, 1995 12. Desautels RF, Walter CW, Graves RC, et al: Technical advances in the prevention of urinary tract infection. J Urol 87487490, 1962 13. Desautels RF: Aseptic management of catheter drainage. N Engl J Med 263:189-191, 1960 14. Dukes C: Urinary infections after excision of the rectum: Their cause and prevention. Proc R SOCMed 22~1-11, 1928 15. Ehrenkranz NJ, Alfonso BC: Failure of bland soap handwashing to prevent hand transfer of patient bacteria to urethral catheters. Infect Control Hosp Epidemiol 123654662, 1991 16. Fierer J, Ekstron M: An outbreak of Providencia stuartii urinary tract infections: Patients with condom catheters are a reservoir of the bacteria. JAMA 245~1553-1555, 1981 17. Gabriel MM, Mayo MS, May LL, et al: In vitro evaluation of the efficacy of a silver-coated catheter. Curr Microbiol 33:1-5, 1996 18. Garibaldi RA, Burke JP, Dickman ML, et al: Factors predisposing to bacteriuria during indwelling urethral catheterization. N Engl J Med 291:215, 1974 19. Garibaldi RA, Burke JP, Britt MR, et al: Meatal colonization and catheter-associated bacteriuria. N Engl J Med 303:316-318, 1980 20. Garibaldi RA, Brodeni S, Matsumiya S: Infections among patients in nursing homes. Policies, prevalence and problems. N Engl J Med 305731-735, 1981 21. Getliffe KA, Mulhall AB: The encrustation of indwelling catheters. Br J Urol67337-341,1991 22. Haley R, Culver D, White J, et al: The nationwide nosocomial infection rate: A new need for vital statistics. Am J Epidemiol 121:159-167, 1985 23. Haley RW, Hooton TM, Culver DH, et al: Nosocomial infection in US hospitals, 197.51976: Estimated frequency by selected characteristics of patients. Am J Med 70:947-959, 1981 24. Hirsh DD, Fainstein V, Musher DM: Do condom catheter collecting systems cause urinary tract infection? JAMA 242340-341, 1979 25. Hodgkinson CP, Hodari AA: Trocar suprapubic cystomy for postoperative bladder drainage in the female. J Obstet Gynecol 96773-783, 1966 26. Horgan AF, Prasad B, Waldson DJ, et al: Acute urinary retention: Comparison of suprapubic and urethral catheterization. Br J Urol 70149-151, 1992

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27. Hukins DWL, Hickey DS, Kennedy AP: Catheter encrustation by struvite. Br J Urol 55:304-305, 1983 28. Huth TS, Burke JP, Larsen RA, et al: Randomized trial of meatal care with silver sulfadiazine cream for the prevention of catheter-associated bacteriuria. J Infect Dis 165:14-18, 1992 29. Ikaheimo R, Sutonen A, Karkkaunen U, et al: Virulence characteristics of E. coli in nosocomial urinary tract infection. Clin Infect Dis 16:785-791, 1993 30. Johnson JR, Roberts PL, Stamm WE: P-fimbriae and other virulence factors in E. coli urosepsis-association with patients’ characteristics. J Infect Dis 156:225229, 1987 31. Kunin CM, Steele C: Culture of the surface of urinary catheters to sample the urethral flora and study the effect of antimicrobial therapy. J Clin Microbiol 21:902-908, 1985 32. Kunin CM, McCormack RC: Prevention of catheterinduced urinary tract infections by sterile closed drainage. N Engl J Med 274:1115, 1966 34. Kunin CM, Chin QF, Chambers ST Formation of encrustations on indwelling urinary catheters in the elderly: A comparison of different types of catheter materials in ’blockers’ and ‘nonblockers.’ J Urol 138:899-902, 1987 35. Lundeberg T Prevention of catheter-associated urinary-tract infections by use of silver-impregnated catheter. Lancet 21031, 1986 36. Maki DG, Henckens CH, Bennet JV, et al: Nosocomial urinary tract infection with Sermtia marcescens: An epidemiologic study. J Infect Dis 128579-587, 1973 37. Marcos MA, Abdalla S, Pedraza F, et al: Epidemiological markers of Acinetobacter baumanni clinical isolates from a spinal cord unit. J Hosp Infect 28:3948, 1994 38. Matsumoto T, Sakumoto M, Tabahashi K, et al: Prevention of catheter-associated urinary tract infection by meatal disinfection. Dermatology 195(suppl2):7377, 1997 39. Miller A, Gillespie WA, Slade N, et al: Prevention of urinary infection after prostatectomy. Lancet 2:886888, 1960 40. Mobley HLT, Chippendale GR, Tenney JH, et al: MR/ K hemagglutination of Prouidencia stunrtii correlates with catheter adherence and with persistence in catheter-associated bacteriuria. J Infect Dis 157264271, 1988 41. Montgomerie JZ, Morrow J W Pseudomonas colonization in patients with spinal cord injury. Am J Epidemiol 108:328-336, 1978 42. Morrison AJ, Wenzel RP: Nosocomial urinary tract infection d u e to enterococci. Arch Intern Med 146~1549-1551,1986 43. Mountokalakis T, Skounakis M, Tselentis J: Shortterm versus prolonged systemic antibiotic prophylaxis in patients treated with indwelling catheters. J Urol 134:506-508, 1985 44. Mulholland SG, Bruun JN: A study of hospital urinary tract infections. J Urol 110:245247, 1973 45. Mulholland SG,McGarrity GJ, Ross OA, et al: Experience with detailed surveillance of nosocomial infection. Surg Gynecol Obstet 140941-945, 1975 46. Nickel JC, Gristina AG, Costerton JW: Electron microscopic study of an infected Foley catheter. Can J Surg 28:50-52, 1985 47. Nyren P, Runeberg L, Kostiala AI, et al: Prophylactic metheneamine hippurate or nitrofurantoin in patients with indwelling urinary catheter. Ann Clin Res 13:16-21, 1981 48. Ouslander JG, Greengold 8,Chen S: Complications

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of chronic indwelling catheters among male nursing home patients: A prospective study. J Urol 138:11911195, 1987 49. Ouslander J, Greengold B, Chen S External catheter use and urinary tract infection among incontinent male nursing home patients. J Am Geriatr SOC 35:1063-1070, 1987 50. Platt R, Polk BF, Murdock B, et al: Risk factors for nosocomial urinary tract infection. Am J Epidemiol 1241977-985, 1986 51. Platt R, Polk BF, Murdock B, et al: Mortality associated with nosocomial urinary tract infection. N Engl J Med 307:637442, 1982 52. Ramsay JWA, Garnham AJ, Mulhall AB, et al: Biofilms, bacteria and bladder catheter. Br J Urol64395398, 1989 53. Reid G, Sharma S, Advikolama K, et al: Effects of ciprofloxacin, norfloxacin, and ofloxacin on in vitro adhesion and survival of Pseudomonas aeruginosa AK1 on urinary catheters. Antimicrob Agent Chemother 38:2768-2774,1994 54. Saint S, Elmore JG, Sullivan SD, et a1 The efficacy of silver alloy-coated urinary catheters in preventing urinary tract infection-a meta-analysis. Am J Med 105:236-241, 1998 55. Schaberg DR, Haley RW, Highsmith AK, et al: Nosocomial bacteriuria: A prospective study of case clustering and antimicrobial resistance. Ann Intern Med 93:420424, 1980 56. Schaeffer A]: Catheter-associated bacteriuria. Urol Clin North Am 4735-758, 1986 57. Schaeffer AJ, Story KO, Johnson SM: Effect of silver oxide/trichloroisocyanuric acid antimicrobial drainage system on catheter-associated bacteriuria. J Urol 139~69-72,1988 58. Schiotz HA, Malme PA, Tanbo TG: Urinary tract infections and asymptomatic bacteriuria after vaginal plastic surgery: A comparison of suprapubic and transurethral catheter. Acta Obstet Gynecol Scand 68:453-455, 1989 59. Speller DCE, Stephens ME, Viant AC: Hospital infection by Pseudornonas cepacia. Lancet 1:798-799, 1971

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