Urinary Tract Infection at a University Hospital in Saudi Arabia: Incidence, Microbiology, and Antimicrobial Susceptibility

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1 Urinary Tract Infection at a University Hospital in Saudi Arabia: Incidence, Microbiology, and Antimicrobial Susceptibility Ahmed T. Eltahawy, MB, BCh, DipBact, PhD; Ragaa M. F. Khalaf, MB, BCh, DipBact, PhD From the Department of Microbiology, King Abdulaziz University Hospital (Dr. Eltahawy) and Faculty of Medicine, King Abdulaziz University (Dr. Khalaf), Jeddah. Address reprint requests and correspondence to Dr. Eltahawy: Consultant Microbiologist, King Abdulaziz University Hospital, P.O. Box 6615, Jeddah 21452, Saudi Arabia. Accepted for publication 12 September ABSTRACT Midstream and catheter stream specimens of urine from inpatients and outpatients at King Abdulaziz University Hospital in Jeddah, Saudi Arabia, were collected over a period of 12 months to determine prospectively the incidence of urinary tract infection, the predominant causative organisms, and their antimicrobial susceptibility. A total of 575 of 9845 specimens (5.8%) showed significant bacteriuria. The overall prevalence of urinary tract infection was 12.1%, 7.4% in inpatients and 4.7% in outpatients. Infection was found more frequently in females than males (2:1). Four percent of the patients were catheterized at the time of the survey; 21% of catheterized patients and 6% of noncatheterized patients were infected. A knowledge of local organisms and their antimicrobial susceptibility pattern is invaluable for the empirical treatment of urinary tract infection. Guidelines for the use of the urethral catheter, when introduced and followed, can reduce hospital-acquired urinary tract infection. AT Eltahawy, RMF Khalaf, Urinary Tract Infection at a University Hospital in Saudi Arabia: Incidence, Microbiology, and Antimicrobial Susceptibility. 1988; 8(4): 1-6 MeSH KEYWORDS: Urinary tract infections, microbiology; Escherichia coli infections; Klebsiella infection URINARY TRACT INFECTION is a relatively common condition in both hospitalized and nonhospitalized patients, particularly females. 1 Infections of the urinary tract are one important cause of bacteremia due to gram-negative microorganisms in Saudi Arabia 2 and other countries. 3-5 Early detection and eradication of bacteriuria and prevention of recurrence reduce the incidence of subsequent life-threatening consequences of persistent or repetitive urinary tract infection. The aim of this study was to determine the incidence of urinary tract infection in both hospitalized and nonhospitalized patients, the predominant causative organisms, and their antimicrobial susceptibilities. Materials and Methods Midstream and catheter stream specimens of urine from inpatients and outpatients were collected over a period of 12 months from October 1985 through September Patients were given instructions in Arabic on how to wash and collect a midstream specimen of urine in a sterile universal container. Urine samples obtained from indwelling catheters were collected by aspiration from the tube after the tube was cleaned with alcohol pads and

2 clamped for approximately 30 minutes. Urine samples were either transported to the Microbiology Laboratory for culture within 30 minutes of collection or refrigerated. Care was taken to avoid duplicate measurement of the same isolates. Microscopic examination of unspun, well-mixed samples was done for white and red blood cells and organisms by a counting chamber method. Culture of urine and determination of bacterial counts were performed by a routine semiquantitative method using filter paper screening method by Leigh and Williams. 6 The foot of the filter paper has a measured standardized area, and the urine-inoculated foot is pressed against the surface of the cystine-lactose-electrolyte-deficient (CLED) agar plate. Each plate was inoculated with six tests, each in duplicate. After overnight incubation at 37 C, the number of colonies in the impression area was counted, and if over 25 colonies were present, the original urine sample was known to have contained greater than 10 5 organisms per milliliter, indicating significant bacteriuria. 1 Low counts were accepted in catheter specimens if the organism persisted or was isolated from successive specimens. The isolates were identified using standard methods. 7 Gramnegative bacilli were identified using the API 20 (Analytab Inc). Antimicrobial susceptibilities were determined using the method of Stokes. 8 The antibiotics tested on each disk were ampicillin, 25 µg; carbenicillin, 100 µg; cephaloridine, 30 µg; gentamicin, 10 µg; nalidixic acid, 30 µg; nitrofurantoin, 200 µg; sulfamethoxazole, 100 µg; tetracycline, 20 µg; and trimethoprim, 1.25 µg. For the purpose of analysis the urinary tract infections of inpatients that occurred at or after 3 days of hospitalization were considered hospitalacquired. Urinary tract infections occurring before this time were considered to have originated in the community unless the infection was clearly related to a procedure performed after hospital admission. Results The specimens of urine collected from inpatients and outpatients at King Abdulaziz University Hospital (200 beds) in Jeddah, Saudi Arabia, during a 12-month period totaled 9845, 5832 (59%) from outpatients and 4013 (41%) from inpatients. Five hundred seventy-five specimens (5.8%) showed significant bacteriuria, 52% were from outpatients and 48% from inpatients. Female patients had more positive specimens than male patients, 380 of 578 (66%). The female prevalence was noticed in both inpatients and outpatients, as shown in Table 1. The age of patients is also shown in this table. Urinary tract infection was more frequent in women than men up to the age of 50 years. More than 50% of patients with significant bacteriuria were in the age group Table 1. Occurrence of urinary tract infection by age and sex. Inpatients Outpatients Age group (y) Total no. % Female % Male Total no. % Female % Male < > The organisms isolated from urine of inpatients and outpatients with urinary tract infections are shown in Table 2. The most frequently encountered organisms were Escherichia coli, Klebsiella-Enterobacter species, and Pseudomonas species. There was no significant difference in the microbial etiology in urinary tract infections in inpatients and outpatients. Table 3 shows the resistance pattern of the organisms isolated from urine of patients with urinary tract infection compared with the average of the resistant strains isolated over the period 1983 through E. coli showed high resistance to sulfamethoxazole, ampicillin, tetracycline, and carbenicillin. Resistance of Klebsiella-Enterobacter species was substantial against sulfamethoxazole, ampicillin, and carbenicillin. Serratia and Citrobacter species also showed high resistance against sulfamethoxazole and ampicillin. Proteus species were highly resistant not only to

3 sulfamethoxazole but also to trimethoprim; on the other hand, only 32% of Proteus species were resistant to ampicillin. Sixty-five percent of Pseudomonas species were resistant to carbenicillin and % to gentamicin. Resistance to three or more antimicrobial agents was observed in 81% of E. coli, 83% of Proteus organisms, and 91% of Klebsiella-Enterobacter species. More than 20% of Pseudomonas species were resistant to both gentamicin and carbenicillin. Table 2. Organisms isolated from urine of inpatients and outpatients with urinary tract infection. Organisms Inpatients (n = 300) No. (%) Outpatients (n = 275) No. (%) E. coli 111(37) 110(40) Klebsiella-Enterobacter 99(33) 80(29) Pseudomonas 33(11) 16(6) Serratia 18(6) 25(9) Proteus 12(4) 11(4) Citrobacter 15(5) 11(4) Providencia 1(0.3) 0 Acinetobacter 0 1(0.4) Staphylococcus aureus 3(1) 3(1) Staphylococcus albus 1(0.3) 0 Streptococcus faecalis 9(3) 16(6) Candida 1(0.3) 1(0.4) Antimicrobial E. coli agent (n = 22) Trimethoprim 59 (45) Sulfamethoxazole 87 (64) Nalidixic acid 10 (16) Nitrofurantoin 32 (20) Carbenicillin 63 (56) Gentamicin 3 (1.6) Ampicillin 69 (63) Cephaloridine 37 (41) Tetracycline 69 (62) Table 3. Resistance pattern of organisms isolated from urine.* Klebsiella- Enterobacter (n = 179) 59 (42) 86 (67) 21 (18) 71 (35) 78 (66) 3 (5) 84 (87) 41 (36) 54 (47) Pseudomonas (n = 50) 64 (44) (19) Serratia (n = 43) 54 (91) (18) 42 (45) 63 (91) 7 (10) 72 (79) 58 (29) 65 (71) Proteus (n = 23) 91 (90) 78 (97) (19) (16) 4 (6) (32) (13) 70 (80) Citrobacter (n = 23) 65 (40) 83 (80) 17 (10) 44 (60) 57 (50) 4 (20) 70 (70) 30 (60) 61 (50) S. faecalis (n = 23) 61 (54) *Top number indicates percentage of resistant strains. Bottom number in parentheses indicates average percentage of resistant strains over the last 3 years (1983 through 1985). The occurrence of urinary tract infection according to clinical service is shown in Table 4. Surgical patients accounted for about 34% of all admissions, but only 25% of patients with urinary tract infection. On the other hand, medical patients accounted for about 11% of all admissions but for 23% of patients with urinary tract infection. More females (60%) than males (40%) were admitted, and a much greater preponderance of females (65%) was noted among patients with urinary tract infection. The rate of infection among females was also higher (32/1000 female admissions versus 28/1000 males) (Table 4) (71) (45)

4 Table 4. Occurrence of urinary tract infection according to clinical service. Analysis No. of hospital admissions (%) No. of urinary tract infection cases (%) Rate of infection/1000 admissions Service Medical 1049 (11) 69 (23) 66 Surgical 3251 (34) 74 (25) 23 Obstetric and gynecology 2704 (28) 92 (31) 34 Pediatrics 23 (27) 65 (22) 25 Sex Male 3851 (40) 106 (35) 28 Female 5776 (60) 194 (65) 34 Total The distribution of urinary tract infection and urinary catheter infection by specialty is given in Table 5. Urinary tract infection not associated with catheterization occurred most frequently in pediatric, genitourinary, and medical wards, in that order (Table 5). These infections were mainly community-acquired. On the other hand, catheterassociated urinary tract infections were encountered most frequently in obstetric and gynecology, genitourinary, and surgery wards, in that order. These infections were mostly hospital-acquired. The association between urinary catheter, urinary tract infection, and sex of the patients is shown in Table 6. There was no significant difference between males and females in the prevalence of catheter among those infected. There was also no significant difference between males and females in prevalence of infection among those catheterized. Twenty-one percent of catheterized patients were diagnosed as having infection compared with only 6% of noncatheterized patients. Table 5. The distribution of urinary tract infection and urinary catheter by specialty. Infected noncatheterized Community- Hospitalacquired acquired Infected catheterized Community- Hospitalacquired acquired Service No. (%) No. (%) No. (%) (%) No. Medical 37 (4) 30 (3.3) 0 2 (6.6) Surgical 10 (2.2) 15 (3.2) 1 (3.4) 9 (31) Genitourinary 11 (5.6) 0 8 (9.3) 20 (23) Obstetric and 35 (2.5) 14 (1) 0 43 (17) gynecology Pediatric 28 (4) 37 (5.6) 0 0 Total 121 (3.3) 96 (2.7) 9 (2.3) 74 (18.6) Table 6. Association between the presence of a catheter and urinary tract infection by sex. Catheterized Infected Not infected Total % Infected Male Female Noncatheterized Male Female Total

5 Discussion In view of the anatomic differences between males and females, it is not surprising that infection was found more frequently in females than in males (2:1); the same ratio approximately applied to inpatients and outpatients (1.9:1 and 2.1:1, respectively). This female prevalence agrees with that reported by others. 3,9-11 The overall prevalence of inpatient urinary tract infection of 7.5% agrees with that reported by Jepsen et al, 3 but is higher than reported elsewhere. 9,12 Urinary tract infection is the most common kind of hospital-acquired infection at KAUH, representing 33% of hospital-acquired infection (unpublished data). The spectrum of microorganisms isolated from urine showed no unexpected features and conformed well with that described by others 10,13,14 but differs from the report by Mahgoub et al, 11 where E. coli accounted for 75% of the isolates, Klebsiella-Enterobacter 15%, and Pseudomonas 2%. The result of our survey showed E. coli as the single most common pathogen, and both E. coli and Klebsiella species were the main causes of urinary tract infection at KAUH where they accounted for approximately 70% of the isolates. The urine isolates were reasonably sensitive to nalidixic acid (82%) and cephaloridine (64%). Resistance to gentamicin was observed in only 8% of the strains. On the other hand, 78% of the strains were resistant to sulfamethoxazole and 55% to trimethoprim, two widely used drugs. About 64% of the urine isolates were resistant to ampicillin as well as carbenicillin, but 46% only were resistant to nitrofurantoin. The reason for the high degree of antibiotic resistance among isolated organisms at KAUH is obviously the misuse of antibiotics which encourages selection of resistant strains. 15 There was no outbreak of infection by a resistant organism during the period of the study. Urinary tract infection in male patients who did not have catheters was more prevalent from the age of 50 onward, unlike female patients, who had urinary tract infection most frequently between the ages of 20 and 40 years. With catheter-associated urinary tract infection, on the other hand, age' did not appear as a predisposing factor to urinary tract infection as 71% of catheterized males were over 40 years, but 82% of catheterized females were under 40 years. As a risk factor, age may be secondary to the foreign body effect of the catheter. The role of the catheter in relation to the acquisition of urinary tract infection was clearly confirmed in this study, as reported by others. 14,16,17 Urinary catheters were present in 4% of the patients at the time of the survey. The distribution of catheters by specialty was generally in accord with the distribution of infections, though it must be acknowledged that other factors (duration of catheterization and technical difficulty) must be taken into account. Twenty-one percent of those catheterized were infected, and 28% of those infected were catheterized. The latter association is insignificant, though the association is stronger for males than for females. It has been suggested that the importance of urinary tract infection lies in the fact that a proportion of patients go on to develop life-threatening septicemia. 17 In our study of septicemia at KAUH, 2 the urinary tract was the source of septicemia in 16% of hospital-acquired infections and in 19% of community-acquired infections, and E. coli was the predominant causative organism. The differences in the prevalence of catheter-associated urinary tract infection in different specialties indicate that varying policies had been adopted. The variables that are alterable, such as the indication for and the technique of catheterization, require more attention and realistic policy which must be strictly followed. Knowledge of local organisms and their antimicrobial susceptibilities will enable clinicians and clinical microbiologists to decide on the most appropriate antibiotic for the treatment of urinary tract infection and reduce the incidence of life-threatening septicemia. References 1. Kass EH, Miall WE, Stuart KL, Rosner B. Epidemiologic aspects of infections of the urinary tract. In: Kass EH, Brumfitt W, eds. Infections of the urinary tract. Chicago: University of Chicago Press, 1978: Eltahawy ATAE, Khalaf RMF. Bacteraemia at a university hospital in Saudi Arabia: incidence, microbiology, and therapeutic considerations. Saudi Med J 1986;7(6): Jepsen OB, Larsen SO, Dankert J, et al. Urinary-tract infection and bacteraemia in hospitalized medical patients a European multicentre prevalence survey on nosocomial infection. J Hosp Infect 1982;3(3): Svanbom M. Septicemia: 1. a prospective study on etiology, underlying factors and sources of infection. Scand J Infect Dis 1979;11: McGowan JE Jr, Parrott PL, Duty VP. Nosocomial bacteremia: potential for prevention of procedure-related cases. JAMA 1977;233(25): Leigh DA, Williams JD. Method for the detection of significant bacteriuria in large groups of patients. J Clin Pathol

6 1964;17: Cowan ST. Cowan and Steel's manual for the identification of medical bacteria. 2nd ed. Cambridge: Cambridge University Press, 1981: Stokes EJ, Waterworth PM. Antibiotic sensitivity tests by diffusion methods. ACP Broadsheet 1972;55: Meers PD, Ayliffe GAJ, Emmerson, et al. Survey of infection in hospitals, J Hosp Infect 1981;2(suppl Dec): Talukder MAS, Al-Admawy AMO, Abu Al-Saud A. Urinary tract infection: a study of bacterial etiology in Riyadh Military Hospital. Proceedings of the 4th Saudi medical meeting 1979; Mahgoub E, Chowdhury H, Jamjoom GA, Kambal AM. The pattern of bacteriuria of urinary tract infection at King Abda- Aziz Teaching Hospital, Riyadh. Proceedings of the 7th Saudi medical meeting 1982; Nystrom B. Prevalence studies of the incidence of hospital infections. Lakartidningen 1976;73: Bernander S, Hanbraeus A, Myrback KE, et al. Prevalence of hospital-associated infections in five Swedish hospitals in November Scand J Infect Dis 1978;10(l): Kunin CM. Urinary tract infections. In: Bennett JV, Brachman PS, eds. Hospital infections. Boston: Little, Brown, 1979: Altahawy ATAA, Khalaf RMF. Antimicrobial prescribing at university hospital in Saudi Arabia. Saudi Med J 1987;8(l): Andriole VT. Hospital acquired urinary tract infections and the indwelling catheter. Urol Clin North Am 1975;2(3): Stamm WE. Infection related to medical devices. Ann Intern Med 1978;89(5, pt 2 suppl):764-9.