Infection/Inflammation
Day of Surgery Urine Cultures Identify Urogynecologic Patients at Increased Risk for Postoperative Urinary Tract Infection Cynthia S. Fok,* Kathleen McKinley, Elizabeth R. Mueller,† Kimberly Kenton, Paul Schreckenberger, Alan Wolfe and Linda Brubaker From the Division of Female Pelvic Medicine and Reconstructive Surgery, Departments of Urology and Obstetrics & Gynecology (CSF, ERM, KK, LB), Department of Pathology (KM, PS), and Department of Microbiology and Immunology (AW), Stritch School of Medicine, Loyola University Chicago, Maywood, Illinois
Purpose: Despite preoperative screening and treatment for urinary tract infections, a postoperative urinary tract infection develops in approximately 1 in 5 urogynecologic patients. In this study we assess the proportion of urogynecologic patients with a positive day of surgery urine culture, the clinical consequences of a positive day of surgery culture and differences in postoperative urinary tract infection risks based on day of surgery culture. Materials and Methods: After institutional review board approval, patients undergoing urogynecologic surgery at Loyola University Medical Center were recruited for the study. Catheterized urine samples were collected in the operating room before intravenous antibiotic administration. Clinical cultures were considered positive if 1,000 colonies per ml or more bacteria were found on routine culture. For analysis we matched each woman with a positive culture with 2 women with negative culture by age within 10 years and within surgical groups (ie prolapse and/or incontinence). Data were analyzed using SPSS® version 19. Results: Nearly a tenth (9.5%) of participants had positive day of surgery cultures. The clinical and demographic characteristics were similar in women with negative vs positive day of surgery cultures. However, women with positive day of surgery cultures were more likely to experience a postoperative urinary tract infection despite standard perioperative antibiotic administration (29.6% vs 5.6%, p ⫽ 0.005, odds ratio 7.2). Regardless of day of surgery culture status no participant experienced postoperative systemic urinary complications. Conclusions: Nearly a tenth of urogynecologic patients had positive day of surgery cultures. Patients with a positive day of surgery culture had an increased risk (29.6%) of postoperative urinary tract infection within 6 weeks of surgery. These findings highlight an opportunity to identify and treat patients with positive day of surgery cultures and reduce the incidence of postoperative urinary tract infections.
Abbreviations and Acronyms DOS ⫽ day of surgery POP ⫽ pelvic organ prolapse UI ⫽ urinary incontinence UTI ⫽ urinary tract infection Accepted for publication November 29, 2012. Study received institutional review board approval. * Correspondence: Loyola University Medical Center, 2160 S. First Ave., Bldg. 103-Room 1008, Maywood, Illinois 60153 (telephone: 708-216-6016; FAX: 708-216-2171; e-mail:
[email protected]). † Financial interest and/or other relationship with Allergan and Astellas.
Key Words: urologic surgical procedures, gynecologic surgical procedures, urinary tract infections PELVIC floor disorders are common. Approximately 1 in 4 American women will be affected by at least 1 pelvic floor disorder (eg pelvic organ prolapse, urinary incontinence or fecal incontinence) in their lifetime, and approxi-
mately 1 in 10 of these women will undergo POP and/or UI surgery.1–3 Urinary tract infections are also common, with half of American women experiencing a UTI in their lifetime.4 A risk factor for UTI in women is
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lower tract instrumentation during surgery, especially POP/UI procedures. Two large National Institutes of Health randomized surgical trials, the Stress Incontinence Surgical Treatment Efficacy Trial (SISTEr) and the Trial of Mid-Urethral Slings (TOMUS), document that the risk of postoperative UTI in patients undergoing POP/UI surgery ranges from 7% to 24%.5,6 For Medicare beneficiaries undergoing sling surgery for stress UI, the risk of postoperative UTI is approximately 1 in 3.7 In elderly women undergoing obliterative POP surgery the risk of postoperative UTI is even higher at 45%.8 With the high rate of postoperative UTI in women undergoing POP/UI surgery and the economic costs associated with UTI, several groups have sought to identify UTI risk factors.4,9,10 However, many of these studies are limited by the clinical practice of empirically treating UTI with antibiotics without obtaining urine cultures. Although some risk factors for UTI and recurrent UTI have been identified, they are often of limited applicability to the surgeon on the day of surgery. Therefore, we prospectively studied the risk factors of postoperative UTI in women undergoing POP/UI surgery.
METHODS After institutional review board approval, we recruited patients undergoing POP and/or UI surgery at Loyola University Medical Center. This cohort is part of a larger study assessing the female urinary microbiota. Women were excluded from analysis if they were not primarily English speaking, were unable to complete the questionnaires, had surgery with planned transurothelial entry (eg removal of foreign body), had recurrent UTIs, had recent treatment for UTI or were on active treatment for UTI. All participants provided written informed consent for research participation. Consistent with our clinical standard of care, all patients had been assessed at least once for urinary tract infection before surgery. Our clinical algorithm is to obtain a catheterized urine sample and perform a standard dipstick urinalysis for all patients at initial consultation. Urine was sent for urine culture if patient insurance allowed. All patients who underwent preoperative urodynamic testing also had a catheterized urine dipstick performed before urodynamic testing. After the initial visit, urine cultures were only sent if there was clinical suspicion for a UTI. Per our clinical practice all patients who underwent transurethral catheterization for urine specimen or urodynamic testing were given a single dose of appropriate oral antibiotic based on allergy profile. Standard UTI treatment was given to patients when the physician made a clinical diagnosis of UTI and/or if the urine culture was positive. Any patient on antibiotics for a UTI preoperatively was excluded from participation in the study. At surgery the sterile surgical field was established and catheterized urine samples were obtained for routine culture before administration of 1 dose of intravenous peri-
operative antibiotics. These urine samples were sent to our clinical microbiology laboratory for routine culture. Routine urine culture consisted of inoculation of sheep blood agar and MacConkey agar plates with 1 l urine and examination of plates for bacterial growth after 24 hours of incubation at 35C in room atmosphere. For the latter part of our cohort, in addition to routine aerobic culture, anaerobic urine culture was performed by inoculating an anaerobic sheep blood agar plate with 1 l urine followed by examination for bacterial growth after 72 hours of incubation at 35C in an anaerobic atmosphere. A DOS urine culture was considered positive if at least 1,000 bacterial colonies per ml were reported. As it is not clinical practice to obtain DOS cultures, the decision was made a priori that no participant would be treated based on DOS culture status. A catheterized urine culture specimen was collected from women who presented in the first 6 weeks after surgery with signs or symptoms consistent with a UTI (ie positive urine dipstick, dysuria, frequency, urgency). Postoperative UTI was defined as at least 1,000 bacterial colonies per ml. To increase the power of our study to detect any differences should they exist, we opted to use case control matching. Therefore, we matched each woman with a positive DOS culture with 2 women with negative cultures by age within 10 years and within surgical groups (ie POP only, UI only, POP and UI). Demographic and clinical data were collected and analyzed using SPSS version 19.
RESULTS Of 284 study participants 27 (9.4%) had positive DOS cultures. Each woman with a positive DOS culture was age matched within surgical groups to 2 participants who had negative DOS cultures (54). The majority of participants in each cohort underwent POP only surgery with 19 (70%) in the DOS positive group compared to 37 (69%) in the DOS negative group. The DOS positive cohort had only 2 (7%) participants who underwent UI only surgery and 6 (22%) who underwent combined POP/UI surgery. Consistent with our cohort matching the DOS negative group had 4 (7%) participants who underwent UI only surgery and 13 (24%) who underwent combined POP/UI surgery. The 2 groups were similar in the demographic and clinical variables of age (69 vs 66 years), race (Caucasian 93% vs 91%) and body mass index (28 vs 27 kg/m2) (see table). Given that our practice is located at a tertiary care center, sometimes there was a delay from initial presentation to DOS. For most patients that delay was about 1 month. The percentage of patients who had any assessment for UTI within the 4 weeks before surgery was similar for patients with positive and negative DOS cultures (74% vs 78%, p ⫽ 0.34). In our practice only the women who go home with a Foley catheter are given treatment course antibiotics starting the day the catheter is removed. The
URINE CULTURES ON DAY OF UROGYNECOLOGIC SURGERY
Patient demographics
Mean pt age (range) Mean kg/m2 body mass index (range) No. race (%): Caucasian African-American Other No. diabetes (%) No. hypertension (%) No. coronary artery disease (%) No. current smokers (%) No. hormone status (%): Premenopausal Postmenopausal on hormones Postmenopausal no hormones
DOS Pos
DOS Neg
p Value
69 (44–89) 28 (23–44)
66 (40–86) 27 (16–46)
0.32 0.29
25 (92.6) 2 (7.4)
49 4 1 3 20 5 1
(91) (7) (2) (6) (37) (9.3) (2)
0.57
5 11 38
(9) (20)† (70)
0 13 5 0
(48) (19)
4 4 19
(15) (15)* (69)
0.22 0.34 0.24 0.48 0.73
* Systemic hormone replacement in 3 women and vaginal estrogen in 1. † Systemic hormone replacement in 7 women and vaginal estrogen in 4.
percentage of women who went home with an indwelling Foley catheter was also similar for those with positive and negative DOS cultures (15% vs 19%, p ⫽ 0.45). In contrast, women with positive DOS cultures were significantly more likely to experience a postoperative UTI than those with negative DOS cultures (29.6% vs 5.6%, p ⫽ 0.005, odds ratio 7.2). The majority of bacteria found in the urine cultures were typical uropathogens, including Escherichia coli, Pseudomonas, Enterococcus, Klebsiella species and Staphylococcus species. Other cultured bacteria included Corynebacterium, Streptococcus agalactiae (Group B strep) and Lactobacillus. From some of the urine samples the clinical microbiology laboratory also isolated strict or facultative anaerobes, including Lactobacillus, Clostridium and Gemella morbillorum or microaerophilic Streptococcus species. Antibiotic treatment was provided to 10 of 27 (37%) patients with a positive DOS culture during the postoperative period (8 for urinary and 2 for skin indications). Antibiotics were prescribed based on clinical practice for home Foley removal, clinical suspicion for UTI or skin infection. No participant in this small cohort with DOS positive cultures experienced postoperative systemic urinary complications such as pyelonephritis or urosepsis. There was no difference in overall rate of complications between the 2 groups.
DISCUSSION In this small cohort of women undergoing urogynecologic surgery at a tertiary care center we found higher than expected rates of DOS positive urine cultures. We also observed a correlation between DOS positive culture status and increased risk of postoperative UTI. However, DOS positive culture
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status was not associated with any systemic urinary complications. Most bacteria isolated in these urine cultures were usual uropathogens. However, we also observed less common uropathogens and some anaerobes. To our knowledge, this is the first study to examine the rate of positive DOS urine cultures, and the results suggest that preoperative identification of women at risk for DOS positive urine cultures could help tailor their treatment. The outcome of successful tailored treatment would be a decrease in the overall rate of postoperative UTIs in the urogynecologic surgical population. Despite standard clinical care efforts to eliminate UTI before POP/UI surgery, nearly a tenth of our patients undergoing urogynecologic surgery had a positive urine culture on the day of surgery. Despite this higher than expected rate, it is fortunate that no women in this small cohort experienced any systemic complications from lower urinary tract instrumentation with cystoscopy at surgery. Despite the routine use of intravenous antibiotics at the time of POP/UI surgery, women with positive DOS cultures were at higher risk for postoperative UTIs than those with negative DOS cultures. The current guidelines state that women undergoing pelvic floor surgery should receive a single dose of first generation cephalosporin perioperatively.11 However, this observation coupled with a rate of postoperative UTI after POP/UI surgery reported to be as high as a quarter to almost a half, argues that a single dose of intravenous antibiotics may be insufficient to prevent post-instrumentation UTI in the urogynecologic population.5,6,8 Although the positive urine cultures of this cohort contained typical aerobic uropathogens, some also contained anaerobic bacteria. In 1980 Brumfitt et al reported on a case of persistent pyuria that was caused by anaerobic and microaerophilic bacteria.12 The authors argued that routine anaerobic urine culture was unnecessary, but was useful in difficult cases where symptoms persisted despite the inability to grow bacteria on routine urine culture. With advancements in DNA sequencing techniques, the identification of anaerobes in urine has become much easier.13 Using these techniques our group along with others recently reported DNA evidence of aerobic and anaerobic bacteria in the urine of even asymptomatic women with negative culture.14 These findings suggest the need for further studies to better understand the urinary microbiota. The higher than expected rate of positive DOS cultures in patients undergoing POP/UI surgery suggests that identification of those at risk for DOS positive urine cultures may help to decrease the risk of postoperative UTIs in the urogynecologic surgery population. Unfortunately there were no clear clinical factors that we could use to identify such patients, at least in this small cohort. The fact that
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atypical bacteria could be identified in the urine by anaerobic culture methods or by DNA sequencing suggests that we lack sufficient understanding of the urinary microbiota. Increased understanding should not only provide insight for the identification of patients at risk for postoperative UTI, but also for understanding how urinary bacteria impact women with pelvic floor disorders. The incidence of pelvic floor disorders is increasing. It is estimated that by the year 2050 more than 58 million women will suffer from at least 1 pelvic floor disorder.3 Coincident with this increase in pelvic floor disorders will be an increase in the number of women undergoing POP/UI surgery, which is estimated to increase to almost 250,000 by 2050.3 Pre-
venting a postoperative UTI from developing in approximately a quarter of these women could yield significant health care cost savings. Although there are no specific data regarding patient dissatisfaction with postoperative UTI, there is abundant literature showing that postoperative urinary symptoms are a patient dissatisfier.15,16 From a patient care and health care costs standpoint it is clear that an active effort must be made to decrease the current unacceptably high postoperative UTI rate. The surprisingly high rate of DOS positive cultures in women undergoing POP/UI surgery offers the opportunity to develop a preoperative screening tool to identify women at risk for postoperative UTI and then to discover treatments to reduce that risk.
REFERENCES 1. Nygaard I, Barber MD, Burgio KL et al: Prevalence of symptomatic pelvic floor disorders in US women. JAMA 2008; 300: 1311. 2. Olsen AL, Smith VJ, Bergstrom JO et al: Epidemiology of surgically managed pelvic organ prolapse and urinary incontinence. Obstet Gynecol 1997; 89: 501. 3. Wu JM, Kawasaki A, Hundley AF et al: Predicting the number of women who will undergo incontinence and prolapse surgery, 2010 to 2050. Am J Obstet Gynecol 2011; 205: e1. 4. Foxman B and Brown P: Epidemiology of urinary tract infections: transmission and risk factors, incidence, and costs. Infect Dis Clin North Am 2003; 17: 227. 5. Albo ME: The Trial Of Mid-Urethral Slings (TOMUS): design and methodology. J Appl Res 2008; 8: 1.
6. Richter HE, Albo ME, Zyczynski HM et al: Retropubic versus transobturator midurethral slings for stress incontinence. N Engl J Med 2010; 362: 2066. 7. Anger JT, Litwin MS, Wang Q et al: Complications of sling surgery among female Medicare beneficiaries. Obstet Gynecol 2007; 109: 707. 8. FitzGerald MP and Brubaker L: Colpocleisis and urinary incontinence. Am J Obstet Gynecol 2003; 189: 1241. 9. Nygaard I, Brubaker L, Chai TC et al: Risk factors for urinary tract infection following incontinence surgery. Int Urogynecol J 2011; 22: 1255. 10. Sutkin G, Alperin M, Meyn L et al: Symptomatic urinary tract infections after surgery for prolapse and/or incontinence. Int Urogynecol J 2010; 21: 955. 11. Van Eyk N, van Schalkwyk J and Infectious Diseases Committee: Antibiotic prophylaxis in
gynaecologic procedures. J Obstet Gynaecol Can 2012; 34: 382. 12. Brumfitt W, Gargan RA and Hamilton-Miller JM: Diagnosis and cure of recurrent urinary tract infection with microaerophillic and anaerobic bacteria. Br Med J 1980; 281: 909. 13. Imirzalioglu C, Hain T, Chakraborty T et al: Hidden pathogens uncovered: metagenomic analysis of urinary tract infections. Andrologia 2008; 40: 66. 14. Wolfe AJ, Toh E, Shibata N et al: Evidence of uncultivated bacteria in the adult female bladder. J Clin Microbiol 2012; 50: 1376. 15. Pham T, Kenton K, Mueller E et al: New pelvic symptoms are common after reconstructive pelvic surgery. Am J Obstet Gynecol 2009; 200: 88. 16. Mahajan ST, Elkadry EA, Kenton KS et al: Patientcentered surgical outcomes: the impact of goal achievement and urge incontinence on patient satisfaction one year after surgery. Am J Obstet Gynecol 2006; 194: 722.