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High Frequency of Staphylococcus Saprophyticus Urinary Tract Infections Among Female Adolescents

Lo, Denise Swei MD; Shieh, Huei Hsin MD; Barreira, Eliane Roseli MD; Ragazzi, Selma Lopes Betta MD; Gilio, Alfredo Elias PhD

The Pediatric Infectious Disease Journal: September 2015 - Volume 34 - Issue 9 - p 1023–1025
doi: 10.1097/INF.0000000000000780
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Staphylococcus saprophyticus is a rarely reported agent of urinary tract infection (UTI) in the pediatric population. In our retrospective 3-year study, S. saprophyticus comprised 24.5% of 106 isolates of UTIs in female adolescents 12–15 years of age who attended an emergency department. Clinicians should be aware of the high prevalence of this etiology when empirically treating UTIs in female adolescents.

From the Department of Pediatrics, Hospital Universitário of University of Sao Paulo, Sao Paulo, Brazil.

Accepted for publication February 26, 2015.

The authors have no funding or conflicts of interest to disclose.

Address for correspondence: Denise Swei Lo, Departamento de Pediatria, Universidade de São Paulo, Av. Professor Lineu Prestes, 2565 – Butantã, Sao Paulo, CEP 05508-000, Brazil. E-mail:deswlo27@gmail.com.

The microbial etiology of urinary tract infections (UTIs) varies according to age and gender.1–6 In the pediatric population, Escherichia coli is the leading cause of UTIs reported worldwide.2–6 Among sexually active young females, E. coli remains the most important etiologic agent of UTIs, followed by Staphylococcus saprophyticus.1–8 In women 16–25 years old, the frequency of S. saprophyticus UTIs was reported to be 42.3% in 1978.4 Sexual intercourse is one of the most important risk factors for the development of UTIs attributable to this agent.1,4,8 In 2009, a national survey of 60,973 Brazilian teenage students in the 9th grade of public and private high schools showed that 1 of 3 adolescents reported having sexual activity, and most of them had their first sexual intercourse before the age of 13 years.9

In this study, we investigated the frequency and seasonal variations of S. saprophyticus UTIs in female Brazilian adolescents 12–15 years old and we compare clinical and laboratory differences between UTIs caused by S. saprophyticus and those caused by E. coli in this age group.

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METHODS

We conducted a retrospective case–control study at the Pediatric Emergency Department of Hospital Universitário of University of São Paulo, Brazil, which is a public secondary teaching hospital that serves an urban population of about 500,000 inhabitants. We reviewed the medical charts from all the female patients from 12 to 15 years old who had urine cultures performed for suspected UTIs from January 1, 2010 until December 31, 2012. Suspected UTI was defined as the presence of at least one of the following signs and symptoms: abdominal, suprapubic, or flank pain; dysuria; frequent or urgent urination; enuresis; and hematuria. Microbiologically confirmed UTI was defined by a urine culture ≥105 colony-forming units of a single uropathogen per milliliter of urine. Isolates that grew more than 1 uropathogen were considered contaminated and were excluded. For individuals who had multiple confirmed episodes of UTIs within the 3-year period, only 1 episode per month of the same bacteria was used to analyze the epidemiologic pattern. Information on age, treatment regimen (inpatient or outpatient) and the presence of a nitrite-positive test were analyzed from all patients with culture-confirmed S. saprophyticus and E. coli UTIs. Patients with incomplete clinical or laboratory records were excluded.

Urine specimens were obtained under aseptic conditions by freshly voided midstream urine and sent to the local laboratory for microbiologic evaluation within 1 hour. Samples were plated on MacConkey agar and blood agar using quantitative loops and were incubated at 37°C for 24 hours, or for 48 hours in negative cases. Isolates were identified by their biochemical reaction profile according to Vitek® 2 system (BioMérieux, Marcy l’Etoile, France). Data were analyzed using the SPSS statistical package. Categorical variables were compared using the χ2 or Fisher’s exact tests and continuous variables were compared with the Mann–Whitney test. A 2-sided P value less than 0.05 was considered statistically significant. The study was approved by the Committee of Ethics on Research of the Hospital Universitário.

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RESULTS

During the 3-year study period, 8141 urine cultures were performed from patients less than 15 years old who visited our Emergency Department for suspected UTI. Of these, 1072 had culture-confirmed UTIs. Two UTIs cases were excluded because of duplicate urine cultures collected in the same month (1 caused by S. saprophyticus and another by Enterococcus faecalis). Of the 1070 cases included, 780 (72.9%) occurred in females and 290 (27.1%) in males (Table 1). There were 955 cases in children younger than 12 years (89.3% of all UTIs) and 115 cases in adolescents aged 12–15 years old.

Table 1

Table 1

S. saprophyticus accounted for 32 episodes of overall UTIs, with the majority in female adolescents (26 cases). No male adolescent had S. saprophyticus bacteriuria. Among the 106 culture-confirmed UTIs in female teenagers, 87 had 1 positive urine culture in the period, while 9 had more than 1 positive sample. In female adolescents, E. coli was the most common agent and comprised 56 (52.8%) cases, followed by S. saprophyticus with 26 (24.5%) and Proteus mirabilis with 12 (11.3%) episodes. During the 3-year period, the annual range of E. coli isolates was 14–26 per year, and of S. saprophyticus 5–11 per year.

Table 2 shows the comparisons of clinical, seasonal and laboratory patterns between S. saprophyticus and E. coli UTIs in female adolescents. Age distribution was similar in both groups, with most of the isolates obtained from patients 14–15 years old (69.2% of S. saprophyticus and 57.1% of E. coli UTIs). We did not observe any significant seasonal trend in the distribution of S. saprophyticus or E. coli UTIs in our sample. Positive nitrite tests on urinalysis were more frequent for patients with UTIs caused by E. coli in comparison with S. saprophyticus (57.1% vs. 11.5%; P < 0.0001). All patients with S. saprophyticus bacteriuria had uncomplicated UTIs and were treated as outpatients, whereas 6 (10.7%) of the E. coli group patients needed hospitalization; one of these patients was a girl with neuroblastoma who had 2 hospital admissions for UTI within a 10-month interval.

Table 2

Table 2

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DISCUSSION

S. saprophyticus is coagulase-negative staphylococci that mainly colonizes and infects young sexually active women.1–8 Vincent et al8 demonstrated that recent sexual intercourse, the frequency of sexual activity, and the number of sexual partners increase the risk for UTIs in young adult females. The prevalence of UTI due to S. saprophyticus is variable in different studies depending on the age group reported, timing of first sexual intercourse and its frequency. The worldwide prevalence of UTIs due to S. saprophyticus varies from 3.6% to 42.3% in women.1–8 In our study, we found S. saprophyticus to be an important cause of UTIs among female adolescents (24.5%), mostly in older teenagers (14–15 years old). Previous studies reported that the mean age in adult females with S. saprophyticus UTIs is lower than the mean age of the female population as a whole.2–4,6 Our prevalence is higher than that reported recently by Sousa et al7 (16%), in a population of Brazilian women 16–49 years old, older than our study group. Although we did not investigate the pattern of sexual activity in our population, we hypothesize that our high frequency may be associated with early initiation of sexual activity among female Brazilian teenagers, which has been well documented in previous studies in Brazil.9,10 This hypothesis is reinforced by the fact that we found very few cases of S. saprophyticus UTIs in younger children. Furthermore, 19.2% of all births in Brazil are to girls aged 10 to 19 years old.10S. saprophyticus is an uncommon etiology of UTI in young males1,2,4 and we found no case of S. saprophyticus UTI in male adolescent. Our proportion of UTIs between female and male adolescents was 11.8:1. This proportion is in line with previous studies conducted in young adults, which show UTIs as a common infectious disease that affect mainly women.2,11

Seasonal variations in the incidence of S. saprophyticus UTIs have been previously reported. Pead et al1 showed a significant peak of UTIs due to S. saprophyticus during late summer and early fall in Portsmouth, UK, a holiday resort area that serves a large population of students. They speculated that the seasonal increase of S. saprophyticus UTIs was related to the temporary increase in the number of young women in the area. Eriksson et al2 reported similar findings at Stockholm, Sweden, showing higher incidence of S. saprophyticus UTIs in August and September, following the overall increase of UTIs during the summer. In contrast to those previous studies, our hospital is located at an urban area in the Southeast of Brazil, a region with a mild climate and poorly defined seasons, which may explain the lack of seasonal variations of S. saprophyticus UTIs.

E. coli is still reported as a major uropathogen worldwide, accounting for 57–83.8% of all UTIs in women.1–6 Therefore, recognizing the role of S. saprophyticus as a possible etiologic agent in female adolescents is essential to guide appropriate empirical antibiotic treatment, as the antimicrobial resistance pattern of these two bacteria may differ.2,3,6

Clinical suspicions of S. saprophyticus UTI may be reinforced by the finding of a nitrate negative test in the urinalysis. In contrast to E. coli, S. saprophyticus is unable to reduce nitrate,12 as shown by the nitrite negative test in most of our samples. S. saprophyticus UTIs may be, therefore, underdiagnosed if urine samples with nitrite negative test are not sent for culture. In our study, all subjects with S. saprophyticus UTIs were treated as outpatients, which strengthens the concept of a natural course of uncomplicated UTI due to S. saprophyticus, as previously reported.1,4,12

This study shows the highest frequency of S. saprophyticus UTIs ever reported in the pediatric population. Some limitations of this study, however, should be acknowledged. First, we adopted a higher cut-off level than the usual number of 10,000 CFU/mL for the diagnosis of UTI. This may have underestimated the number of S. saprophyticus UTIs in our study, as these coagulase-negative staphylococci tend to form clusters, therefore reducing the number of colonies identified on the culture media.12 Second, due to its retrospective nature, we had little information about the history of sexual activity, previous UTIs, the presence of genitourinary anomalies, outdoor swimming, prior exposure to raw meat or antibiotics—all of which can influence the occurrence of S. saprophyticus UTI.8,11 Finally, our sample was derived from a single center, which may limit the generalizability of our findings.

In conclusion, we found a high prevalence of UTIs due to S. saprophyticus in our sample of female adolescents, with no significant differences in the clinical and epidemiological features from UTIs due to E. coli but for the rarely nitrite positive test. Further studies are necessary to better elucidate the epidemiology and risk factors for S. saprophyticus UTIs. Clinicians should be aware of the high frequency of this etiology when empirically treating UTIs in adolescents and bear in mind the possibility of sexual activity and its consequence, such as unintended pregnancies and sexually transmitted diseases, when diagnosing S. saprophyticus UTIs in female teenagers.

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REFERENCES

1. Pead L, Maskell R, Morris J. Staphylococcus saprophyticus as a urinary pathogen: a six year prospective survey. Br Med J (Clin Res Ed). 1985;291:1157–1159
2. Eriksson A, Giske CG, Ternhag A. The relative importance of Staphylococcus saprophyticus as a urinary tract pathogen: distribution of bacteria among urinary samples analysed during 1 year at a major Swedish laboratory. APMIS. 2013;121:72–78
3. Schito GC, Naber KG, Botto H, et al. The ARESC study: an international survey on the antimicrobial resistance of pathogens involved in uncomplicated urinary tract infections. Int J Antimicrob Agents. 2009;34:407–413
4. Wallmark G, Arremark I, Telander B. Staphylococcus saprophyticus: a frequent cause of acute urinary tract infection among female outpatients. J Infect Dis. 1978;138:791–797
5. Lo DS, Shieh HH, Ragazzi SL, et al. Community-acquired urinary tract infection: age and gender-dependent etiology. J Bras Nefrol. 2013;35:93–98
6. Hayami H, Takahashi S, Ishikawa K, et al. Nationwide surveillance of bacterial pathogens from patients with acute uncomplicated cystitis conducted by the Japanese surveillance committee during 2009 and 2010: antimicrobial susceptibility of Escherichia coli and Staphylococcus saprophyticus. J Infect Chemother. 2013;19:393–403
7. Sousa VS, Rabello RF, Dias RC, et al. Time-based distribution of Staphylococcus saprophyticus pulsed field gel-electrophoresis clusters in community-acquired urinary tract infections. Mem Inst Oswaldo Cruz. 2013;108:73–76
8. Vincent CR, Thomas TL, Reyes L, et al. Symptoms and risk factors associated with first urinary tract infection in college age women: a prospective cohort study. J Urol. 2013;189:904–910
9. Oliveira-Campos M, Giatti L, Malta D, et al. Contextual factors associated with sexual behavior among Brazilian adolescents. Ann Epidemiol. 2013;23:629–635
10. . Ministério da Saúde. Proporção de nascidos vivos de mães adolescentes [DATASUS webside]. 2012 Available at: http://tabnet.datasus.gov.br/cgi/tabcgi.exe?idb2012/g15.def. Acessed February 11, 2015.
11. Hedman P, Ringertz O. Urinary tract infections caused by Staphylococcus saprophyticus. A matched case control study. J Infect. 1991;23:145–153
12. Hovelius B, Mårdh PA. Staphylococcus saprophyticus as a common cause of urinary tract infections. Rev Infect Dis. 1984;6:328–337
Keywords:

Staphylococcus saprophyticus; urinary tract infection; adolescent; Brazil

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