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Clinical significance of Staphylococcus saprophyticus identified on blood culture in a tertiary care hospital
Diagnostic Microbiology and Infectious Disease 56 (2006) 337 – 339 www.elsevier.com/locate/diagmicrobio
Clinical significance of Staphylococcus saprophyticus identified on blood culture in a tertiary care hospital Sang-Ho Choia, Jun Hee Wooa, Jin-Yong Jeonga, Nam Joong Kima, Mi-Na Kimb, Yang Soo Kima,4, Jiso Ryua a
Division of Infectious Diseases, Asan Medical Center, University of Ulsan College of Medicine, and Center for Antimicrobial Resistance and Microbial Genetics, University of Ulsan, Seoul 138-736, South Korea b Department of Laboratory Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul 138-736, South Korea Received 21 August 2006; accepted 21 August 2006
Abstract Staphylococcus saprophyticus is a well-known cause of acute uncomplicated urinary tract infection in young women. However, the clinical significance of this organism isolated from blood culture has not been determined. We assessed the clinical significance and characteristics of S. saprophyticus identified on blood culture. A total of 24 patients were identified, and 7 patients (29.2%) were considered to have clinically significant bacteremia. Of the 7 patients with clinically significant bacteremia, hematologic malignancy was the most common underlying illness (5 patients), and tunneled-central venous catheter was the most common portal of entry (4 patients). In no case did S. saprophyticus bacteremia originate from the urinary tract. One patient died during hospitalization. However, the death was not directly related to bacteremia. In conclusion, our data suggest that bacteremia caused by S. saprophyticus is most commonly associated with tunneled-central venous catheter in patients with hematologic malignancies and may be associated with a lower risk of mortality. D 2006 Elsevier Inc. All rights reserved. Keywords: Staphylococcus; Urinary tract infection; Bacteremia
Staphylococcus saprophyticus is a novobiocin-resistant, coagulase-negative Staphylococcus, which is second only to Escherichia coli as a causative organism of acute uncomplicated urinary tract infection in young women (Jordan et al., 1980; Latham et al., 1983; Pead et al., 1985; Wallmark et al., 1978), accounting for up to 42% of urinary tract infections in this population (Wallmark et al., 1978). However, the clinical significance of this organism when recovered from blood culture has not been determined. To date, only a few case reports of S. saprophyticus bacteremia have been reported (Glimaker et al., 1988; Golledge, 1988; Lee et al., 1987; Olafsen and Melby, 1986). In this study, we attempted to determine the significance and characteristics of S. saprophyticus identified on blood culture in a tertiary care hospital. We retrospectively reviewed the medical records of all patients between January 1997 and May 2004 at Asan Medical Center, a 2200-bed affiliated tertiary hospital 4 Corresponding author. Tel.: +82-23010-3303; fax: +82-3010-3303. E-mail address: [email protected] (Y.S. Kim). 0732-8893/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2006.08.012
(Seoul, Republic of Korea), in whom 1 or more blood cultures yielded S. saprophyticus. During this period, all blood cultures were processed by the hospital microbiology laboratory using a standard blood culturing system (BACTEC 9240; Becton Dickinson, Franklin Lakes, NJ). Antibiotic susceptibilities were determined by a MicroScan (Dade Behring, Deerfield, IL) system using standard criteria prescribed by the Clinical Laboratory Standards Institute. All Staphylococcus species isolated from blood culture were subspeciated using MicroScan Gram-positive combo panels (Dade Behring). S. saprophyticus blood isolates were considered significant if 2 or more separate blood cultures were positive and if systemic inflammatory response syndrome was present without any alternate explanation; that is, patients had to be shown to have at least 2 of the following 4 criteria: i) body temperature of N38.0 or b36 8C, ii) heart rate of N 90 beats per minute, iii) respiratory rate of N20 breaths per minute, and iv) peripheral white blood cells counts of N12 000/mm3 or N 10% bands (Bone et al., 1992). During the study period, 26 blood culture specimens from 24 patients were positive for S. saprophyticus,
338
S.-H. Choi et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 337 – 339
accounting for 0.12% of positive blood cultures and 5.98% of blood culture-positive, coagulase-negative staphylococci. Of these 24 patients, 15 underwent urine culture and concomitant urine analyses, and 2 underwent only urine culture. Only 3 patients had pyuria (= 6 white blood cells per high-power field). In no case was S. saprophyticus
identified on both blood and urine culture; that is, we observed no cases of urinary tract-origin bacteremia. Seven patients were considered to have clinically significant bacteremia, whereas the remaining 13 episodes were regarded as contamination. The clinical and microbiologic characteristics of patients with clinically significant
Table 1 Epidemiologic and clinical characteristics of patients with clinically significant S. saprophyticus bacteremia Case Sex/age Underlying no. (y) disease
Reason for admission
1
M/66
2
F/43
3
M/66
Non-Hodgkin’s Fever lymphoma associated with S. saprophyticus bacteremia
4
M/47
Acute myeloid leukemia
Consolidation chemotherapy
5
F/66
Chronic myeloid leukemia, mitral stenosis
Pulmonary edema
6
M/58
Esophageal cancer
Fever associated with S. saprophyticus bacteremia
7
M/41
Quadriparesis, s/p kidney transplantation
Multiple trauma
Multiple myeloma, chronic renal failure Chronic myeloid leukemia
Probable source of bacteremia
Susceptible antibiotics
Concomitant blood isolate
Recurrent bacteremia
Therapy (duration)
Outcome (cause of death)
Tunneled-central Tetracycline, Autologous stem cell venous catheter vancomycin transplantation
–
–
Vancomycin (11 days)
Recovered
Fever associated with S. saprophyticus bacteremia
S. epidermidis +
Tunneled-central Cephalothin, venous catheter ciprofloxacin, clindamycin, erythromycin, gentamicin, oxacillin, rifampin, tetracycline, trimethoprim/ sulfamethoxazole, vancomyin Tunneled-central Ciprofloxacin, venous catheter clindamycin, erythromycin, rifampin, tetracycline, trimethoprim/ sulfamethoxazole, vancomycin Tunneled-central Ciprofloxacin, venous catheter clindamycin, gentamicin, rifampin, tetracycline, trimethoprim/ sulfamethoxazole, vancomyin Unknown Cephalothin, ciprofloxacin, clindamycin, gentamicin, oxacillin, rifampin, trimethoprim/ sulfamethoxazole, vancomyin Unknown Ciprofloxacin, clindamycin, gentamicin, rifampin, trimethoprim/ sulfamethoxazole, vancomyin Unknown Ciprofloxacin, clindamycin, gentamicin, rifampin, trimethoprim/ sulfamethoxazole, vancomyin
–
Central Recovered catheter removal, no antimicrobial therapy
+ (with Central Klebsiella catheter pneumoniae) removal, vancomycin (9 days)
Recovered
S. epidermidis – plus A. lwoffii
Vancomycin (14 days)
Recovered
–
–
No therapy
Expired (aspiration pneumonia)
–
–
No therapy
Recovered
–
Repeat blood Vancomycin culture not (7 days) done
Recovered
S.-H. Choi et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 337 – 339
S. saprophyticus bacteremia are shown in Table 1. Hematologic malignancy was the most common underlying illness (5 patients), and 4 patients had tunneled-central venous catheters, which we considered as the probable sources of bacteremia. All isolates were susceptible to vancomycin and 5 were resistant to oxacillin. Two patients had polymicrobial bacteremia, with Staphylococcus epidermidis and S. epidermidis plus Acinetobacter lwoffii, respectively. Repeat blood cultures were performed in 6 patients. Two of these patients had recurrent bacteremia, requiring their tunneled-central venous catheters to be removed. None of the 7 patients with clinically significant bacteremia developed serious complications such as shock or secondary suppurative infection. Four patients received antimicrobial therapy with intravenous vancomycin. Although 1 patient died during hospitalization, death was not associated with S. saprophyticus bacteremia. During the past 2 decades, S. epidermidis and other coagulase-negative staphylococci have emerged as major causes of nosocomial infections. The pathogenic potential and clinical significance of S. saprophyticus in a hospital setting, however, have not been studied. To our knowledge, our study is the first describing bacteremia series caused by this organism. When confined to blood isolates, S. saprophyticus appears similar to other coagulase-negative staphylococci in that it is frequently regarded as a contaminant and often causes intravascular catheter-associated bacteremia. Interestingly, we did not identify any cases of non–tunneled venous catheter-associated bacteremia. Considering the fact that S. saprophyticus is regarded as an organism of low virulence, the prolonged presence of a tunneled catheter may offer more frequent opportunity for bacteremia than would a nontunneled catheter. S. saprophyticus has been shown to express several adhesion molecules, including surface-exposed 160-kDa protein (Gatermann et al., 1992b; Gatermann and Meyer, 1994) and 95-kDa surface-associated fibrillar protein (Gatermann et al., 1992a), which may explain the tropism for uroepithelium that has been reported. To date, however, little is known about the pathogenesis of infection associated with medical devices, such as intravascular catheters, and knowledge of the virulence determinants produced by this organism is still scarce. Further molecular and clinical investigations are required to clarify these issues.
339
It seems remarkable that no case of urinary tract-origin bacteremia was documented. Urinary tract infections caused by S. saprophyticus, however, only rarely lead to bacteremia. Furthermore, our study was performed in a tertiary care hospital, and thus included relatively few patients with community-acquired urinary tract infection due to S. saprophyticus. During the study period, a total of 71 urine cultures, including 23 samples from hospitalized patients, were positive for S. saprophyticus (data not shown), but none was associated with bacteremia. In summary, our results suggest that bacteremia caused by S. saprophyticus is most commonly associated with tunneled-central venous catheter in patients with hematologic malignancies and may be associated with a lower risk of mortality.
References Bone RC, Sibbald WJ, Sprung CL (1992) The ACCP-SCCM consensus conference on sepsis and organ failure. Chest 101:1481 – 1483. Gatermann S, Meyer HG (1994) Staphylococcus saprophyticus hemagglutinin binds fibronectin. Infect Immun 62:4556 – 4563. Gatermann S, Kreft B, Marre R, Wanner G (1992a) Identification and characterization of a surface-associated protein (Ssp) of Staphylococcus saprophyticus. Infect Immun 60:1055 – 1060. Gatermann S, Meyer HG, Wanner G (1992b) Staphylococcus saprophyticus hemagglutinin is a 160-kilodalton surface polypeptide. Infect Immun 60:4127 – 4132. Glimaker M, Granert C, Krook A (1988) Septicemia caused by Staphylococcus saprophyticus. Scand J Infect Dis 20:347 – 348. Golledge CL (1988) Staphylococcus saprophyticus bacteremia. J Infect Dis 157:215. Jordan PA, Iravani A, Richard GA, Baer H (1980) Urinary tract infection caused by Staphylococcus saprophyticus. J Infect Dis 142:510 – 515. Latham RH, Running K, Stamm WE (1983) Urinary tract infections in young adult women caused by Staphylococcus saprophyticus. JAMA 250:3063 – 3066. Lee W, Carpenter RJ, Phillips LE, Faro S (1987) Pyelonephritis and sepsis due to Staphylococcus saprophyticus. J Infect Dis 155:1079 – 1080. Olafsen LD, Melby K (1986) Urinary tract infection with septicaemia due to Staphylococcus saprophyticus in a patient with a ureteric calculus. J Infect 13:92 – 93. Pead L, Maskell R, Morris J (1985) Staphylococcus saprophyticus as a urinary pathogen: a six year prospective survey. BMJ (Clin Res Ed) 291:1157 – 1159. Wallmark G, Arremark I, Telander B (1978) Staphylococcus saprophyticus: a frequent cause of acute urinary tract infection among female outpatients. J Infect Dis 138:791 – 797.
Clinical significance of Staphylococcus saprophyticus identified on blood culture in a tertiary care hospital Sang-Ho Choia, Jun Hee Wooa, Jin-Yong Jeonga, Nam Joong Kima, Mi-Na Kimb, Yang Soo Kima,4, Jiso Ryua a
Division of Infectious Diseases, Asan Medical Center, University of Ulsan College of Medicine, and Center for Antimicrobial Resistance and Microbial Genetics, University of Ulsan, Seoul 138-736, South Korea b Department of Laboratory Medicine, Asan Medical Center, University of Ulsan College of Medicine, Seoul 138-736, South Korea Received 21 August 2006; accepted 21 August 2006
Abstract Staphylococcus saprophyticus is a well-known cause of acute uncomplicated urinary tract infection in young women. However, the clinical significance of this organism isolated from blood culture has not been determined. We assessed the clinical significance and characteristics of S. saprophyticus identified on blood culture. A total of 24 patients were identified, and 7 patients (29.2%) were considered to have clinically significant bacteremia. Of the 7 patients with clinically significant bacteremia, hematologic malignancy was the most common underlying illness (5 patients), and tunneled-central venous catheter was the most common portal of entry (4 patients). In no case did S. saprophyticus bacteremia originate from the urinary tract. One patient died during hospitalization. However, the death was not directly related to bacteremia. In conclusion, our data suggest that bacteremia caused by S. saprophyticus is most commonly associated with tunneled-central venous catheter in patients with hematologic malignancies and may be associated with a lower risk of mortality. D 2006 Elsevier Inc. All rights reserved. Keywords: Staphylococcus; Urinary tract infection; Bacteremia
Staphylococcus saprophyticus is a novobiocin-resistant, coagulase-negative Staphylococcus, which is second only to Escherichia coli as a causative organism of acute uncomplicated urinary tract infection in young women (Jordan et al., 1980; Latham et al., 1983; Pead et al., 1985; Wallmark et al., 1978), accounting for up to 42% of urinary tract infections in this population (Wallmark et al., 1978). However, the clinical significance of this organism when recovered from blood culture has not been determined. To date, only a few case reports of S. saprophyticus bacteremia have been reported (Glimaker et al., 1988; Golledge, 1988; Lee et al., 1987; Olafsen and Melby, 1986). In this study, we attempted to determine the significance and characteristics of S. saprophyticus identified on blood culture in a tertiary care hospital. We retrospectively reviewed the medical records of all patients between January 1997 and May 2004 at Asan Medical Center, a 2200-bed affiliated tertiary hospital 4 Corresponding author. Tel.: +82-23010-3303; fax: +82-3010-3303. E-mail address: [email protected] (Y.S. Kim). 0732-8893/$ – see front matter D 2006 Elsevier Inc. All rights reserved. doi:10.1016/j.diagmicrobio.2006.08.012
(Seoul, Republic of Korea), in whom 1 or more blood cultures yielded S. saprophyticus. During this period, all blood cultures were processed by the hospital microbiology laboratory using a standard blood culturing system (BACTEC 9240; Becton Dickinson, Franklin Lakes, NJ). Antibiotic susceptibilities were determined by a MicroScan (Dade Behring, Deerfield, IL) system using standard criteria prescribed by the Clinical Laboratory Standards Institute. All Staphylococcus species isolated from blood culture were subspeciated using MicroScan Gram-positive combo panels (Dade Behring). S. saprophyticus blood isolates were considered significant if 2 or more separate blood cultures were positive and if systemic inflammatory response syndrome was present without any alternate explanation; that is, patients had to be shown to have at least 2 of the following 4 criteria: i) body temperature of N38.0 or b36 8C, ii) heart rate of N 90 beats per minute, iii) respiratory rate of N20 breaths per minute, and iv) peripheral white blood cells counts of N12 000/mm3 or N 10% bands (Bone et al., 1992). During the study period, 26 blood culture specimens from 24 patients were positive for S. saprophyticus,
338
S.-H. Choi et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 337 – 339
accounting for 0.12% of positive blood cultures and 5.98% of blood culture-positive, coagulase-negative staphylococci. Of these 24 patients, 15 underwent urine culture and concomitant urine analyses, and 2 underwent only urine culture. Only 3 patients had pyuria (= 6 white blood cells per high-power field). In no case was S. saprophyticus
identified on both blood and urine culture; that is, we observed no cases of urinary tract-origin bacteremia. Seven patients were considered to have clinically significant bacteremia, whereas the remaining 13 episodes were regarded as contamination. The clinical and microbiologic characteristics of patients with clinically significant
Table 1 Epidemiologic and clinical characteristics of patients with clinically significant S. saprophyticus bacteremia Case Sex/age Underlying no. (y) disease
Reason for admission
1
M/66
2
F/43
3
M/66
Non-Hodgkin’s Fever lymphoma associated with S. saprophyticus bacteremia
4
M/47
Acute myeloid leukemia
Consolidation chemotherapy
5
F/66
Chronic myeloid leukemia, mitral stenosis
Pulmonary edema
6
M/58
Esophageal cancer
Fever associated with S. saprophyticus bacteremia
7
M/41
Quadriparesis, s/p kidney transplantation
Multiple trauma
Multiple myeloma, chronic renal failure Chronic myeloid leukemia
Probable source of bacteremia
Susceptible antibiotics
Concomitant blood isolate
Recurrent bacteremia
Therapy (duration)
Outcome (cause of death)
Tunneled-central Tetracycline, Autologous stem cell venous catheter vancomycin transplantation
–
–
Vancomycin (11 days)
Recovered
Fever associated with S. saprophyticus bacteremia
S. epidermidis +
Tunneled-central Cephalothin, venous catheter ciprofloxacin, clindamycin, erythromycin, gentamicin, oxacillin, rifampin, tetracycline, trimethoprim/ sulfamethoxazole, vancomyin Tunneled-central Ciprofloxacin, venous catheter clindamycin, erythromycin, rifampin, tetracycline, trimethoprim/ sulfamethoxazole, vancomycin Tunneled-central Ciprofloxacin, venous catheter clindamycin, gentamicin, rifampin, tetracycline, trimethoprim/ sulfamethoxazole, vancomyin Unknown Cephalothin, ciprofloxacin, clindamycin, gentamicin, oxacillin, rifampin, trimethoprim/ sulfamethoxazole, vancomyin Unknown Ciprofloxacin, clindamycin, gentamicin, rifampin, trimethoprim/ sulfamethoxazole, vancomyin Unknown Ciprofloxacin, clindamycin, gentamicin, rifampin, trimethoprim/ sulfamethoxazole, vancomyin
–
Central Recovered catheter removal, no antimicrobial therapy
+ (with Central Klebsiella catheter pneumoniae) removal, vancomycin (9 days)
Recovered
S. epidermidis – plus A. lwoffii
Vancomycin (14 days)
Recovered
–
–
No therapy
Expired (aspiration pneumonia)
–
–
No therapy
Recovered
–
Repeat blood Vancomycin culture not (7 days) done
Recovered
S.-H. Choi et al. / Diagnostic Microbiology and Infectious Disease 56 (2006) 337 – 339
S. saprophyticus bacteremia are shown in Table 1. Hematologic malignancy was the most common underlying illness (5 patients), and 4 patients had tunneled-central venous catheters, which we considered as the probable sources of bacteremia. All isolates were susceptible to vancomycin and 5 were resistant to oxacillin. Two patients had polymicrobial bacteremia, with Staphylococcus epidermidis and S. epidermidis plus Acinetobacter lwoffii, respectively. Repeat blood cultures were performed in 6 patients. Two of these patients had recurrent bacteremia, requiring their tunneled-central venous catheters to be removed. None of the 7 patients with clinically significant bacteremia developed serious complications such as shock or secondary suppurative infection. Four patients received antimicrobial therapy with intravenous vancomycin. Although 1 patient died during hospitalization, death was not associated with S. saprophyticus bacteremia. During the past 2 decades, S. epidermidis and other coagulase-negative staphylococci have emerged as major causes of nosocomial infections. The pathogenic potential and clinical significance of S. saprophyticus in a hospital setting, however, have not been studied. To our knowledge, our study is the first describing bacteremia series caused by this organism. When confined to blood isolates, S. saprophyticus appears similar to other coagulase-negative staphylococci in that it is frequently regarded as a contaminant and often causes intravascular catheter-associated bacteremia. Interestingly, we did not identify any cases of non–tunneled venous catheter-associated bacteremia. Considering the fact that S. saprophyticus is regarded as an organism of low virulence, the prolonged presence of a tunneled catheter may offer more frequent opportunity for bacteremia than would a nontunneled catheter. S. saprophyticus has been shown to express several adhesion molecules, including surface-exposed 160-kDa protein (Gatermann et al., 1992b; Gatermann and Meyer, 1994) and 95-kDa surface-associated fibrillar protein (Gatermann et al., 1992a), which may explain the tropism for uroepithelium that has been reported. To date, however, little is known about the pathogenesis of infection associated with medical devices, such as intravascular catheters, and knowledge of the virulence determinants produced by this organism is still scarce. Further molecular and clinical investigations are required to clarify these issues.
339
It seems remarkable that no case of urinary tract-origin bacteremia was documented. Urinary tract infections caused by S. saprophyticus, however, only rarely lead to bacteremia. Furthermore, our study was performed in a tertiary care hospital, and thus included relatively few patients with community-acquired urinary tract infection due to S. saprophyticus. During the study period, a total of 71 urine cultures, including 23 samples from hospitalized patients, were positive for S. saprophyticus (data not shown), but none was associated with bacteremia. In summary, our results suggest that bacteremia caused by S. saprophyticus is most commonly associated with tunneled-central venous catheter in patients with hematologic malignancies and may be associated with a lower risk of mortality.
References Bone RC, Sibbald WJ, Sprung CL (1992) The ACCP-SCCM consensus conference on sepsis and organ failure. Chest 101:1481 – 1483. Gatermann S, Meyer HG (1994) Staphylococcus saprophyticus hemagglutinin binds fibronectin. Infect Immun 62:4556 – 4563. Gatermann S, Kreft B, Marre R, Wanner G (1992a) Identification and characterization of a surface-associated protein (Ssp) of Staphylococcus saprophyticus. Infect Immun 60:1055 – 1060. Gatermann S, Meyer HG, Wanner G (1992b) Staphylococcus saprophyticus hemagglutinin is a 160-kilodalton surface polypeptide. Infect Immun 60:4127 – 4132. Glimaker M, Granert C, Krook A (1988) Septicemia caused by Staphylococcus saprophyticus. Scand J Infect Dis 20:347 – 348. Golledge CL (1988) Staphylococcus saprophyticus bacteremia. J Infect Dis 157:215. Jordan PA, Iravani A, Richard GA, Baer H (1980) Urinary tract infection caused by Staphylococcus saprophyticus. J Infect Dis 142:510 – 515. Latham RH, Running K, Stamm WE (1983) Urinary tract infections in young adult women caused by Staphylococcus saprophyticus. JAMA 250:3063 – 3066. Lee W, Carpenter RJ, Phillips LE, Faro S (1987) Pyelonephritis and sepsis due to Staphylococcus saprophyticus. J Infect Dis 155:1079 – 1080. Olafsen LD, Melby K (1986) Urinary tract infection with septicaemia due to Staphylococcus saprophyticus in a patient with a ureteric calculus. J Infect 13:92 – 93. Pead L, Maskell R, Morris J (1985) Staphylococcus saprophyticus as a urinary pathogen: a six year prospective survey. BMJ (Clin Res Ed) 291:1157 – 1159. Wallmark G, Arremark I, Telander B (1978) Staphylococcus saprophyticus: a frequent cause of acute urinary tract infection among female outpatients. J Infect Dis 138:791 – 797.