- Email: [email protected]
Urosepsis caused by Globicatella sanguinis and Corynebacterium riegelii in an adult: case report and literature review
J Infect Chemother (2012) 18:552–554 DOI 10.1007/s10156-011-0335-x
CASE REPORT
Urosepsis caused by Globicatella sanguinis and Corynebacterium riegelii in an adult: case report and literature review Masatoshi Matusnami • Yoshihito Otsuka • Kiyofumi Ohkusu • Misa Sogi • Hidetaka Kitazono Naoto Hosokawa
•
Received: 13 July 2011 / Accepted: 11 October 2011 / Published online: 12 November 2011 Ó Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases 2011
Keywords Globicatella sanguinis Corynebacterium riegelii Urinary tract infection
Corynebacterium, which was isolated from female patients with symptomatic urinary tract infections. It is nonlipophilic, weakly fermentative, facultatively anaerobic [5], and difficult to identify, and it may have been misidentified or unidentified in the past. Here we report a case of G. sanguinis and C. riegelii urinary tract coinfection in an adult who was diagnosed by 16S ribosomal RNA (rRNA) gene sequencing, and we present a literature review of this coinfection.
Introduction
Case report
Globicatella sanguinis was described in 1992 as a new genus and species of catalase-negative, facultatively anaerobic, nonmotile, nonhemolytic, gram-positive cocci [1–4]. There are few reports regarding Globicatella isolation in humans, and the clinical significance of this rarely encountered genus is unknown. G. sanguinis is part of the resident human flora in several mucosal surfaces. It has rarely been recorded from a human clinical specimen but has been described as an opportunistic invective agent [1]. C. riegelii was described in 1998 as a new species of
A 94-year-old Japanese man was admitted to our hospital with a 3-day history of back pain and fever. He was almost bed-bound and was cared for at home by his son before admission. He had dementia, hypertension, hyperlipidemia, and osteoporosis. His outpatient medications were donepezil hydrochloride, antihypertensive medication, and a calcium product orally. On examination, he had temperature of 38.4°C, blood pressure 126/86 mmHg, pulse 100 bpm, respiratory rate 16 breaths/min, and pulse oxygen saturation 93% on room air. He appeared lethargic. Physical examination showed left costovertebral angle tenderness. Laboratory data was leucocyte count 10,200/ll, C-reactive protein 9.5 mg/dl, hemoglobin level 10.7 g/dl, platelet count 271,000/ll, blood urea nitrogen 52 mg/dl, creatine 1.74 mg/dl, albumin 3.3 g/dl, alkaline phosphatase 247 IU/L, and alanine aminotransferase 14 IU/L. Urinary leukocyte count was [100 cells per high power field. Urinary gram stain showed gram-positive coccus in chain. Abdominal computed tomography (CT) revealed an obstructing urinary stone in the left ureter, with hydronephrosis. Blood cultures from the date of admission yielded growth of gram-positive cocci in chains
Abstract We report an extremely rare case of urosepsis caused by Globicatella sanguinis and Corynebacterium riegelii coinfection in a 94-year-old Japanese man with nephrolithiasis. Prompt identification of this coinfection is important so that effective antimicrobial coverage can be initiated.
M. Matusnami (&) M. Sogi H. Kitazono N. Hosokawa Department of General Internal Medicine and Infectious Diseases, Kameda Medical Center, 929 Higashi-cho, Kamogawa, Chiba 296-8602, Japan e-mail: [email protected] Y. Otsuka Department of Laboratory Medicine, Kameda Medical Center, Kamogawa, Japan K. Ohkusu Department of Microbiology, Gifu University Graduate School of Medicine, Gifu, Japan
123
J Infect Chemother (2012) 18:552–554
553
in two of four bottles, eventually identified as G. sanguinis, and yielded coryneform gram-positive rod in one of four bottles, eventually identified as C. riegelii. Identification details are described below. Urine culture showed the same two bacteria. Antimicrobial susceptibility testing on both organisms showed susceptibility to penicillin (Table 1). The patient was initially treated empirically with ampicillin/sulbactam and then switched to vancomycin when the blood cultures showed gram-positive organisms. Once the susceptibility was available, vancomycin was replaced with penicillin G. The patient received a total of three weeks of therapy, recovered, and was discharged in good condition. He has been followed up at our clinic and has no sign of recurrence 1 year later. Table 1 Antibiotic-susceptibility testing of the clinical isolate strains for blood culture using the microbroth dilution test Antibiotics
Range (MIC: lg/ml)
Corynebacterium riegelii (MIC: lg/ml)
Penicillin G
0.06–8
Ampicillin
0.25–16
B0.25
Cefazolin
0.5–16
1
[16
Cefotiam
2.0–8
B2.0
[8
Ceftriaxone
1.0–32
B1.0
4
0.12
Globicatella sanguinis (MIC: lg/ml)
B0.25
0.12–8
B0.12
0.5
Erythromycin
0.25–4
[4
B0.25
Clarithromycin
0.5–8
[8
B0.5
Amikacin
1.0–32
B1.0
4
Levofloxacin
0.5–4
[4
[4
Minocycline
2.0–8
B2.0
B2.0
Vancomycin
0.5–16
B0.5
B0.5
[2
0.5
B0.5 B2.0
B0.5 B2.0
Teicoplanin Linezolid
0.25–2 0.5–16 2.0–4
We describe a case of G. sanguinis and C. riegelii urosepsis characterized by 16S rRNA gene sequencing. G. sanguinis was first described in 1992 by Collins and coworkers, who named it G. sanguis. It was renamed G. sanguinis in 1997 by Truper and de’ Clare [1, 2]. These bacteria have been isolated from blood cultures of patients with bacteremia, urine of patients with urinary tract infections, and cerebrospinal fluid of a patient with meningitis, but the clinical details were not described [1–4]. There are four reports of G. sanguinis [1–4] (Table 2). The reported patient age range was from 23 to 92 years. Of patients in these reports, six were women and only one was a man. Only two cases were urinary tract infection: one of them was in a 92-year-old woman with acute pyelonephritis underlying dementia [3], and the other was an
MIC minimum inhibitory concentration
Table 2 Reported cases of Globicatella sanguinis infection
ND no data
We could not identify the two pathogens using the routine automatic identification system (Walkaway by SIEMENS). Further analysis on the gram-positive cocci using the API 20 STREP V7.0 (bioMe´rieux) reported possible Aerococcus viridans, but with the probability of only 69.7%. This result was felt to be unreliable. Further analysis on the gram-positive rod using RapIDTM CB Plus (remel) reported C. pseudotuberculosis with the probability of [99.9%. However, the colony appearance on the isolated grampositive rod ([1.0-mm diameter and cream-colored) was different from the typical colony appearance of C. pseudotuberculosis (approximately 0.5-mm diameter). Thus, the result was felt to be unreliable. We then performed 16S ribosomal RNA (rRNA) gene sequencing [9], which has become the gold standard for for this purpose. Gene sequencing was performed at Gifu University Graduate School of Medicine, Department of Microbiology.
Discussion
0.25
Meropenem
Clindamycin
Identification
Reference
Age
Sex
Underlying disease
Clinical diagnosis
Treatment
Outcome
Abdul et al. [1]
23
F
Hepatitis C
Endocarditis
Cefuroxime
Recovered
Abdul et al. [1]
82
F
Alzheimer’s disease
UTI
Penicillin
Recovered
Abdul et al. [1] Seegmu¨ller et al. [2]
56
M
Crohn’s disease
Erysipelas
Cefuroxime
Recovered
69
F
Hydrocephalus
Meningitis
Ceftriaxone
Recovered
Lau et al. [3]
80
F
Gouty arthritis
Nosocomial sepsis
ND
Died
Lau et al. [3] He´ry et al. [4]
92
F
Dementia
UTI
Antibiotic
Recovered
56
F
ND
Meningitis
Cefotaxime, fosfomycin
Recovered
123
554
J Infect Chemother (2012) 18:552–554
Table 3 Reported cases of Corynebacterium riegelii infection Reference
Age
Sex
Underlying disease
Clinical diagnosis
Treatment
Outcome
Funke et al. [5]
21–62
F
None
UTI
ND
ND
Verdaguer et al. [7]
80
F
Ischemic heart disease
UTI
Fosfomycin
Recovered
Ferrer et al. [8]
39
M
Down syndrome
UTI
Amoxicillin-clavulanate
Recovered
UTI urinary tract infection, ND no data
82-year-old woman with urosepticemia underlying Alzheimer’s disease [1]. One case, a patient aged 80 years, was complicated with sepsis underlying gouty arthritis, and the patient died of bacteremia [3]. Two cases were meningitis [2, 4], one was endocarditis [1], and one erysipelas [1]. C. riegelii was first described in 1998 by Funke et al. [5] in female patients with symptomatic urinary tract infection. This bacterium is nonlipophilic, weakly fermentative, and facultatively anaerobic. Similar to the lipophilic C. urealyticum, it demonstrates strong urease activity. Coryneform bacteria are widely distributed in the environment as normal inhabitants of soil and water. They are commensals colonizing the skin and mucous membranes of humans and other animals [6]. There are three reports of C. riegelii causing urinary tract infection [5, 7, 8] (Table 3); two are in Spanish. In our patient, both species were isolated on both blood and urine culture. Here we report the first case of urosepsis in an elderly man that was caused by the two uncommon pathogens G. sanguinis and C. riegelii. As G. sanguinis and C. riegelii are rarely encountered in clinical laboratories, most technicians and microbiologists are not familiar with their phenotypic characteristics how to identify them. As a result, the bacteria may be overlooked when isolated or may be reported as unidentified Streptococcus-like organisms. Sequencing of the 16S rRNA gene is useful for identifying rarely encountered bacteria or those that are difficult to identify by traditional biochemical techniques. As polymerase chain reaction (PCR) and sequencing techniques are becoming more readily available in clinical laboratories, we may more often find these two previously ‘‘uncommon’’ organisms in clinical specimens. Further studies are required to
123
investigate the pathogenesis and risk factors of G. sanguinis and C. riegelii in infections in humans. Acknowledgments We are grateful for the diligent and thorough critical reading of our manuscript by David H. Gremillion, M.D. FACP, professor in residence, Kameda Medical Center (Japan).
References 1. Abdul-Redha RJ, Balslew U, Christensen JJ, Kemp M. Globicatella sanguinis bacteraemia identified by partial 16S rRNA gene sequencing. Scand J Infect Dis. 2007;39:745–8. 2. Seegmuller I, van der Linden M, Heeg C, Reinert RR. Globicatella sanguinis is an etiological agent of ventriculoperitoneal shuntassociated meningitis. J Clin Microbiol. 2007;45:666–7. 3. Lau SK, Woo PC, Li NK, Teng JL, Leung KW, Ng KH, et al. Globicatella bacteraemia identified by 16S ribosomal RNA gene sequencing. J Clin Pathol. 2006;59:303–7. 4. He´ry-Arnaud G, Doloy A, Ansart S, Le Lay G, Le Fle`che-Mate´os A, Seizeur R, et al. Globicatella sanguinis meningitis associated with human carriage. J Clin Microbiol. 2010;48:1491–3. 5. Funke G, Lawson PA, Collins MD. Corynebacterium riegelii sp. nov., an unusual species isolated from female patients with urinary tract infections. J Clin Microbiol. 1998;36:624–7. 6. von Graevenitz A, Pu¨nter-Streit V, Riegel P, Funke G. Coryneform bacteria in throat cultures of healthy individuals. J Clin Microbiol. 1998;36:2087–8. 7. Verdaguer R, Tubau F, Va´zquez Z, Lucena J. Urinary tract infection caused by Corynebacterium riegelii. Enferm Infecc Microbiol Clin. 2008;26:669–70 (in Spanish). 8. Ferrer I, Marne C, Jose´ Revillo M, Isabel Lo´pez A, Jose´ Velasco J, Bautista Garcı´a-Moya J. Corynebacterium riegelii urinary tract infection. Enferm Infecc Microbiol Clin. 2001;19:284–5 (in Spanish). 9. Otsuka Y, Kawamura Y, Koyama T, Iihara H, Ohkusu K, Ezaki T. Corynebacterium resistens sp. nov., a new multidrug-resistant coryneform bacterium isolated from human infections. J Clin Microbiol. 2005;43:3713–7.
CASE REPORT
Urosepsis caused by Globicatella sanguinis and Corynebacterium riegelii in an adult: case report and literature review Masatoshi Matusnami • Yoshihito Otsuka • Kiyofumi Ohkusu • Misa Sogi • Hidetaka Kitazono Naoto Hosokawa
•
Received: 13 July 2011 / Accepted: 11 October 2011 / Published online: 12 November 2011 Ó Japanese Society of Chemotherapy and The Japanese Association for Infectious Diseases 2011
Keywords Globicatella sanguinis Corynebacterium riegelii Urinary tract infection
Corynebacterium, which was isolated from female patients with symptomatic urinary tract infections. It is nonlipophilic, weakly fermentative, facultatively anaerobic [5], and difficult to identify, and it may have been misidentified or unidentified in the past. Here we report a case of G. sanguinis and C. riegelii urinary tract coinfection in an adult who was diagnosed by 16S ribosomal RNA (rRNA) gene sequencing, and we present a literature review of this coinfection.
Introduction
Case report
Globicatella sanguinis was described in 1992 as a new genus and species of catalase-negative, facultatively anaerobic, nonmotile, nonhemolytic, gram-positive cocci [1–4]. There are few reports regarding Globicatella isolation in humans, and the clinical significance of this rarely encountered genus is unknown. G. sanguinis is part of the resident human flora in several mucosal surfaces. It has rarely been recorded from a human clinical specimen but has been described as an opportunistic invective agent [1]. C. riegelii was described in 1998 as a new species of
A 94-year-old Japanese man was admitted to our hospital with a 3-day history of back pain and fever. He was almost bed-bound and was cared for at home by his son before admission. He had dementia, hypertension, hyperlipidemia, and osteoporosis. His outpatient medications were donepezil hydrochloride, antihypertensive medication, and a calcium product orally. On examination, he had temperature of 38.4°C, blood pressure 126/86 mmHg, pulse 100 bpm, respiratory rate 16 breaths/min, and pulse oxygen saturation 93% on room air. He appeared lethargic. Physical examination showed left costovertebral angle tenderness. Laboratory data was leucocyte count 10,200/ll, C-reactive protein 9.5 mg/dl, hemoglobin level 10.7 g/dl, platelet count 271,000/ll, blood urea nitrogen 52 mg/dl, creatine 1.74 mg/dl, albumin 3.3 g/dl, alkaline phosphatase 247 IU/L, and alanine aminotransferase 14 IU/L. Urinary leukocyte count was [100 cells per high power field. Urinary gram stain showed gram-positive coccus in chain. Abdominal computed tomography (CT) revealed an obstructing urinary stone in the left ureter, with hydronephrosis. Blood cultures from the date of admission yielded growth of gram-positive cocci in chains
Abstract We report an extremely rare case of urosepsis caused by Globicatella sanguinis and Corynebacterium riegelii coinfection in a 94-year-old Japanese man with nephrolithiasis. Prompt identification of this coinfection is important so that effective antimicrobial coverage can be initiated.
M. Matusnami (&) M. Sogi H. Kitazono N. Hosokawa Department of General Internal Medicine and Infectious Diseases, Kameda Medical Center, 929 Higashi-cho, Kamogawa, Chiba 296-8602, Japan e-mail: [email protected] Y. Otsuka Department of Laboratory Medicine, Kameda Medical Center, Kamogawa, Japan K. Ohkusu Department of Microbiology, Gifu University Graduate School of Medicine, Gifu, Japan
123
J Infect Chemother (2012) 18:552–554
553
in two of four bottles, eventually identified as G. sanguinis, and yielded coryneform gram-positive rod in one of four bottles, eventually identified as C. riegelii. Identification details are described below. Urine culture showed the same two bacteria. Antimicrobial susceptibility testing on both organisms showed susceptibility to penicillin (Table 1). The patient was initially treated empirically with ampicillin/sulbactam and then switched to vancomycin when the blood cultures showed gram-positive organisms. Once the susceptibility was available, vancomycin was replaced with penicillin G. The patient received a total of three weeks of therapy, recovered, and was discharged in good condition. He has been followed up at our clinic and has no sign of recurrence 1 year later. Table 1 Antibiotic-susceptibility testing of the clinical isolate strains for blood culture using the microbroth dilution test Antibiotics
Range (MIC: lg/ml)
Corynebacterium riegelii (MIC: lg/ml)
Penicillin G
0.06–8
Ampicillin
0.25–16
B0.25
Cefazolin
0.5–16
1
[16
Cefotiam
2.0–8
B2.0
[8
Ceftriaxone
1.0–32
B1.0
4
0.12
Globicatella sanguinis (MIC: lg/ml)
B0.25
0.12–8
B0.12
0.5
Erythromycin
0.25–4
[4
B0.25
Clarithromycin
0.5–8
[8
B0.5
Amikacin
1.0–32
B1.0
4
Levofloxacin
0.5–4
[4
[4
Minocycline
2.0–8
B2.0
B2.0
Vancomycin
0.5–16
B0.5
B0.5
[2
0.5
B0.5 B2.0
B0.5 B2.0
Teicoplanin Linezolid
0.25–2 0.5–16 2.0–4
We describe a case of G. sanguinis and C. riegelii urosepsis characterized by 16S rRNA gene sequencing. G. sanguinis was first described in 1992 by Collins and coworkers, who named it G. sanguis. It was renamed G. sanguinis in 1997 by Truper and de’ Clare [1, 2]. These bacteria have been isolated from blood cultures of patients with bacteremia, urine of patients with urinary tract infections, and cerebrospinal fluid of a patient with meningitis, but the clinical details were not described [1–4]. There are four reports of G. sanguinis [1–4] (Table 2). The reported patient age range was from 23 to 92 years. Of patients in these reports, six were women and only one was a man. Only two cases were urinary tract infection: one of them was in a 92-year-old woman with acute pyelonephritis underlying dementia [3], and the other was an
MIC minimum inhibitory concentration
Table 2 Reported cases of Globicatella sanguinis infection
ND no data
We could not identify the two pathogens using the routine automatic identification system (Walkaway by SIEMENS). Further analysis on the gram-positive cocci using the API 20 STREP V7.0 (bioMe´rieux) reported possible Aerococcus viridans, but with the probability of only 69.7%. This result was felt to be unreliable. Further analysis on the gram-positive rod using RapIDTM CB Plus (remel) reported C. pseudotuberculosis with the probability of [99.9%. However, the colony appearance on the isolated grampositive rod ([1.0-mm diameter and cream-colored) was different from the typical colony appearance of C. pseudotuberculosis (approximately 0.5-mm diameter). Thus, the result was felt to be unreliable. We then performed 16S ribosomal RNA (rRNA) gene sequencing [9], which has become the gold standard for for this purpose. Gene sequencing was performed at Gifu University Graduate School of Medicine, Department of Microbiology.
Discussion
0.25
Meropenem
Clindamycin
Identification
Reference
Age
Sex
Underlying disease
Clinical diagnosis
Treatment
Outcome
Abdul et al. [1]
23
F
Hepatitis C
Endocarditis
Cefuroxime
Recovered
Abdul et al. [1]
82
F
Alzheimer’s disease
UTI
Penicillin
Recovered
Abdul et al. [1] Seegmu¨ller et al. [2]
56
M
Crohn’s disease
Erysipelas
Cefuroxime
Recovered
69
F
Hydrocephalus
Meningitis
Ceftriaxone
Recovered
Lau et al. [3]
80
F
Gouty arthritis
Nosocomial sepsis
ND
Died
Lau et al. [3] He´ry et al. [4]
92
F
Dementia
UTI
Antibiotic
Recovered
56
F
ND
Meningitis
Cefotaxime, fosfomycin
Recovered
123
554
J Infect Chemother (2012) 18:552–554
Table 3 Reported cases of Corynebacterium riegelii infection Reference
Age
Sex
Underlying disease
Clinical diagnosis
Treatment
Outcome
Funke et al. [5]
21–62
F
None
UTI
ND
ND
Verdaguer et al. [7]
80
F
Ischemic heart disease
UTI
Fosfomycin
Recovered
Ferrer et al. [8]
39
M
Down syndrome
UTI
Amoxicillin-clavulanate
Recovered
UTI urinary tract infection, ND no data
82-year-old woman with urosepticemia underlying Alzheimer’s disease [1]. One case, a patient aged 80 years, was complicated with sepsis underlying gouty arthritis, and the patient died of bacteremia [3]. Two cases were meningitis [2, 4], one was endocarditis [1], and one erysipelas [1]. C. riegelii was first described in 1998 by Funke et al. [5] in female patients with symptomatic urinary tract infection. This bacterium is nonlipophilic, weakly fermentative, and facultatively anaerobic. Similar to the lipophilic C. urealyticum, it demonstrates strong urease activity. Coryneform bacteria are widely distributed in the environment as normal inhabitants of soil and water. They are commensals colonizing the skin and mucous membranes of humans and other animals [6]. There are three reports of C. riegelii causing urinary tract infection [5, 7, 8] (Table 3); two are in Spanish. In our patient, both species were isolated on both blood and urine culture. Here we report the first case of urosepsis in an elderly man that was caused by the two uncommon pathogens G. sanguinis and C. riegelii. As G. sanguinis and C. riegelii are rarely encountered in clinical laboratories, most technicians and microbiologists are not familiar with their phenotypic characteristics how to identify them. As a result, the bacteria may be overlooked when isolated or may be reported as unidentified Streptococcus-like organisms. Sequencing of the 16S rRNA gene is useful for identifying rarely encountered bacteria or those that are difficult to identify by traditional biochemical techniques. As polymerase chain reaction (PCR) and sequencing techniques are becoming more readily available in clinical laboratories, we may more often find these two previously ‘‘uncommon’’ organisms in clinical specimens. Further studies are required to
123
investigate the pathogenesis and risk factors of G. sanguinis and C. riegelii in infections in humans. Acknowledgments We are grateful for the diligent and thorough critical reading of our manuscript by David H. Gremillion, M.D. FACP, professor in residence, Kameda Medical Center (Japan).
References 1. Abdul-Redha RJ, Balslew U, Christensen JJ, Kemp M. Globicatella sanguinis bacteraemia identified by partial 16S rRNA gene sequencing. Scand J Infect Dis. 2007;39:745–8. 2. Seegmuller I, van der Linden M, Heeg C, Reinert RR. Globicatella sanguinis is an etiological agent of ventriculoperitoneal shuntassociated meningitis. J Clin Microbiol. 2007;45:666–7. 3. Lau SK, Woo PC, Li NK, Teng JL, Leung KW, Ng KH, et al. Globicatella bacteraemia identified by 16S ribosomal RNA gene sequencing. J Clin Pathol. 2006;59:303–7. 4. He´ry-Arnaud G, Doloy A, Ansart S, Le Lay G, Le Fle`che-Mate´os A, Seizeur R, et al. Globicatella sanguinis meningitis associated with human carriage. J Clin Microbiol. 2010;48:1491–3. 5. Funke G, Lawson PA, Collins MD. Corynebacterium riegelii sp. nov., an unusual species isolated from female patients with urinary tract infections. J Clin Microbiol. 1998;36:624–7. 6. von Graevenitz A, Pu¨nter-Streit V, Riegel P, Funke G. Coryneform bacteria in throat cultures of healthy individuals. J Clin Microbiol. 1998;36:2087–8. 7. Verdaguer R, Tubau F, Va´zquez Z, Lucena J. Urinary tract infection caused by Corynebacterium riegelii. Enferm Infecc Microbiol Clin. 2008;26:669–70 (in Spanish). 8. Ferrer I, Marne C, Jose´ Revillo M, Isabel Lo´pez A, Jose´ Velasco J, Bautista Garcı´a-Moya J. Corynebacterium riegelii urinary tract infection. Enferm Infecc Microbiol Clin. 2001;19:284–5 (in Spanish). 9. Otsuka Y, Kawamura Y, Koyama T, Iihara H, Ohkusu K, Ezaki T. Corynebacterium resistens sp. nov., a new multidrug-resistant coryneform bacterium isolated from human infections. J Clin Microbiol. 2005;43:3713–7.