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The first case report of emphysematous pyelonephritis and bacteremia due to Oligella urethralis
Accepted Manuscript Title: The First Case Report of Emphysematous Pyelonephritis and Bacteremia Due to Oligella urethralis Authors: Hirotaka Yamaguchi, Yukihiro Yamaguchi, Yoshiro Hadano, Kenichi Hayashi, Chie Nagahara, Tetsuro Muratani, Kiyofumi Ohkusu PII: DOI: Reference:
S1438-4221(16)30286-7 http://dx.doi.org/doi:10.1016/j.ijmm.2017.01.004 IJMM 51107
To appear in: Received date: Revised date:
30-9-2016 12-12-2016
Please cite this article as: Yamaguchi, Hirotaka, Yamaguchi, Yukihiro, Hadano, Yoshiro, Hayashi, Kenichi, Nagahara, Chie, Muratani, Tetsuro, Ohkusu, Kiyofumi, The First Case Report of Emphysematous Pyelonephritis and Bacteremia Due to Oligella urethralis.International Journal of Medical Microbiology http://dx.doi.org/10.1016/j.ijmm.2017.01.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Title The First Case Report of Emphysematous Pyelonephritis and Bacteremia Due to Oligella urethralis.
Hirotaka Yamaguchi a, Yukihiro Yamaguchi
a c
, Yoshiro Hadano a, Kenichi Hayashi a, Chie Nagahara e,
Tetsuro Muratani d, Kiyofumi Ohkusu b
a.
Division of Infectious Diseases, Kenwakai Otemachi Hospital, Kitakyushu, Japan
b
Department of Microbiology, Tokyo Medical University, Tokyo, Japan
c
KRICT (Kitakyushu Regional Infection Control Team)
d
Kyurin Medical Laboratory, Kitakyushu, Japan
e
Department of Microbiology, Kenwakai Otemachi Hospital, Kitakyushu, Japan
Correspondence to Dr. Hirotaka Yamaguchi, [email protected]
Abstract Oligella urethralis (O. urethralis) is an organism that rarely causes infections in humans. We report the case of a 90-year-old bedridden woman with progressive dementia who was placed in a long-term-care facility. She was admitted to our hospital due to fever and unconsciousness with pyuria. The abdominal computed tomography showed left pneumatosis and urinary stone. Fluoroquinolones-resistant O. urethralis, which was identified by the Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry (MALDI-TOF MS) and the 16S rRNA gene sequencing, was isolated form the blood and urine cultures at admission. To the best of our knowledge, this is the first case of emphysematous pyelonephritis caused by O. urethralis.
Keywords Oligella urethralis (O. urethralis); emphysematous pyelonephritis; rare causative organism; rare species; Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry (MALDI-TOF MS); 16S rRNA gene sequencing
1. Introduction O. urethralis is a Gram-negative rod, aerobic, oxidase-positive, non-fermentative, formerly of the genus Moraxella, which has been isolated mainly from urine and the female genital tract, considered to be of low
virulence (Pugliese et al., 1993; Escobar et al., 2001; Catala et al., 2001; Abdolrasouli et al., 2006; Mesnard et al., 1992; Riley et al., 1996; Murase et al., 2015). Additionally, emphysematous pyelonephritis is an acute severe necrotizing infection of the renal parenchyma and its surrounding tissues that result in the presence of gas in the renal parenchyma, collecting system, or perinephric tissues (Ubee et al., 2011). Up to 95 % of the cases with emphysematous pyelonephritis have underlying uncontrolled diabetes mellitus and enterobacteriaceae is the most common causative pathogen in the previous reported cases (Ubee et al., 2011). In this report, we describe the first case of an emphysematous pyelonephritis caused by O. urethralis.
2. Case Report A 90-year-old Japanese woman with diabetes mellitus without insulin therapy was admitted to our hospital because of a single-day fever and impaired consciousness. Her temperature was 38.0℃, pulse rate was 130 beats per minute and regular, systolic blood pressure was 70mmHg and respiratory rate was 30 breaths per minute on room air. Physical examination was unremarkable except for the disturbance of consciousness. In the Emergency department, blood cultures were collected and meropenem was administered under a diagnosis of septic shock with unknown focus. Laboratory data obtained on the admission revealed a white blood cell count of 7,800/μL with 92.3% neutrophils, 4.4% lymphocytes, and 2.2% monocytes. Hemoglobin was 9.8 mg/dL with an MCV of 91.3 fL. Platelet count was 412,000/μL. Serum chemistries revealed sodium of 143 mEq/L, potassium 6.5 mEq/L,
chloride 113 mEq/L, blood urea nitrogen (BUN) 101 mg/dL, creatinine 1.5 mg/dL, glucose 998 mg/dL, albumin 2.2 g/dL, AST 18 IU/L, ALT 11 IU/L, total bilirubin 0.4 mg/dL, LDH 173 IU/L, CRP 8.5 mg/dL, and HbA1c 7.9 %. Her clean-catch urine which was collected by catheterization showed many WBCs and bacteria under high power. Chest radiography showed no evidence of acute pulmonary disease. The computed tomography of abdomen revealed severe hydronephrosis and pneumatosis with renal stones in the left kidney, and pneumatosis cystoides intestinalis with emphysema in portal vein (Fig. 1). A diagnosis of urosepsis secondary to emphysematous pyelonephritis was made. Expeditiously, ureteral stents were inserted to both urinary ducts. Although exploratory laparotomy was done to rule out the small intestinal necrosis, the findings of the operation were intact. After the surgical interventions, the primary team changed meropenem to cefmetazole 1g every 12 hours. On third hospital day, infectious disease specialist was consulted. Because the patient was still septic shock at that time, cefmetazole was switched to meropenem 1g every 12 hours for three days to cover rare gram-negative bacillus and anaerobes. On forth hospital day, blood cultures became positive for gram-negative rod. Her symptoms improved on the sixth hospital day. We changed meropenem to cefmetazole 1g every 12 hours for additional six days.
3. Microbiology One set of blood cultures and the urine cultures from both the ureteral stents yielded gram-negative rod, we show the colony on the 5% sheep blood and Drigalski agar of the blood culture (Fig. 2). Although precise identification of the bacteria was difficult using MicroScan Walkaway 96 Plus (Beckman Coulter, Tokyo,
Japan), which was identified by the BACTEC (Nippon Becton Dickinson, Tokyo, Japan). The gram-negative rod was identified Oligella urethralis by MALDI-TOF MS (VITEK-MS™, Sysmex bioMérieux, Tokyo Japan) and its confidence value of identification was 99.9%. In addition, we performed molecular identification by PCR amplification and sequencing analysis of the 16S rRNA gene using DNA extracted from the isolate of blood culture. The sequence of the 16S rRNA gene was 99.9% identical (1,401 bp over the entire 1,402 bp fragment) with the type strain of O. urethralis. (ATCC 17960, accession number AF227163). Based on these results, we identified the isolate as O. urethralis. The susceptibilities of all O. urethralis of this case were similar. The minimum inhibitory concentrations (MICs) showed that the isolates of the blood and urine culture were susceptible to ampicillin (<=0.5mg/l), ceftriaxone (<=0.5mg/l), meropenem (<=0.25mg/l), clarithromycin (<=8mg/l), minocycline (<=1mg/l), sulfamethoxazole/trimethoprim (<=10mg/l) and resistant to levofloxacin (>4mg/l), garenoxacin (>4mg/l) and tosufloxacin (>2mg/l).
4. Discussion There have been case reports of O. urethralis causing bacteremia (Pugliese et al., 1993; Mesnard et al., 1992; Murase et al., 2015), urinary tract infection (Pugliese et al., 1993; Escobar et al., 2001; Abdolrasouli et al., 2006; Murase et al., 2015), chronic ambulatory peritoneal dialysis (CAPD) peritonitis (Riley et al., 1996), septic arthritis (Mesnard et al., 1992) and genital infection (Catala et al., 2001). The low virulence of this organism may contribute to the paucity of recognized cases but Oligella spp. can be misidentified as
phenotypically similar organisms, such as Bordetella bronchiseptica and Achromobacter spp.. Some cases may also have been dismissed as contamination because of laboratorians’ and clinicians’ lack of familiarity with this bacterium (Simmons et al., 2015). Emphysematous pyelonephritis is a severe, necrotizing form of acute bacterial pyelonephritis with underlying uncontrolled diabetes mellitus (Ubee et al., 2011; Huang et al., 2000). Previous report cases show that Escherichia coli is the most common pathogen in nearly 70% of emphysematous pyelonephritis, followed by Proteus mirabilis, Klebsiella pneumoniae, Group D Streptococcus, and coagulase-negative Staphylococcus (Ubee et al., 2011; Huang et al., 2000). O. urethralis has not been reported as the causative organism of emphysematous pyelonephritis. O. urethralis is usually susceptible to beta-lactam antibiotics, but beta-lactamase-producing strains, as well as strains resistant to fluoroquinolones, have been reported (Mammeri et al., 2003). In this case, the isolate was resistant to levofloxacin, garenoxacin and tosufloxacin, but susceptible to other antimicrobial agents including ampicillin and ceftriaxone. In the present day, levofloxacin has been widely used and our patient had received levofloxacin on previous occasions. In the last two months, the patient was prescribed two periods of levofloxacin by primary care doctors of the long-term-care facility. Quinolone resistance in O. urethralis has been also described for a case of an infection leading to chronic ambulatory peritoneal dialysis peritonitis (Riley et al., 1996), in this case, previous levofloxacin usage may have caused the resistance to quinolone.
In conclusion, we report here a case of emphysematous pyelonephritis and bacteremia caused by O. urethralis and successful control of the infection with antibiotic therapy and intervention to both urinary ducts. To the best of our knowledge, this is the first case of emphysematous pyelonephritis caused by O. urethralis reported. The causative organism was identified by MALDI-TOF MS and the 16S rRNA gene sequencing. O. urethralis is known to be a commensal of the human genitourinary tract, and rarely pathogenic for humans (Murase et al., 2015). However, we believe that this organism is a potential opportunistic pathogen for the elderly, especially in patients with diabetes and obstruction of the urinary tract (i.e., renal stones and disorder of urination).
Acknowledgement We would like to thank Brannon Raney for his support in the preparation of this manuscript.
References 1.
Pugliese A, Pacris B, Schoch PE, Cunha BA., 1993. Oligella urethralis urosepsis. Clin Infect Dis. 17, 1069-70.
2.
Escobar Mora S, Marne Trapero C, Gascón Val M, López Calleja AI., 2001. Infección urinaria por Oligella urethralis. Atención Primaria. 30, 620-3.
3.
Catala A, Simha V, Guillotel B, Rousseau MC., 2001. Genital infection with Oligella urethralis. La Presse Medicale. 30, 1007-8.
4.
Abdolrasouli A, Aligholi M, Hemmati Y., 2006. Quinolone Resistance in Oligella Urethralis-Associated Urinary Tract Infection. Iranian J Phamacol Ther. 5, 83-5.
5.
Mesnard R, Sire JM, Donnio PY, Riou JY, Avril JL., 1992. Septic arthritis due to Oligella urethralis. Eur J Clin Microbiol Infect Dis. 11, 195-6.
6.
Riley UB, Bignardi G, Goldberg L, Johnson AP, Holmes B., 1996. Quinolone resistance in Oligella urethralis-associated chronic ambulatory peritoneal dialysis peritonitis. J Infect. 32, 155-6.
7.
Mammeri H, Poirel L, Mangeney N, Nordmann P., 2003. Chromosomal integration of a cephalosporinase gene from Acinetobacter baumannii into Oligella urethralis as a source of acquired resistance to beta-lactams. Antimicrob Agents Chemother. 47, 1536-42.
8.
Murase K, Noda K, Otaki Y, Yasuda J, Oda T, Yokozawa T, Kikuchi K., 2015. A Case of Bacteremia Which Followed a Urinary Tract Infection by Oligella urethralis. Kansenshogaku Zasshi. The Journal of the Japanese Association for Infectious Diseases. 89, 274-278.
9.
Simmons T, Fennelly E, Loughran D., 2015. Oligella ureolytica Bacteremia in Elderly Woman, United States. Emerging Infectious Diseases. 21, 1271-3.
10. Ubee SS, McGlynn L, Fordham M., 2011. Emphysematous pyelonephritis. BJU Int. 107, 1474-8.
11. Huang JJ, Tseng CC., 2000. Emphysematous pyelonephritis: clinicoradiological classification, management, prognosis, and pathogenesis. Arch Intern Med. 160, 797-805.
Fig. 1. Hydronephrosis and pneumatosis with renal stones in the left kidney, and emphysema in portal vein with pneumatosis cystoides intestinalis.
Fig. 2. Colony on the 5% sheep blood and Drigalski agar of the blood culture.
S1438-4221(16)30286-7 http://dx.doi.org/doi:10.1016/j.ijmm.2017.01.004 IJMM 51107
To appear in: Received date: Revised date:
30-9-2016 12-12-2016
Please cite this article as: Yamaguchi, Hirotaka, Yamaguchi, Yukihiro, Hadano, Yoshiro, Hayashi, Kenichi, Nagahara, Chie, Muratani, Tetsuro, Ohkusu, Kiyofumi, The First Case Report of Emphysematous Pyelonephritis and Bacteremia Due to Oligella urethralis.International Journal of Medical Microbiology http://dx.doi.org/10.1016/j.ijmm.2017.01.004 This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
Title The First Case Report of Emphysematous Pyelonephritis and Bacteremia Due to Oligella urethralis.
Hirotaka Yamaguchi a, Yukihiro Yamaguchi
a c
, Yoshiro Hadano a, Kenichi Hayashi a, Chie Nagahara e,
Tetsuro Muratani d, Kiyofumi Ohkusu b
a.
Division of Infectious Diseases, Kenwakai Otemachi Hospital, Kitakyushu, Japan
b
Department of Microbiology, Tokyo Medical University, Tokyo, Japan
c
KRICT (Kitakyushu Regional Infection Control Team)
d
Kyurin Medical Laboratory, Kitakyushu, Japan
e
Department of Microbiology, Kenwakai Otemachi Hospital, Kitakyushu, Japan
Correspondence to Dr. Hirotaka Yamaguchi, [email protected]
Abstract Oligella urethralis (O. urethralis) is an organism that rarely causes infections in humans. We report the case of a 90-year-old bedridden woman with progressive dementia who was placed in a long-term-care facility. She was admitted to our hospital due to fever and unconsciousness with pyuria. The abdominal computed tomography showed left pneumatosis and urinary stone. Fluoroquinolones-resistant O. urethralis, which was identified by the Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry (MALDI-TOF MS) and the 16S rRNA gene sequencing, was isolated form the blood and urine cultures at admission. To the best of our knowledge, this is the first case of emphysematous pyelonephritis caused by O. urethralis.
Keywords Oligella urethralis (O. urethralis); emphysematous pyelonephritis; rare causative organism; rare species; Matrix-Assisted Laser Desorption Ionization–Time of Flight Mass Spectrometry (MALDI-TOF MS); 16S rRNA gene sequencing
1. Introduction O. urethralis is a Gram-negative rod, aerobic, oxidase-positive, non-fermentative, formerly of the genus Moraxella, which has been isolated mainly from urine and the female genital tract, considered to be of low
virulence (Pugliese et al., 1993; Escobar et al., 2001; Catala et al., 2001; Abdolrasouli et al., 2006; Mesnard et al., 1992; Riley et al., 1996; Murase et al., 2015). Additionally, emphysematous pyelonephritis is an acute severe necrotizing infection of the renal parenchyma and its surrounding tissues that result in the presence of gas in the renal parenchyma, collecting system, or perinephric tissues (Ubee et al., 2011). Up to 95 % of the cases with emphysematous pyelonephritis have underlying uncontrolled diabetes mellitus and enterobacteriaceae is the most common causative pathogen in the previous reported cases (Ubee et al., 2011). In this report, we describe the first case of an emphysematous pyelonephritis caused by O. urethralis.
2. Case Report A 90-year-old Japanese woman with diabetes mellitus without insulin therapy was admitted to our hospital because of a single-day fever and impaired consciousness. Her temperature was 38.0℃, pulse rate was 130 beats per minute and regular, systolic blood pressure was 70mmHg and respiratory rate was 30 breaths per minute on room air. Physical examination was unremarkable except for the disturbance of consciousness. In the Emergency department, blood cultures were collected and meropenem was administered under a diagnosis of septic shock with unknown focus. Laboratory data obtained on the admission revealed a white blood cell count of 7,800/μL with 92.3% neutrophils, 4.4% lymphocytes, and 2.2% monocytes. Hemoglobin was 9.8 mg/dL with an MCV of 91.3 fL. Platelet count was 412,000/μL. Serum chemistries revealed sodium of 143 mEq/L, potassium 6.5 mEq/L,
chloride 113 mEq/L, blood urea nitrogen (BUN) 101 mg/dL, creatinine 1.5 mg/dL, glucose 998 mg/dL, albumin 2.2 g/dL, AST 18 IU/L, ALT 11 IU/L, total bilirubin 0.4 mg/dL, LDH 173 IU/L, CRP 8.5 mg/dL, and HbA1c 7.9 %. Her clean-catch urine which was collected by catheterization showed many WBCs and bacteria under high power. Chest radiography showed no evidence of acute pulmonary disease. The computed tomography of abdomen revealed severe hydronephrosis and pneumatosis with renal stones in the left kidney, and pneumatosis cystoides intestinalis with emphysema in portal vein (Fig. 1). A diagnosis of urosepsis secondary to emphysematous pyelonephritis was made. Expeditiously, ureteral stents were inserted to both urinary ducts. Although exploratory laparotomy was done to rule out the small intestinal necrosis, the findings of the operation were intact. After the surgical interventions, the primary team changed meropenem to cefmetazole 1g every 12 hours. On third hospital day, infectious disease specialist was consulted. Because the patient was still septic shock at that time, cefmetazole was switched to meropenem 1g every 12 hours for three days to cover rare gram-negative bacillus and anaerobes. On forth hospital day, blood cultures became positive for gram-negative rod. Her symptoms improved on the sixth hospital day. We changed meropenem to cefmetazole 1g every 12 hours for additional six days.
3. Microbiology One set of blood cultures and the urine cultures from both the ureteral stents yielded gram-negative rod, we show the colony on the 5% sheep blood and Drigalski agar of the blood culture (Fig. 2). Although precise identification of the bacteria was difficult using MicroScan Walkaway 96 Plus (Beckman Coulter, Tokyo,
Japan), which was identified by the BACTEC (Nippon Becton Dickinson, Tokyo, Japan). The gram-negative rod was identified Oligella urethralis by MALDI-TOF MS (VITEK-MS™, Sysmex bioMérieux, Tokyo Japan) and its confidence value of identification was 99.9%. In addition, we performed molecular identification by PCR amplification and sequencing analysis of the 16S rRNA gene using DNA extracted from the isolate of blood culture. The sequence of the 16S rRNA gene was 99.9% identical (1,401 bp over the entire 1,402 bp fragment) with the type strain of O. urethralis. (ATCC 17960, accession number AF227163). Based on these results, we identified the isolate as O. urethralis. The susceptibilities of all O. urethralis of this case were similar. The minimum inhibitory concentrations (MICs) showed that the isolates of the blood and urine culture were susceptible to ampicillin (<=0.5mg/l), ceftriaxone (<=0.5mg/l), meropenem (<=0.25mg/l), clarithromycin (<=8mg/l), minocycline (<=1mg/l), sulfamethoxazole/trimethoprim (<=10mg/l) and resistant to levofloxacin (>4mg/l), garenoxacin (>4mg/l) and tosufloxacin (>2mg/l).
4. Discussion There have been case reports of O. urethralis causing bacteremia (Pugliese et al., 1993; Mesnard et al., 1992; Murase et al., 2015), urinary tract infection (Pugliese et al., 1993; Escobar et al., 2001; Abdolrasouli et al., 2006; Murase et al., 2015), chronic ambulatory peritoneal dialysis (CAPD) peritonitis (Riley et al., 1996), septic arthritis (Mesnard et al., 1992) and genital infection (Catala et al., 2001). The low virulence of this organism may contribute to the paucity of recognized cases but Oligella spp. can be misidentified as
phenotypically similar organisms, such as Bordetella bronchiseptica and Achromobacter spp.. Some cases may also have been dismissed as contamination because of laboratorians’ and clinicians’ lack of familiarity with this bacterium (Simmons et al., 2015). Emphysematous pyelonephritis is a severe, necrotizing form of acute bacterial pyelonephritis with underlying uncontrolled diabetes mellitus (Ubee et al., 2011; Huang et al., 2000). Previous report cases show that Escherichia coli is the most common pathogen in nearly 70% of emphysematous pyelonephritis, followed by Proteus mirabilis, Klebsiella pneumoniae, Group D Streptococcus, and coagulase-negative Staphylococcus (Ubee et al., 2011; Huang et al., 2000). O. urethralis has not been reported as the causative organism of emphysematous pyelonephritis. O. urethralis is usually susceptible to beta-lactam antibiotics, but beta-lactamase-producing strains, as well as strains resistant to fluoroquinolones, have been reported (Mammeri et al., 2003). In this case, the isolate was resistant to levofloxacin, garenoxacin and tosufloxacin, but susceptible to other antimicrobial agents including ampicillin and ceftriaxone. In the present day, levofloxacin has been widely used and our patient had received levofloxacin on previous occasions. In the last two months, the patient was prescribed two periods of levofloxacin by primary care doctors of the long-term-care facility. Quinolone resistance in O. urethralis has been also described for a case of an infection leading to chronic ambulatory peritoneal dialysis peritonitis (Riley et al., 1996), in this case, previous levofloxacin usage may have caused the resistance to quinolone.
In conclusion, we report here a case of emphysematous pyelonephritis and bacteremia caused by O. urethralis and successful control of the infection with antibiotic therapy and intervention to both urinary ducts. To the best of our knowledge, this is the first case of emphysematous pyelonephritis caused by O. urethralis reported. The causative organism was identified by MALDI-TOF MS and the 16S rRNA gene sequencing. O. urethralis is known to be a commensal of the human genitourinary tract, and rarely pathogenic for humans (Murase et al., 2015). However, we believe that this organism is a potential opportunistic pathogen for the elderly, especially in patients with diabetes and obstruction of the urinary tract (i.e., renal stones and disorder of urination).
Acknowledgement We would like to thank Brannon Raney for his support in the preparation of this manuscript.
References 1.
Pugliese A, Pacris B, Schoch PE, Cunha BA., 1993. Oligella urethralis urosepsis. Clin Infect Dis. 17, 1069-70.
2.
Escobar Mora S, Marne Trapero C, Gascón Val M, López Calleja AI., 2001. Infección urinaria por Oligella urethralis. Atención Primaria. 30, 620-3.
3.
Catala A, Simha V, Guillotel B, Rousseau MC., 2001. Genital infection with Oligella urethralis. La Presse Medicale. 30, 1007-8.
4.
Abdolrasouli A, Aligholi M, Hemmati Y., 2006. Quinolone Resistance in Oligella Urethralis-Associated Urinary Tract Infection. Iranian J Phamacol Ther. 5, 83-5.
5.
Mesnard R, Sire JM, Donnio PY, Riou JY, Avril JL., 1992. Septic arthritis due to Oligella urethralis. Eur J Clin Microbiol Infect Dis. 11, 195-6.
6.
Riley UB, Bignardi G, Goldberg L, Johnson AP, Holmes B., 1996. Quinolone resistance in Oligella urethralis-associated chronic ambulatory peritoneal dialysis peritonitis. J Infect. 32, 155-6.
7.
Mammeri H, Poirel L, Mangeney N, Nordmann P., 2003. Chromosomal integration of a cephalosporinase gene from Acinetobacter baumannii into Oligella urethralis as a source of acquired resistance to beta-lactams. Antimicrob Agents Chemother. 47, 1536-42.
8.
Murase K, Noda K, Otaki Y, Yasuda J, Oda T, Yokozawa T, Kikuchi K., 2015. A Case of Bacteremia Which Followed a Urinary Tract Infection by Oligella urethralis. Kansenshogaku Zasshi. The Journal of the Japanese Association for Infectious Diseases. 89, 274-278.
9.
Simmons T, Fennelly E, Loughran D., 2015. Oligella ureolytica Bacteremia in Elderly Woman, United States. Emerging Infectious Diseases. 21, 1271-3.
10. Ubee SS, McGlynn L, Fordham M., 2011. Emphysematous pyelonephritis. BJU Int. 107, 1474-8.
11. Huang JJ, Tseng CC., 2000. Emphysematous pyelonephritis: clinicoradiological classification, management, prognosis, and pathogenesis. Arch Intern Med. 160, 797-805.
Fig. 1. Hydronephrosis and pneumatosis with renal stones in the left kidney, and emphysema in portal vein with pneumatosis cystoides intestinalis.
Fig. 2. Colony on the 5% sheep blood and Drigalski agar of the blood culture.