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Proteus penneri urosepsis in a patient with diabetes mellitus
Proteus penneri urosepsis in a patient with diabetes mellitus Dorota K. Latuszynski, MD, Paul Schoch, PhD, Mohammad T. Qadir, MD, and Burke A. Cunha, MD, Mineola and Stony Brook, N.Y.
Proteus penneri has been isolated from m a n y different clinical sources, including surgical w o u n d infections, urine, and blood. We describe the first reported case of P. penneri nosocomial urosepsis in a patient with diabetes. P. penneri was subsequently isolated from bronchoalveolar Iavage fluid and a p u l m o n a r y artery catheter tip. (Heart Lung e 1998;27:146-8)
n 1982 certain taxonomic changes were made in the genus Proteus. This resulted in a separate species emerging from what was, until then, the somewhat heterogeneous P. vulgaris. The introduction of P. penneri, a new m e m b e r of the genus, d i d not represent a newly discovered species, b u t instead emphasized that a group of organisms, previously classified as either P. penneri biogroup 1 or atypical (ornithine negative) P. mirabilis, d e m o n s t r a t e d high enough DNA relatedness within the group to justify classification as a separate species. ~'3 Currently, four species are recognized within the genus Proteus: P. mirabilis, P. vulgaris, P. myxofaciens (not a human pathogen), and P. penneri. P. penneri is a nosoco~ mial pathogen that causes urinary tract infec~ tions, surgical wound infections, and may cause severe invasive infections in p a t i e n t s with leukopenia. We report a case which, to our knowledge, is the first case report' in the litera~ ture of P. penneri urosepsis in a patient with diabetes.
I
CASE REPORT A 74-year-01d woman with a long-standing history of diabetes mellitus, hypothyroidism, and peptic
From the Microbiology Laboratory, the Pathology Department, and the Infectious Disease Division, Winthrop~University Hospital, Mineola, and the State University of New York School of Medicine, Stony Brook. Reprint requests: BurkeA. Cunha, MD, Chief, Infectious Disease Division, Winthrop-UniversRy Hospital, Mineola, NY 11501. Copyright © 1998by Mosby, inc. 0147-9563/98/$5.00+ 0 2/I/84980 146
ulcer disease was admitted to Winthrop-University Hospital with unstable angina. Based on serial cardiac enzymes and electrocardiogram, she had not had a myocardial infarction; she was worked up initially for sinus bradycardia with intermittent 2:1 atrial ventricular block requiring a permanent pacemaker. She also was found to have four-vessel disease by cardiac catheterization and underwent coronary arterial bypass grafting. Her hospital course was complicated on postoperative day 8, when respiratory distress and cough developed. Chest radiograph revealed right hemidiaphragm elevation with pleural effusion, and a right chest tube was inserted, from which 500 ml of serosanguinous fluid was drained; she was later intubated secondary to respiratory failure. Ampicillin/sulbactam was started empirically, 1.5 gm intravenously (IV) every 6 hours. Her white blood cell count was 17,000 mm 3. Urine and blood cultures grew P. penneri resistant to piperacillin, ampicillin/ sulbactam, cefazolin, and cefoperazone, but s e n s i t i v e to t r i m e t h o p r i m - s u l f a m e t h o x a z o l e , ciprofloxacin, ceftazidime, and gentamicin. She was switched to ciprofloxacin 400 mg IV every 12 hours. Subsequently, the pulmonary artery catheter tip also grew P. penneri. The patient's condition gradually improved, and she was extubated successfully. She completed a 14-day course of ciprofloxacin 400 mg IV every 12 hours, and she ultimately was discharged home. DISCUSSION
All P. penneri strains exhibit most of the biochemical properties typical of P. vulgaris and other Proteus species. There are only three reactions that allow reliable differentiation between P. penneri and P. vulgaris. These include the inability of P. penned MARCH/APRIL 1998 HEART & LUNG
to produce indole, failure to hydrolyze esculin, and lack of salicin fermentation. Also, in contrast to P. vulgaris, P. penneri shows resistance to chloramphenicol, as demonstrated by both agar diffusion and broth dilution methods. U Maltose fermentation, sucrose fermentation, and lack of omithine decarboxylase activity differentiate P. penneri from P. mirabilis, l As with other Proteus species, P. penneri has the ability to hemolyze sheep and human red blood cells, which is believed to represent a virulence factor. In P. penneri, alpha hemolysin activity may be correlated with cytotoxic activity. The cytotoxic effects of P. penneri-soluble hemolysin are different from the action of the common Proteus hemolysin produced in fluid cultures. The latter seems to facilitate cell penetration without causing cytotoxic effects. 5"8 Other potential virulence factors produced by P. penneri include urease, IgA protease, hemagglutinins, and fimbriae. 7,9 P.. penneri strains have been isolated from different clinical sources including urine, stool, wounds, bronchial exudate, conjunctiva, and blood. However, the extent of its clinical significance remains unclear. There are reports of nosocomial P. penneri urinary tract infection with formation of urinary bladder calculi associated with indwelling catheters. 1°,1~ From currently limited epidemiologic data, pure P. penneri isolates were cultured predominantly from urine. There is also a report of pure blood and subcutaneous abscess cultures from a patient with leukemia.12 A pure culture of the organism was obtained from an epidural abscess complicating chronic suppurative otitis media, j3 In most cases, however, cultures tend to yield, in addition to P. penneri, other gram-negative organisms and gram-positive cocci, thereby, creating difficulty in establishing the extent of its pathogenic role. 8,~1,12 Several comparative studies of antimicrobic susceptibility have revealed many similarities in antibiotic profile between P. vulgaris and P. penneri, such as susceptibility to ceftazidime and aminoglycosides and resistance to cefazolin.2,14 However, significant differences have also been noted. P. penneri is generally susceptible to ceftizoxime and tetracycline, with increased resistance to ceftriaxone, cefoperazone, cefuroxime, and the ureidopenicillins. 2,15,16 The latter observation points to the need for identification of Proteus isolates to the species level. In addition, because strain differences have been noted, antimicrobial susceptibiliw testing of each Proteus isolate is warranted to avoid inappropriate or less than optimal therapy.2,18-20
HEART & LUNG
VOL. 27, NO. 2
To facilitate the identification of expanding and reclassified species of the family Enterobacteriaceae, several commercial, nonautomated and automated systems are available. These are, in general, easy to interpret and provide correct identification. However, a small percentage of isolate tests in these systems, or isolates that are identified presumptively using rapid tests such as spot indole, may be either misidentified or produce a code with no interpretation in the database. When such discrepancies occur, supplemental testing may be necessary. 17 Since the reclassification of P. vulgaris as indole negative or positive biogroup 1 as P. penneri in 1982, only a few cases of nosocomially acquired infection associated with P. penneri have been described in the literature. Most cases involve the urinary tract. Occasionally, massive upper urinary tract infection, with the formation of struvite stones by splitting urease and alkalinizing urine, impedes the urinary flow, traumatizing uroepithelial lining, causing inflammation, and thus spreading infection. In our case, the patient did not have urinary tract stones nor was urine pH reported as alkaline. We believe this is the first case of nosocomially acquired P. penneri urosepsis occurring in a patient with diabetes. Usually, P. penneri is associated with urinary tract infections or abdominal wound infections. In the current case, P. penneri was isolated from urine and blood as well as the pulmonary artery catheter tip. This patient with diabetes mellitus had urosepsis caused by P. penneri. Bacteremia of bladder origin only occurs in the setting of preexisting renal disease, partial or total obstruction, or in nonleukopenic compromised hosts, i.e., systemic lupus erythematosus, chronic steroid use, chronic alcoholics, or in diabetics, which was the underlying cause in the case presented here.
REFERENCES
I. Hickman FW, Steigerwalt H, Farmer IJ III, Brenner Dl. Identification of Proteuspenneri sp. nov., formerly known as Proteusvulgarisindole negativeor as ProteusvuIgarisBiogroup I. I Clin Microbiol 1982;15:1097~102. 2. Na'Was TE, Mawajdeh S, Dababneh A, Al:Omari. In vitro activities of antimicrobial agentsagainst Proteusspeciesfrom clinical specimens. Br JBiomed Sci 1994;51:95~9. 3. SidorczykZ, Zych K. Selected properties of the Proteuspenneri sp. nov. from the American Collection. Med Dosw Mikrobiol 1993;45:69~73. 4. LukomskiS, PytlosM, SerwecinskaL, SidorczykZ, JaworskiA. Analysis of antibiotic resistance determinants in Proteuspenneri. Eurl Clin MicrobioI Infect Dis 1993;12:467~9. 5. LukomskiS, Muller B, Schmidt G. Extracellular hemolysin of Proteuspennericoded by chromosomal genes is similar to the alpha~hemolysin of E. coll. lnt JMed 1990;273:I50-5.
147
6. Rozalski A, Kotelko K. Hemolytic activity and invasiveness in strains of Proteus penneri. ] Clin Microbiol 1987;26:1094-6. 7. Lukomski S, Serwecinska L, Rozalski A, Dziadek J, Staczek P, Jaworski A. Ceil-free and cell-bound hemolytic activities or Proteus penneri determined by different determinants. Can J Microbiol 1991;37:419-24. 8. Mtiller HE. Occurrence and pathogenic role of MorganeUa9.
10.
1i.
12.
13.
Proteus-Providencia group bacteria in human feces. J Ciin Microbiol 1986;23:404-5. Zych K, Swierzko A, Sidorczyk Z. Serological characterization of Proteus penneri species novum. Arch lmmunol Ther Exp 1992;40:92-8. Krajden S, Fuksa M, Lizewski W, Barton L, Lee A. Proteus penneri isolated from the pus of a patient with epidural abscess. Kansenshogaku Zasshi 1991;66:144-8. Engler HD, Troy K, Bottone EJ. Bacteremia and subcutaneous abscess caused by Proteus penneri in a neutropenic host. J Clin Microbiol 1990;28:1645-6. Kitch TT, Jacobs MR, Appelbaum PC. Evaluation of Rapid one system for identification of 379 strains in the family Enterobacteriaceae and oxidase-negative, gram-negative nonfermenters. J Clin Microbiol 1994;32:931-4. Krajden S, Fuksa M, Petrea C, Crisp LJ. Expanded clinical spectrum of infections caused by Proteus penneri. J Clin Microbiol I987;25:578-9.
14. Fuksa M, Krajden S, Lee A. Susceptibilities of 45 clinical isolates of Proteus penneri. Antimicrob Agents Chemother 1984;26:419-20. 15. Miro E, Barthelemy M, Peduzzi ], Reynau A, Morand A, Prats G, et aI. Properties of a cephalosporinase produced by Proteus penneri which is inhibited by clavulanic acid. Pathol Biol 1994;42:487-90. 16. Hawkey PM, Hawkey CA. Comparative in vitro activity of quinolone carboxylic acids against Proteae. J Antimicrob Chemother 1984; 14:485-9. 17. Reeves DS, Bywater MJ, Holt HA. The activity of cefpirome and ten other antimicrobial agents against 2858 clinical isolates collected from 20 centers. J Antimicrob Chemother 1993;31:345-62. i8. Mobley HLT, Jones BD, Penner JL. Urease activity of Proteus penneri. J Clin Microbiol 1987;25:2302-5. 19. Picolomini R, Cellini L, Allocati N, DiGiroamo A, Ravagnan G. Comparative in vitro susceptibilities of 13 antimicrobiaI agents against Morganella-Proteus-Providencia group bacteria from urinary tract infections. Antimicrob Agents Chemother 1987;31:1644-7. 20. Rozalski A, Bartoziejska B, Wykrota M, Serwecinska L, bukomski S, Kotelko K. Characterization of hemolytic activity of Proteus penneri. Med Dosw MikrobioI 1993;45:79-83.
Don't miss a single issue of the journal! To ensure prompt service when you change your address, please photocopy and complete the form below. Please send your change of address notification at least six weeks before your move to ensure continued service. We regret we cannot guarantee replacement of issues missed due to late notification. J O U R N A L TITLE: Fill in the title of the journal here.
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Affix the address label from a recent issue of the journal here.
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314-432-1158
1-800-453-4351 Outside the U.S.,call 314-453-4351
148
Mosby
MARCH/APRIL1997 HEART & LUNG
Proteus penneri has been isolated from m a n y different clinical sources, including surgical w o u n d infections, urine, and blood. We describe the first reported case of P. penneri nosocomial urosepsis in a patient with diabetes. P. penneri was subsequently isolated from bronchoalveolar Iavage fluid and a p u l m o n a r y artery catheter tip. (Heart Lung e 1998;27:146-8)
n 1982 certain taxonomic changes were made in the genus Proteus. This resulted in a separate species emerging from what was, until then, the somewhat heterogeneous P. vulgaris. The introduction of P. penneri, a new m e m b e r of the genus, d i d not represent a newly discovered species, b u t instead emphasized that a group of organisms, previously classified as either P. penneri biogroup 1 or atypical (ornithine negative) P. mirabilis, d e m o n s t r a t e d high enough DNA relatedness within the group to justify classification as a separate species. ~'3 Currently, four species are recognized within the genus Proteus: P. mirabilis, P. vulgaris, P. myxofaciens (not a human pathogen), and P. penneri. P. penneri is a nosoco~ mial pathogen that causes urinary tract infec~ tions, surgical wound infections, and may cause severe invasive infections in p a t i e n t s with leukopenia. We report a case which, to our knowledge, is the first case report' in the litera~ ture of P. penneri urosepsis in a patient with diabetes.
I
CASE REPORT A 74-year-01d woman with a long-standing history of diabetes mellitus, hypothyroidism, and peptic
From the Microbiology Laboratory, the Pathology Department, and the Infectious Disease Division, Winthrop~University Hospital, Mineola, and the State University of New York School of Medicine, Stony Brook. Reprint requests: BurkeA. Cunha, MD, Chief, Infectious Disease Division, Winthrop-UniversRy Hospital, Mineola, NY 11501. Copyright © 1998by Mosby, inc. 0147-9563/98/$5.00+ 0 2/I/84980 146
ulcer disease was admitted to Winthrop-University Hospital with unstable angina. Based on serial cardiac enzymes and electrocardiogram, she had not had a myocardial infarction; she was worked up initially for sinus bradycardia with intermittent 2:1 atrial ventricular block requiring a permanent pacemaker. She also was found to have four-vessel disease by cardiac catheterization and underwent coronary arterial bypass grafting. Her hospital course was complicated on postoperative day 8, when respiratory distress and cough developed. Chest radiograph revealed right hemidiaphragm elevation with pleural effusion, and a right chest tube was inserted, from which 500 ml of serosanguinous fluid was drained; she was later intubated secondary to respiratory failure. Ampicillin/sulbactam was started empirically, 1.5 gm intravenously (IV) every 6 hours. Her white blood cell count was 17,000 mm 3. Urine and blood cultures grew P. penneri resistant to piperacillin, ampicillin/ sulbactam, cefazolin, and cefoperazone, but s e n s i t i v e to t r i m e t h o p r i m - s u l f a m e t h o x a z o l e , ciprofloxacin, ceftazidime, and gentamicin. She was switched to ciprofloxacin 400 mg IV every 12 hours. Subsequently, the pulmonary artery catheter tip also grew P. penneri. The patient's condition gradually improved, and she was extubated successfully. She completed a 14-day course of ciprofloxacin 400 mg IV every 12 hours, and she ultimately was discharged home. DISCUSSION
All P. penneri strains exhibit most of the biochemical properties typical of P. vulgaris and other Proteus species. There are only three reactions that allow reliable differentiation between P. penneri and P. vulgaris. These include the inability of P. penned MARCH/APRIL 1998 HEART & LUNG
to produce indole, failure to hydrolyze esculin, and lack of salicin fermentation. Also, in contrast to P. vulgaris, P. penneri shows resistance to chloramphenicol, as demonstrated by both agar diffusion and broth dilution methods. U Maltose fermentation, sucrose fermentation, and lack of omithine decarboxylase activity differentiate P. penneri from P. mirabilis, l As with other Proteus species, P. penneri has the ability to hemolyze sheep and human red blood cells, which is believed to represent a virulence factor. In P. penneri, alpha hemolysin activity may be correlated with cytotoxic activity. The cytotoxic effects of P. penneri-soluble hemolysin are different from the action of the common Proteus hemolysin produced in fluid cultures. The latter seems to facilitate cell penetration without causing cytotoxic effects. 5"8 Other potential virulence factors produced by P. penneri include urease, IgA protease, hemagglutinins, and fimbriae. 7,9 P.. penneri strains have been isolated from different clinical sources including urine, stool, wounds, bronchial exudate, conjunctiva, and blood. However, the extent of its clinical significance remains unclear. There are reports of nosocomial P. penneri urinary tract infection with formation of urinary bladder calculi associated with indwelling catheters. 1°,1~ From currently limited epidemiologic data, pure P. penneri isolates were cultured predominantly from urine. There is also a report of pure blood and subcutaneous abscess cultures from a patient with leukemia.12 A pure culture of the organism was obtained from an epidural abscess complicating chronic suppurative otitis media, j3 In most cases, however, cultures tend to yield, in addition to P. penneri, other gram-negative organisms and gram-positive cocci, thereby, creating difficulty in establishing the extent of its pathogenic role. 8,~1,12 Several comparative studies of antimicrobic susceptibility have revealed many similarities in antibiotic profile between P. vulgaris and P. penneri, such as susceptibility to ceftazidime and aminoglycosides and resistance to cefazolin.2,14 However, significant differences have also been noted. P. penneri is generally susceptible to ceftizoxime and tetracycline, with increased resistance to ceftriaxone, cefoperazone, cefuroxime, and the ureidopenicillins. 2,15,16 The latter observation points to the need for identification of Proteus isolates to the species level. In addition, because strain differences have been noted, antimicrobial susceptibiliw testing of each Proteus isolate is warranted to avoid inappropriate or less than optimal therapy.2,18-20
HEART & LUNG
VOL. 27, NO. 2
To facilitate the identification of expanding and reclassified species of the family Enterobacteriaceae, several commercial, nonautomated and automated systems are available. These are, in general, easy to interpret and provide correct identification. However, a small percentage of isolate tests in these systems, or isolates that are identified presumptively using rapid tests such as spot indole, may be either misidentified or produce a code with no interpretation in the database. When such discrepancies occur, supplemental testing may be necessary. 17 Since the reclassification of P. vulgaris as indole negative or positive biogroup 1 as P. penneri in 1982, only a few cases of nosocomially acquired infection associated with P. penneri have been described in the literature. Most cases involve the urinary tract. Occasionally, massive upper urinary tract infection, with the formation of struvite stones by splitting urease and alkalinizing urine, impedes the urinary flow, traumatizing uroepithelial lining, causing inflammation, and thus spreading infection. In our case, the patient did not have urinary tract stones nor was urine pH reported as alkaline. We believe this is the first case of nosocomially acquired P. penneri urosepsis occurring in a patient with diabetes. Usually, P. penneri is associated with urinary tract infections or abdominal wound infections. In the current case, P. penneri was isolated from urine and blood as well as the pulmonary artery catheter tip. This patient with diabetes mellitus had urosepsis caused by P. penneri. Bacteremia of bladder origin only occurs in the setting of preexisting renal disease, partial or total obstruction, or in nonleukopenic compromised hosts, i.e., systemic lupus erythematosus, chronic steroid use, chronic alcoholics, or in diabetics, which was the underlying cause in the case presented here.
REFERENCES
I. Hickman FW, Steigerwalt H, Farmer IJ III, Brenner Dl. Identification of Proteuspenneri sp. nov., formerly known as Proteusvulgarisindole negativeor as ProteusvuIgarisBiogroup I. I Clin Microbiol 1982;15:1097~102. 2. Na'Was TE, Mawajdeh S, Dababneh A, Al:Omari. In vitro activities of antimicrobial agentsagainst Proteusspeciesfrom clinical specimens. Br JBiomed Sci 1994;51:95~9. 3. SidorczykZ, Zych K. Selected properties of the Proteuspenneri sp. nov. from the American Collection. Med Dosw Mikrobiol 1993;45:69~73. 4. LukomskiS, PytlosM, SerwecinskaL, SidorczykZ, JaworskiA. Analysis of antibiotic resistance determinants in Proteuspenneri. Eurl Clin MicrobioI Infect Dis 1993;12:467~9. 5. LukomskiS, Muller B, Schmidt G. Extracellular hemolysin of Proteuspennericoded by chromosomal genes is similar to the alpha~hemolysin of E. coll. lnt JMed 1990;273:I50-5.
147
6. Rozalski A, Kotelko K. Hemolytic activity and invasiveness in strains of Proteus penneri. ] Clin Microbiol 1987;26:1094-6. 7. Lukomski S, Serwecinska L, Rozalski A, Dziadek J, Staczek P, Jaworski A. Ceil-free and cell-bound hemolytic activities or Proteus penneri determined by different determinants. Can J Microbiol 1991;37:419-24. 8. Mtiller HE. Occurrence and pathogenic role of MorganeUa9.
10.
1i.
12.
13.
Proteus-Providencia group bacteria in human feces. J Ciin Microbiol 1986;23:404-5. Zych K, Swierzko A, Sidorczyk Z. Serological characterization of Proteus penneri species novum. Arch lmmunol Ther Exp 1992;40:92-8. Krajden S, Fuksa M, Lizewski W, Barton L, Lee A. Proteus penneri isolated from the pus of a patient with epidural abscess. Kansenshogaku Zasshi 1991;66:144-8. Engler HD, Troy K, Bottone EJ. Bacteremia and subcutaneous abscess caused by Proteus penneri in a neutropenic host. J Clin Microbiol 1990;28:1645-6. Kitch TT, Jacobs MR, Appelbaum PC. Evaluation of Rapid one system for identification of 379 strains in the family Enterobacteriaceae and oxidase-negative, gram-negative nonfermenters. J Clin Microbiol 1994;32:931-4. Krajden S, Fuksa M, Petrea C, Crisp LJ. Expanded clinical spectrum of infections caused by Proteus penneri. J Clin Microbiol I987;25:578-9.
14. Fuksa M, Krajden S, Lee A. Susceptibilities of 45 clinical isolates of Proteus penneri. Antimicrob Agents Chemother 1984;26:419-20. 15. Miro E, Barthelemy M, Peduzzi ], Reynau A, Morand A, Prats G, et aI. Properties of a cephalosporinase produced by Proteus penneri which is inhibited by clavulanic acid. Pathol Biol 1994;42:487-90. 16. Hawkey PM, Hawkey CA. Comparative in vitro activity of quinolone carboxylic acids against Proteae. J Antimicrob Chemother 1984; 14:485-9. 17. Reeves DS, Bywater MJ, Holt HA. The activity of cefpirome and ten other antimicrobial agents against 2858 clinical isolates collected from 20 centers. J Antimicrob Chemother 1993;31:345-62. i8. Mobley HLT, Jones BD, Penner JL. Urease activity of Proteus penneri. J Clin Microbiol 1987;25:2302-5. 19. Picolomini R, Cellini L, Allocati N, DiGiroamo A, Ravagnan G. Comparative in vitro susceptibilities of 13 antimicrobiaI agents against Morganella-Proteus-Providencia group bacteria from urinary tract infections. Antimicrob Agents Chemother 1987;31:1644-7. 20. Rozalski A, Bartoziejska B, Wykrota M, Serwecinska L, bukomski S, Kotelko K. Characterization of hemolytic activity of Proteus penneri. Med Dosw MikrobioI 1993;45:79-83.
Don't miss a single issue of the journal! To ensure prompt service when you change your address, please photocopy and complete the form below. Please send your change of address notification at least six weeks before your move to ensure continued service. We regret we cannot guarantee replacement of issues missed due to late notification. J O U R N A L TITLE: Fill in the title of the journal here.
OLD A D D R E S S :
NEW ADDRESS:
Affix the address label from a recent issue of the journal here.
Clearly print your new address here. Name Address City/State/ZIP
COPY A N D MAIL THIS F O R M TO:
OR FAX TO:
OR PHONE:
Journal Subscription Services M o s b y , Inc. 11830 W e s t l i n e I n d u s t r i a l Dr. St. L o u i s , M O 6 3 1 4 6 - 3 3 1 8
314-432-1158
1-800-453-4351 Outside the U.S.,call 314-453-4351
148
Mosby
MARCH/APRIL1997 HEART & LUNG