Providencia species
Authors: Chelsie E Armbruster, PhD., Harry Mobley, PhD.
Previous authors: Robert R. Muder, M.D., Masashi Narita, M.D.
Microbiology
Providencia is a genus within the Enterobacteriaceae family closely related to the Providencia and Morganella genera. There are currently 8 recognized species within the genus: P. alcalifaciens, P. burhodogranaeriae, P. heimbachae, P. rettgeri, P. rustigianii, P. sneebia, P. stuartii,and P. vermicola (22, 61, 66, 71). Like other members of the tribe Proteeae, Providencia species produce the enzyme phenylalanine deaminase, which catalyzes the conversion of phenylalanine to phenylpyruvate.
Epidemiology
P. stuartii is the most frequently encountered human pathogen within the genus. The most frequent site of isolation is the urinary tract of chronically catheterized patients (29, 38, 39, 61) in hospitals and long-term care facilities. Among this patient population, P. stuartii is recognized as a persistent colonizer (76, 77). It is common for multiple strains to be present simultaneously in a particular institution (29, 82). The urine of chronically catheterized patients is the usual reservoir of the organism (17). Nosocomially acquired P. stuartii are typically resistant to multiple antimicrobials (54, 65). P. rettgeri is also primarily a cause of nosocomial urinary tract infection (61). Neither organism is likely to cause urinary tract infection in ambulatory persons.
Reservoirs of P. alclifaciens include water, wastewater and soil. It appears to be an agent of gastrointestinal infections in humans (3, 27) and has been reported to cause hemorrhagic pneumonia in piglets (75). Settings in which this agent has been implicated include foodborne enteritis and traveler's diarrhea (3, 13, 27, 58). A large food-borne outbreak of P. alcalifaciens-associated diarrhea occurred in Japan (58). An outbreak of enteritis caused by P. alcalifaciens occurred among Czech Army Field Hospital personnel during their stay in Turkey (13).
Human isolates of P. rustigianii and P. heimbachae are rare; their role, if any, in human disease is uncertain (31, 57). P. vermicola was first isolated from a nematode (71) and later from a diseased rohu fish (56), but this species has not been implicated in human infection. P. sneebia and P.burhodogranaeriae were isolated from fruit flies (36) and have not been reported to cause human infection.
Clinical Manifestations
The most frequent clinical manifestation of P. stuartii infection is urinary tract infections in the catheterized patient (29, 38, 39, 78). Wound infections and pneumonia may also occur, particularly in critically ill patients (4, 21, 50, 84). P. stuartii bacteremia most commonly arises from urinary tract infection (54, 81). Bacteremia in the course of pneumonia or burn wound infection may occur as well (79). As of 2014, there have been three documented cases of P. stuartii meningitis (67, 70, 73), and P. stuartii has also been isolated from a case of Fournier's gangrene (11).
Clinical P. rettgeri infection presents as nosocomial urinary tract infection in the majority of cases. P. rettgeri has also been isolated from burn wounds (2, 25) and intra-abdominal infections (69).
P. alcalifacians causes an acute enteritis characterized by abdominal pain and watery diarrhea (58). Fever is present in one quarter of patients; tenesmus is uncommon. Based on a common source food-borne outbreak, the mean incubation period is 69 hours.
Laboratory Diagnosis
Providencia species are readily isolated from urine and blood using standard laboratory media. Most commercially available identification systems used in clinical laboratories accurately identify P. stuartii, P. alcalifaciens, and P. rettgeri (61). P. alcalifaciens appears as lactose-negative colonies on MacConkey agar (58). Urease activity is variable but common in Providencia spp., particularly those isolated from urinary tract infections (35, 52). Transfer of large conjugative plasmids from one Providencia species to another can add phenotypic traits that alter the species as identified by commercially available systems (16, 42). These traits include ability to ferment lactose and sucrose.
Pathogenesis
P. stuartii can directly adhere to urinary catheters (18), and adherence is associated with the presence of the mannose-resistant/Klebsiella-like hemagglutinatin, also known as MR/K fimbriae (50). P. stuartii isolates are also capable of adhering to uroepithelial cells through a process that also appears to involve fimbriae (53). P. stuartii pathogenesis can be investigated using a mouse model of ascending urinary tract infection (6, 34). In this model, infection with P. stuartii results in robust colonization of the bladder and kidneys, and bacteremia in a small percentage of mice (6)
P. alcalifaciens is an invasive enteric pathogen. Strains of P. alcalifaciens, isolated from patients with diarrhea, show invasion of Hep-2 and HeLa cells in vitro (4, 5, 28). Janda et al. reported that some P. alcalifaciens strains, as well as strains of P. stuartii and P. rettgeri, can invade HEp-2 monolayers (33). Injection of an outbreak strain into a rabbit ileal loop caused fluid accumulation, along with evidence of mucosal inflammation on histologic examination (58).
SUSCEPTIBILITY IN VITRO AND IN VIVO
In keeping with their role as nosocomial pathogens, strains of P. stuartii and P. rettgeri are often resistant to multiple antimicrobials. A study from Ethiopia reported that 75% of Providencia isolates were multi-drug resistant (25) and another study identified Providencia spp. as one of the two most common multi-drug resistant urinary tract infection isolates (43). Antimicrobial resistance patterns for 319 Providencia isolates collected over a 10-year period in Portugal are reported in Table 1 (43). Over 90% of isolates were resistant to aminoglycosides (amikacin, gentamicin, isepamicin, and netilmicin), 1st generation cephalosporins (cefazolin and cephradine), and amoxicillin. Approximately 20% of isolates were resistant to other penicillins (augmentin, piperacillin/tazobactam, and pivmecillinam), quinolones (ciprofloxacin, lomefloxacin, norfloxacin, and ofloxacin), and sulfonamides (co-trimoxazole). Roughly 10% of isolates were resistant to 2nd generation cephalosporins (cefoxitin and cefuroxime), and 5% of isolates were resistant to aztreonam. Approximately 99% of isolates remained susceptible to carbapenems (imipenem), 3rd generation cephalosporins (cefadizime, ceftazidime, and ceftibuten), and 4th generation cephalosporins (cefepime). However, it is important to note that these isolates were collected between 1999 and 2009 and may therefore underestimate the current level of antibiotic resistance.
Table 2 shows antibiotic resistance data for P. stuartii and P. rettgeri isolated from diverse sources including urinary tract infections, wounds, Fournier's gangrene, meningitis, blood, pus, and rectal swabs (2, 8, 9, 10, 11, 23, 24, 30, 32, 41, 44, 48, 49, 59, 62, 63, 70, 72, 73, 83, 84). The majority of these strains were isolatedbetween 2005 and 2011.
Providencia stuartii Antibiotic Susceptibility
As shown in Table 2, greater than 40% of P. stuartii isolates were reported to be resistant to aminoglycosides (gentamicin, spectinomycin, streptomycin, tobramycin), 1st generation cephalosporins (cefazolin and cephradine), 2nd generation cephalosporins (cefoxitin and cefuroxime), one 3rd generations cephalosporin (cefotaxime), nitrofurantoin, penicillins (amoxicillin, augmentin, ampicillin, ampicillin-sulbactam, and ticaricillin), quinolones (ciprofoloxacin, fluoroquinolone, levofloxacin, and nalidixic acid), trimethoprim/sulfamethoxazole, polymixins (including colisitin), tetracycline, and chloramphenicol (12, 64, 81). The beta-lactamase enzymes of most strains are not inhibited by clavulanate or sulbactam, but are inhibited by tazobactam; thus, most isolates are susceptible to piperacillin/tazobactam (21, 30). Most isolates remain susceptible to third-generation cephalosporins (20, 37, 81), but cefotaxime resistance has been observed in several cases (9, 41, 83). Virtually all isolates of P. stuartii remain susceptible to meropenem (8, 30, 56, 80, 81). However, carbapenem resistance needs to be carefully monitored. One study reported an outbreak of carbapenem resistance in Brazil, in which approximately 35% of P. stuartii isolates were resistant to ertapenem and imipenem (83), and other P. stuartii isolates have been reported to produce carbapenemases(49).
There has been a recent increase in reports of P. stuartii producing class A and class D extended-spectrum beta-lactamases (ESBLs) (1, 5, 11, 21, 23, 31, 37, 39, 40, 50, 78), which provide resistance to third-generation cephalosporins. Emerging P. stuartii beta-lactamases include the class A TEM, CTX-M, VEB, and the New Delhi metallo-β-lactamase (NDM-1) (2, 9, 32, 41, 44, 47, 48, 49, 59, 83),and the class D OXA-10 (2, 44, 47). Molecular epidemiologic evidence indicates that plasmids encoding ESBLs can be transferred from P. stuartii to other Enterobacteriaceae, including E. coli and Enterobacter aerogenes (2, 7, 9, 32, 41, 59). Although ESBL-producing strains are relatively uncommon in the community, large hospital-associated outbreaks of these strains may occur (9, 49, 74, 83). As is the case with other Enterobacteriaceae, standard susceptibility tests used by clinical laboratories may fail to detect ESBL production by P. stuartii isolates. AmpC-type β-lactamases (CBLs) have also recently been reported in P. stuartii isolates (2, 8, 83). These enzymes are capable of degrading penicillins and most cephalosporins and possibly carbapenems (83), and they are only poorly inhibited by β-lactamase inactivators(8). Spread of CBLs is of great concern if they contribute to carbapenem resistance, one of the few classes of antibiotics effective against P. stuartii.
Historically P. stuartii has been susceptible to ciprofloxacin, but two recent studies show that approximately 67% of current isolates are now resistant (8, 30). Quinolone resistant P. stuartii are endemic in a number of long-term care facilities (42, 56); frequent use of quinolones to treat urinary tract infection in these facilities is a pre-disposing factor. A gene that provides quinolone resistance (qnrA) has been identified on a P. stuartii plasmid (47) and detected in several P. stuartii isolates (2, 44, 59). Quinolone resistance via qnrA is readily transferred from P. stuartii to susceptible bacteria (2, 8) and will likely contribute to the spread of resistance. This is particularly troublesome as transfer of qnrA can be coupled with transfer of genes encoding ESBLs and aminoglycoside-modifying enzymes (47, 59)
Providencia rettgeri Antibiotic Susceptibility
The antimicrobial susceptibility patterns of P. rettgeri are generally similar to those of P. stuartii. Resistance is common for penicillins (amoxicillin-clavulanic acid, ampicillin, ampicillin-sulbactam, and piperacillin/tazobactam), polymyxins (including colistin), and 1st and 2nd generation cephalosporins (9, 10, 23, 24, 46, 65, 72, 80, 84). Some strains are aminoglycoside-susceptible, although aminoglycoside resistance is fairly frequent (2, 10, 23, 24, 63, 72, 84). Most strains are susceptible to quinolones, 3rd generation cephalosporins, aztreonam, imipenem, and meropenem (20, 21, 65, 80). However, recent reports of multi-drug resistant P. rettgeri have identified strains resistant to carbapenems (imipenem and meropenem), quinolones (ciprofloxacin), 3rd generation cephalosporins (cefotaxime, ceftazidime, and ceftriaxone), and even 4th generation cephalosporins (cefepime) (2, 10, 23, 24, 40, 63, 72, 84).
ESBLs and CBLs have been reported in several P. rettgeri isolates (2, 9, 45, 63, 69, 72). A Japanese laboratory identified 3 isolates of P. rettgeri that produced a metallo-β-lactamase, an enzyme capable of hydrolyzing imipenem and meropenem (60). NDM-1 has also been detected in P. rettgeri isolates (10, 24, 72, 84), and a qnr gene for quinolone resistance has also recently been detected in P. rettgeri isolates from France and Nigeria (2, 26).
Antibiotic Susceptible of Other Providencia spp.
P. alcalifaciens and P. rustigianii are typically susceptible to ampicillin, cephalosporins, and aminoglycosides (31, 64). The P. alcalifaciens responsible for hemorrhagic pneumonia in piglets had at least intermediate resistance to several aminoglycosides (amikacin, spectinomycin, streptomycin, kanamycin), quinolones (ofloxacin, levofloxacin, and ciprofloxacin), some penicillins (penicillin, piperacillin, and oxacillin), chloramphenicol, vancomycin, trimethoprim-sulfamethoxazole, minocycline, furantoin, tetracycline, medemycin, erythromycin, clarithromycin, polymyxin, and cefazolin (75). The isolate was susceptible to ampicillin, some aminoglycosides (gentamycin, streptomycin, and tobramycin), aztreonam, 2nd generation cephalosporins (cefoxitin and cefuroxime), 3rd generation cephalosporins (ceftriaxone, cefotaxime, and ceftazidime), and 4th generation cephalosporins (cefepime).
ANTIMICROBIAL THERAPY
Drug of Choice
Based on emerging patterns of antimicrobial resistance, definitive therapy for infection due to P. stuartii or P. rettgeri requires appropriate antimicrobial susceptibility testing. Because of widespread resistance to multiple antimicrobials and emerging resistance to fluoroquinolones, third generation cephalosporins (cefotaxime, ceftriaxone, and cefepime should be considered first line therapy for infections due to these species. Although there is very little information upon which to base treatment recommendations for infections due to P. alcalifaciens, ampicillin or a 2nd generation cephalosporin would be a reasonable choice based upon in vitro susceptibility testing.
Specific Infections
Urinary Tract Infection: Infections due to P. stuartii or P. rettgeri may be treated with third-generation cephalosporins. Seriously ill patients, or those unable to take oral medications, should receive parenteral therapy. Appropriate regimens include ceftriaxone 1 gm daily, cefotaxime 1 gm every 6-8 hours, and cefepime 0.5 – 1 gm every 12 hours. Stable patients able to take oral medications may receive an oral expanded-spectrum cephalosporin such as cefixime 500 mg daily or cefpodoxime 200 mg every 12 hours. Oral cephalosporin therapy may be particularly appropriate for treatment of urinary tract infections in nursing home patients, in whom parenteral therapy may be impractical. Because urinary tract infections due to these organisms is nearly always complicated by catheterization or other anatomic or functional abnormality of the urinary tract, treatment duration should be 10-14 days.
Bacteremia: Bacteremic infection due to P. stuartii or P. rettgeri most frequently arises from the urinary tract, although bacteremia may occur secondary to pneumonia or burn wound infection. Patients should receive treatment with a third-generation cephalosporin as outlined above. As ESBL production by P. stuartii and P. rettgeri is on the rise, it would be reasonable to test blood isolates for ESBL production since it may not be detected by routine clinical laboratory susceptibility tests.
Enteritis: Enteritis due to P. alcalifaciens appears to be of mild-to-moderate severity in healthy adults and children. It is likely that the majority of infections resolve spontaneously without treatment; there are no published studies of therapy. It would be reasonable to treat patients with severe or prolonged diarrhea with ampicillin or amoxicillin, 500 mg four times daily.
Alternative Therapy
Infections Due to P. stuartii or P. rettgeri: Aztreonam is an appropriate alternative to cephalosporins in patients with cephalosporin allergy. Aminoglycosides are another alternative if the infecting isolate is susceptible, but resistance to multiple aminoglycosides is common. If the isolate produces an ESBL, imipenem or meropenem would be appropriate. Parenteral or oral quinolones could be considered based on susceptibility. However, frequent use of quinolones in a facility tends to foster widespread quinolone resistance among multiple different strains of Providencia. Thus routine quinolone use is not recommended.
Enteritis Due to P. alcalifaciens: Reasonable alternatives to ampicillin or a cephalosporin include certain aminoglycosides, aztreonam or tetracycline, based on the results of susceptibility testing.
ADJUNCTIVE THERAPY
Urinary catheters of patients with urinary tract infections should be removed or changed; this is particularly important for infections due to P. stuartii, since the continuing presence of adherent organisms on the catheter may provide a nidus for recurrent infection. Fluid and electrolyte replacement are essential in the treatment of P. alcalifaciens enteritis.
ENDPOINTS FOR MONITORING THERAPY
In patients with urinary tract infection and bacteremia, defervescence and clearing of the organism from the urine or blood are appropriate endpoints.
VACCINES
There are no available vaccines.
PREVENTION
Because of the strong association of Providencia urinary tract infections with urinary catheterization, avoidance of urinary catheterization, removal of catheters after they are no longer needed, appropriate catheter care, and hand hygiene by healthcare workers may reduce the transmission of Providencia spp. in hospitals and nursing homes. Although data are limited, safe food handling practices designed to prevent transmission of other enteric pathogens should be effective in preventing food-borne transmission of P. alcalifaciens.
REFERENCES
1. Acar JF, Goldstein FW. Trends in bacterial resistance to fluoroquinolones. Clin Infect Dis 1997;24:S67-73. [PubMed]
2. Aibinu IE, Pfeifer Y, Ogunsola F, Odugbemi T, Koenig W, Ghebremedhin B. Emergence of β-lactamases OXA-10, VEB-1 and CMY in Providencia spp. from Nigeria. J Antimicrobiol Chemother 2011;66:1931-1932. [PubMed]
3. Albert MH, Faruque AS, Mahalanbis D. Association of Providencia alcalifaciens with diarrhea in children. J Clin Microbiol 1998;36:1433-14345. [PubMed]
4. Albert MJ, Albert MJ, Ansaruzzaman M, Bhuiyan NA, Neogi PK, Faruque AS. Characteristics of invasion of HEp-2 cells by Providencia alcalifaciens. J Med Microbiol, 1995;42:186-90. [PubMed]
5. Albert MJ, Alam K, Ansaruzzaman M, Islam MM, Rahman AS, Haider K, Bhuiyan NA, Nahar S, Ryan N, Montanaro J, et al. Pathogenesis of Providencia alcalifaciens-induced diarrhea. Infect Immun, 1992: 60: 5017-24. [PubMed]
6. Armbruster CE, Smith SN, Yep A, Mobley HL. Increased Incidence of Urolithiasis and Bacteremia During Providencia mirabilis and Providencia stuartii Coinfection Due to Synergistic Induction of Urease Activity. J Infect Dis 2014;209:1524-1532.[PubMed]
7. Arpin C, Dubois V, Coulange L, Andre C, Fischer I, Noury P, Grobost F, Brochet JP, Jullin J, Dutilh B, Larribet G, Lagrange I, Quentin C. Extended spectrum β-lactamase-producing Enterobacterieaceae in Community and Private Health Centers. Antimicrob Agents Chemother 2003;47:3506-3514. [PubMed]
8. Arpin C, Thabet L, Yassine H, Messadi AA, Boukadida J, Dubois V, Coulange-Mayonnove L, Andre C, Quentin C. Evolution of an Incompatibility Group IncA/C Plasmid Harboring blaCMY-16 and qnrA6 Genes and Its Transfer through Three Clones of Providencia stuartii during a Two-Year Outbreak in a Tunisian Burn Unit. Antimicrob Agents Chemother 2012;56:1342-1349. [PubMed]
9. Barl P, Bedenić B, Sardelić S, Uzunović S, Vraneš J, Plečko V. Spread of CTX-M-15 positive Providencia spp. causing urinary tract infections at the University Hospital Split in Croatia. Med Glas (Zenica) 2012;9:317-24.[PubMed]
10. Barrios H, Garza-Ramos U, Reyna-Flores F, Sanchez-Perez A, Rojas-Moreno T, Garza-Gonzalez E, Llaca-Diaz JM, Camacho-Ortiz A, Guzmán-López S, Silva-Sanchez J. Isolation of carbapenem-resistant NDM-1-positive Providencia rettgeri in Mexico. J Antimicrob Chemother 2013;68:1934-1936[PubMed]
11. Bjurlin MA, O'Grady T, Kim DY, Divakaruni N, Drago A, Blumetti J, Hollowell CM. Causative pathogens, antibiotic sensitivity, resistance patterns, and severity in a contemporary series of Fournier's gangrene. Urology, 2013;81:752-8.[PubMed]
12.Bonfiglio G, Perilli M, Stefani S, Amicosante G, Nicoletti G. Prevalence of extended spectrum beta-lactamases among Enterobacteriaceae: an Italian survey. Int J. Antimicrob Agents 2002; 19:213-217. [PubMed]
13.Chlibek R, Jirous J, and Beran J. Diarrhea outbreak among Czech Army Field Hospital personnel caused by Providencia alcalifaciens. J Travel Med 2002; 9: 151-152. [PubMed]
14. Cornaglia G, Frugoni S, Mazzanariol A, Piacentini E, Berluscori A, Fontana R. Activities of oral antibiotics on Providencia strains isolated from institutionalized elderly patients with urinary tract infections, Antimicrob Agents Chemother 1995;39:2819-2921. [PubMed]
15.de Champs C, Monne C, Bonnet R, Sougakoff W, Sirot D, Chanal C, Sirot J. New TEM variant (TEM-92) produced by Providencia mirabilis and Providencia stuartii isolates. Antimicrob Agents Chemother 2001; 45:1278-1280. [PubMed]
16. Farmer JJ, Hickman FW, Brenner DJ, Schreiber M, Rickenbach DG.Unusual Enterobacteriaceae. "Providencia rettgeri" that "change" into Providencia stuartii. J Clin Microbiol, 1977;6:373-8.[PubMed]
17. Fierer J, Ekstrom M. An outbreak of Providencia stuartii urinary tract infections. Patients with condom catheters are a reservoir of the bacteria. JAMA 1981;245:1553-1555. [PubMed]
18. Fletcher M, Oppenheimer S, Warren JW. Colonization of urinary catheters by Escherichia coli and Providencia stuartii in a laboratory model system. J Urol 1994;152:232-236.[PubMed]
19. Fass RJ, Barnishan J, Ayers KW. Emergence of bacterial resistance to imipenem and ciprofloxacin in a university hospital. J Antimicrob Chemother 1995; 36:343-353. [PubMed]
20. Fu KP, Lafredo SC, Foleno B, Isaacson DM, Barrett JF, Tobia AJ, Rosenthale ME. In vitro and in vivo antibacterial activities of levofloxacin (l-ofloxacin), an optically active ofloxacin. Antimicrob Agents Chemother 1992;36:860-868. [PubMed]
21. Fung-Tomc J, Bush K, Minassian B, Kolek B, Flamm R, Gradelski E, Bonner D. Antibacterial activity of BMS-180680, a new catechol-containing monobactam. Antimicrob Agents Chemother 1997; 41:1010-1016. [PubMed]
22. Galac MR, Lazzaro BP. Comparative pathology of bacteria in the genus Providencia to a natural host, Drosophila melanogaster. Microbes Infect 2011;13:673-83. [PubMed]
23. Garbati MA, Bin Abdulhak A, Baba K, Sakkijha H. Infection due to colistin-resistant Enterobacteriacae in critically-ill patients. J Infect Dev Ctries, 2013;7:713-9.[PubMed]
24. Gefen-Halevi, S., et al., Isolation of genetically unrelated bla(NDM-1)-positive Providencia rettgeri strains in Israel. J Clin Microbiol, 2013. 51(5): p. 1642-3.[PubMed]
25. Godebo G. Kibru G, Tassew H. Multidrug-resistant bacterial isolates in infected wounds at Jimma University Specialized Hospital, Ethiopia. Ann Clin Microbiol Antimicrob, 2013;12:17.[PubMed]
26.Guillard T, Cambau E, Neuwirth C, Nenninger T, Mbadi A, Brasme L, Vernet-Garnier V, Bajolet O, de Champs C. Description of a 2,683-Base-Pair Plasmid Containing qnrD in Two Providencia rettgeri Isolates. Antimicrobial Agents and Chemotherapy, 2012;56:565-568.[PubMed]
27.Guth BE, Irino K, Trabulsi LR. Clonal structure of Providencia alcalifaciens strains isolated from diarrhoeal stools in Sao Paulo, Brazil. J Med Microbiol 1999; 48:205-209. [PubMed]
28. Guth BE, Perrella E. Prevalence of invasive ability and other virulence associated characteristics in Providencia alcalifaciens strains isolated in Sao Paulo, Brazil. J Med Microbiol 1996; 45:459-462. [PubMed]
29. Hawkey PM. Providencia stuartii: a review of a multiply antibiotic-resistant bacterium. J Antimicrob Chemother 1984;13:209-226. [PubMed]
30.Hayakawa K, Marchaim D, Divine GW, Pogue JM, Kumar S, Lephart P, Risko K, Sobel JD, Kaye KS. Growing prevalence of Providencia stuartii associated with the increased usage of colistin at a tertiary health care center. Int J Infect Dis, 2012;16:e646-8. [PubMed]
31. Hickman-Brenner FW, Farmer JJ, Steigerwalt AG, Brenner DJ. Providencia rustigianii: a new species in the family Enterobacteriaceae formerly known as Providencia alcalifaciens biogroup 3. J Clin Microbiol 1983;17:1057-1060. [PubMed]
32. Idowu OJ, Onipede AO, Orimolade AE, Akinyoola LA, Babalola GO. Extended-spectrum Beta-lactamase Orthopedic Wound Infections in Nigeria. J Glob Infect Dis, 2011;3:211-5. [PubMed]
33. Janda JM, Abbott SL, Woodward D, Khashe S. Invasion of HEp-2 and other eukaryotic cell lines by Providenciae: further evidence supporting the role of Providencia alcalifaciens in bacterial gastroenteritis. Curr Microbiol, 1998;37:159-65. [PubMed]
34. Johnson DE, Lockatell CV, Hall-Craigs M, Mobley HL, Warren JW. Uropathogenicity in rats and mice of Providencia stuartii from long-term catheterized patients. J Urol, 1987;138:632-5. [PubMed]
35. Jones BD, Mobley HL. Genetic and biochemical diversity of ureases of Providencia, Providencia, and Morganella species isolated from urinary tract infection. Infect Immun, 1987;55: 2198-203. [PubMed]
36. Juneja P, Lazzaro BP. Providencia sneebia sp. nov. and Providencia burhodogranariea sp. nov., isolated from wild Drosophila melanogaster. Int J System Evol Microbiol 2009;59:1108-1111. [PubMed]
37. Kessler RE, Fung-Tomc J. Susceptibility of bacterial isolates to Beta-lactam antibiotics from US clinical trials over a 5-year period. Am J Med 1996;100:13S-19S. [PubMed]
38. Klastersky J, Bogaerts AM, Noterman J, VanLaer e, Daneau D, Mouawad E. Infections caused by Providence bacilli. Scand J Infect Dis 1974;6:153-160. [PubMed]
39. Kocka FE, Srinivasan S, Mowjood M, Kantor HS. Nosocomial multiply resistant Providencia stuartii: a long-term outbreak with multiple biotypes and serotypes at one hospital. J Clin MicrobioI1980;11:167-169. [PubMed]
40. Kolar M, Urbanek K, Latal T. Antibiotic selective pressure and development of bacterial resistance. Int J Antimicrob Agents 2001; 17:357-363. [PubMed]
41. Lahlaoui H, et al., First detection of TEM-116 extended-spectrum beta-lactamase in a Providencia stuartii isolate from a Tunisian hospital. Indian J Med Microbiol, 2011. 29(3): p. 258-61.
42. Lee Y-L, Ceasario T, McCauley V, Filonis L, Pax A, Thrupp L. Low-level colonization and infection with ciprofloxacin-resistant gram-negaitve bacilli in a skilled nursing facility. Am J Infect Control 1998;26:552-557. [PubMed]
43. Linhares I, Raposo T, Rodrigues A, Almeida A. Frequency and antimicrobial resistance patterns of bacteria implicated in community urinary tract infections: a ten-year surveillance study (2000-2009). BMC Infect Dis 2013;13: 19. [PubMed]
44.Mahrouki S, Chihi H, Bourouis A, Ben Moussa M, Belhadj O. First characterization of a Providencia stuartii clinical isolate from a Tunisian intensive care unit coproducing VEB-1-a, OXA-2, qnrA6 and aac(6′)-Ib-cr determinants. The Brazilian Journal of Infectious Diseases, 2014;18:211-214 [PubMed]
45. Marchandin H, Carriere C, Sirot D, Pierre HJ, Darbas H. TEM-24 produced by four different species of Enterobacteriaceae including Providencia rettgeri, in a single patient. Antimicrob Agents Chemother 1999; 43:2069-2073. [PubMed]
46. Markowitz SM, Williams DS, Hanna CB, Parker JL, Pierce MA, Steele JC, Jr. A multicenter comparative study of the in vitro activity of fleroxacin and other antimicrobial agents. Chemotherapy 1995;41:477-486. [PubMed]
47. McGann P, Hang J, Clifford RJ, Yang Y, Kwak YI, Kuschner RA, Lesho EP, Waterman PE. Complete sequence of a novel 178-kilobase plasmid carrying bla(NDM-1) in a Providencia stuartii strain isolated in Afghanistan. Antimicrob Agents Chemother, 2012; 56:1673-9. [PubMed]
48. Miro E, Grünbaum F, Gómez L, Rivera A, Mirelis B, Coll P, Navarro F. Characterization of aminoglycoside-modifying enzymes in Enterobacteriaceae clinical strains and characterization of the plasmids implicated in their diffusion. Microb Drug Resist, 2013;19:94-9 [PubMed]
49. Mnif B, Ktari S, Chaari A, Medhioub F, Rhimi F, Bouaziz M, Hammami A. Nosocomial dissemination of Providencia stuartii isolates carrying bla OXA-48, bla PER-1, bla CMY-4 and qnrA6 in a Tunisian hospital. J Antimicrob Chemother, 2013;68: 329-32. [PubMed]
50. Mobley HL, Chippendale GR, Tenney JR, Mayrer A, Crisp U, Penner JL, Warren JW. MR/K hemagglutination of Providencia stuartii correlates with adherence to catheters and with persistence in catheter-associated bacteriuria. J Infect Dis 1988;157: 264-271. [PubMed]
51. Mobley HL, Chippendale GR, Fraiman MH, Tenney JH, Warren JW. Variable phenotypes of Providencia stuartii due to plasmid-encoded traits. J Clin Microbiol, 1985:22: 851-853. [PubMed]
52. Mobley HL, Jones BD, Jerse AE. Cloning of urease gene sequences from Providencia stuartii. Infect Immun, 1986;54:161-169. [PubMed]
53. Mobley, H.L.T., et al., Adherence to Uroepithelial Cells of Providencia stuartii Isolated from the Catheterized Urinary Tract. Journal of General Microbiology, 1986. 132(10): p. 2863-2872. [PubMed]
54. Muder RR, Brennen C, Drenning SD, Stout JE, Wagener MM. Multiply antibiotic-resistant gram-negative bacilli in a long-term-care facility: a case-control study of patient risk factors and prior antibiotic use. Infect Control Hosp Epidemiol 1997;18:809-813. [PubMed]
55 Muder RR, Brennen C, Wagener MM, Goetz AM. Bacteremia in a long term care facility: a five year prospective study of 163 consecutive episodes. Clin Infect Dis 1992; 14:647 654. [PubMed]
56. Muder RR, Brennen C, Goetz AM, Wagener MM, Rihs JD. Association with prior fluoroquinolone therapy of widespread ciprofloxacin resistance among gram-negative isoaltes in a Veterans' Affairs Medical Center. Antimicrob Agents Chemother 1991; 35:256-258. [PubMed]
57. Muller HE, O'Hara M, Fanning GR, Hickman-Brenner FW, Swenson JM, Brenner DL. Providencia heimbachae, a new specie of Enterobacteriaceae isolated from animals. Int J Syst Bacteriol 1986;36:252-256.
58. Murata T, Iida T, Shiomi Y, Tagomori K, Akeda Y, Yanagihara I, Mushiake S, Ishiguro F, Honda T. A large outbreak of foodborne illness attributed to Providencia alcalifaciens. J Infect Dis 2001;184:1050-1055. [PubMed]
59. Nazik H, Bektöre B, Öngen B, Özyurt M, Baylan O, Haznedaroğlu T. Co-expression of plasmid-mediated quinolone resistance-qnrA1 and blaVEB-1 gene in a Providencia stuartii strain. New Microbiol, 2011;34:225-8. [PubMed]
60. Nishio H, Komatsu M, Shibata N, Shimakawa K, Sueyoshi N, Ura T, Satoh K, Toyokawa M, Nakamura T, Wada Y, Orita T, Kofuku T, Yamasaki K, Sakamoto M, Kinoshita S, Aihara M, Arakawa Y. Metallo-β-lactamase-producing Gram-negative bacilli: laboratory-based surveillance in cooperation with 13 clinical laboratories in the Kinki region of Japan. J Clin Microbiol 2004;42:5256-5263. [PubMed]
61. O'Hara CO, Brenner FW, Miller JM. Classification, identification, and clinical significance of Providencia, Providencia, and Morganella. Clin Microbiol Rev 2000;13:534-536. [PubMed]
62. Otajevwo FD. Urinary tract infection among symptomatic outpatients visiting a tertiary hospital based in midwestern Nigeria. Glob J Health Sci, 2013;5:187-99. [PubMed]
63. Patel MH, Trivedi GR, Patel SM, Vegad MM. Antibiotic susceptibility pattern in urinary isolates of gram negative bacilli with special reference to AmpC beta-lactamase in a tertiary care hospital. Urol Ann, 2010;2:7-11. [PubMed]
64. Penner JL, Preston MA. Differences among Providencia species in their in vitro susceptibilities to five antibiotics. Antimicrob Agents Chemother 1980;18:868-871. [PubMed]
65. Pitkin DH, Sheikh W, Nadler H. Comparative in vitro activity of meropenem versus other extended-spectrum antimicrobials against randomly chosen and selected resistant clinical isolates tested in 26 North American centers. Clin Infect Dis 1997;24:S238-248. [PubMed]
66. Ramkumar R, et al. Description of Providencia vermicola isolated from diseased Indian major carp, Labeo rohita (Hamilton, 1822). Aquaculture, 2014;420–421:193-197.
67.Scapellato PG, Ormazabal C, Scapellato JL, Bottaro EG. Meningitis due to vancomycin-resistant Enterococcus faecium successfully treated with combined intravenous and intraventricular chloramphenicol. J Clin Microbiol, 2005;43:3578-9. [PubMed]
68. Senior BW. Media for the detection and recognition of the enteropathogen Providencia alcalifaciens in faeces. J Med Microbiol 1997;46:524-527. [PubMed]
69. Sheng WH, Badal RE, Hsueh PR. Distribution of extended-spectrum beta-lactamases, AmpC beta-lactamases, and carbapenemases among Enterobacteriaceae isolates causing intra-abdominal infections in the Asia-Pacific region: results of the study for Monitoring Antimicrobial Resistance Trends (SMART). Antimicrob Agents Chemother, 2013;57:2981-8. [PubMed]
70. Sipahi OR, Bardak-Ozcem S, Ozgiray E, Aydemir S, Yurtseven T, Yamazhan T, Tasbakan M, Ulusoy S. Meningitis due to Providencia stuartii. J Clin Microbiol, 2010;48:4667-8. [PubMed]
71. Somvanshi VS, Lang E, Sträubler B, Spröer C, Schumann P, Ganguly S, Saxena AK, Stackebrandt E. Providencia vermicola sp. nov., isolated from infective juveniles of the entomopathogenic nematode Steinernema thermophilum. Int J System Evol Microbiol, 2006;56:629-633. [PubMed]
72. Tada T, Miyoshi-Akiyama T, Dahal RK, Sah MK, Ohara H, Shimada K, Kirikae T, Pokhrel BM. NDM-1 Metallo-beta-Lactamase and ArmA 16S rRNA methylase producing Providencia rettgeri clinical isolates in Nepal. BMC Infect Dis, 2014;14:56. [PubMed]
73. Teiner A, Kocak Tufan Z, Akif Bayer M, Tascioglu T, Selim Erkoc Y, Hatipoglu C. Journal Neurological Research 2011, (http://www.neurores.org/index.php/neurores/article/view/14)
74. Tumbarello M, Citton R, Spanu T, Sanguinetti M, Romano L, Fadda G, Cauda R. ESBL-producing multidrug-resistant Providencia stuartii infection in a university hospital. J Antimicrob Chemother 2004;53:277-282. [PubMed]
75. Wang X, Wang J, Hao H, Qiu L, Liu H, Chen S, Dang R, Yang Z. Pathogenic Providencia alcalifaciens strain that causes fatal hemorrhagic pneumonia in piglets. Curr Microbiol, 2014;68: 278-84.[PubMed]
76. Warren JW. Providencia stuartii: a common cause of antibiotic-resistant bacteriuria in patients with long-term indwelling catheters. Rev Infect Dis, 1986;8:61-7.[PubMed]
77. Warren JW, Tenney JH, Hoopes JM, Muncie HL, Anthony WC. A Prospective Microbiologic Study of Bacteriuria in Patients with Chronic Indwelling Urethral Catheters. J Infect Dis, 1982;146:719-723. [PubMed]
78. Warren JW. Providencia stuartii: a common cause of antibiotic- resistant bacteriuria in patients with long-term indwelling catheters. Rev Infect Dis 1986;8:61-67. [PubMed]
79. Wenzel RP, Hunting KJ, Osterman CA, Sande MA. Providencia stuartii, a hospital pathogen: potential factors for its emergence and transmission. Am J Epidemiol 1976;104:170-180. [PubMed]
80. Wiseman LR, Wagstaff AJ, Brogden RN, Bryson HM. Meropenem. A review of its antibacterial activity, pharmacokinetic properties and clinical efficacy. Drugs 1995;1:73-101. [PubMed]
81. Woods TD, Watanakunakorn C. Bacteremia due to Providencia stuartii: review of 49 episodes. South Med J 1996;89:221-224. [PubMed]
82. Yee YC, Muder RR, Hseih MH, Lee TC. Molecular epidemiology of endemic ciprofloxacin-susceptible and –resistant Enterobacteriaceae. Infect Control Hosp Epidemiol. 1992;13:706-710. [PubMed
83. Zavascki AP, Carvalhaes CG, da Silva GL, Tavares Soares SP, de Alcântara LR, Elias LS, Sandri AM, Gales AC. Outbreak of Carbapenem-Resistant Providencia stuartii in an Intensive Care Unit. Infect Control Hosp Epidemiol 2012;33:627-630.[PubMed]
84. Zhou G, Guo S, Luo Y, Ye L, Song Y, Sun G, Guo L, Chen Y, Han L, Yang J. NDM-1-producing strains, family Enterobacteriaceae, in hospital, Beijing, China. Emerg Infect Dis, 2014;20:340-2. [PubMed]
Tables
Table 1.: Resistance of Providencia Species to Selected Antibiotics
| Antibiotics | aResistant Isolates/Total Number Tested (%) |
|---|---|
| Aminoglycosides: | |
| Amikacin | 285/307 (92.8%) |
| Gentamicin | 288/307 (93.8%) |
| Isepamicin | 262/282 (92.9%) |
| Netilmicin | 289/306 (94.4%) |
| Spectinomycin | NR |
| Streptomycin | NR |
| Tobramycin | NR |
| Carbapenems: | |
| Ertapenem | NR |
| Imipenem | 4/308 (1.4%) |
| Merepenem | NR |
| 1st Generation Cephalosporins: | |
| Cefazolin (Cephazolin) | 298/311 (95.8%) |
| Cephradine | 300/310 (96.8%) |
| 2nd Generation Cephalosporins: | |
| Cefoxitin | 26/308 (8.4%) |
| Cefuroxime | 32/317 (10.1%) |
| 3rd Generation Cephalosporins: | |
| Cefadizime | 3/269 (1.1%) |
| Cefotaxime (Cefatam) | NR |
| Ceftazidime | 0/313 (0%) |
| Ceftibuten | 0/313 (0%) |
| Ceftriaxone (Rocephin/Epicephin) | NR |
| 4th Generation Cephalosporins: | |
| Cefepime | 0/314 (0%) |
| Monbactams: | |
| Aztreonam | 16/310 (5.2%) |
| Nitrofurans: | |
| Nitrofurantoin | 268/307 (87.3%) |
| Penicillins: | |
| Amoxicillin | 311/314 (99.0%) |
| Amoxicillin-Clavulanic Acid (Augmentin) | 57/309 (18.4%) |
| Ampicillin | NR |
| Ampicillin-Sulbactam | NR |
| Piperacillin/Tazobactam | 80/300 (26.7%) |
| Pivmecillinam | 69/285 (24.2%) |
| Ticarcillin | NR |
| Quinolones: | |
| Ciprofloxacin | 57/312 (18.3%) |
| Fluoroquinolone | NR |
| Levofloxacin | NR |
| Lomefloxacin | 51/272 (18.7%) |
| Nalidixic Acid | NR |
| Norfloxacin | 59/307 (19.2%) |
| Ofloxacin | 60/310 (19.3) |
| Sulfonamides: | |
| Trimethoprim-sulfamethoxazole (Co-trimoxazole) | 70/303 (23.1%) |
| Polymyxins: | |
| Colistin (Polymyxin E) | NR |
| Polymyxin B | NR |
| Tetracyclines: | |
| Tetracycline | NR |
| Glycylcyclines: | |
| Tigecycline | NR |
| Dichloroacetic Acid Derivatives: | |
| Chloramphenicol | NR |
a319 isolates were included in the study; NR=not reported
Table 2. Antibiotic resistance of recent P. stuartii and P. rettgeri isolates
| Antibiotic | aP. stuartii | bP. rettgeri |
|---|---|---|
Resistant Isolates/Total Number Tested (%) |
||
| Aminoglycosides: | ||
| Amikacin | 71/1067 (6.6%) | 16/20 (80.0%) |
| Gentamicin | 649/1064 (61.0%) | 11/11 (100%) |
| Isepamicin | NR | NR |
| Netilmicin | NR | NR |
| Spectinomycin | 67/67 (100%) | NR |
| Streptomycin | 70/72 (97.2%) | NR |
| Tobramycin | 70/71 (98.6%) | NR |
| Carbapenems: | ||
| Ertapenem | 11/31 (35.5%) | NR |
| Imipenem | 11/32 (34.4%) | 15/23 (65.2%) |
| Merepenem | 11/1012 (1.1%) | 10/12 (83.3%) |
| 1st Generation Cephalosporins: | ||
| Cefazolin (Cephazolin) | 874/990 (88.3%) | NR |
| Cephradine | NR | NR |
| 2nd Generation Cephalosporins: | ||
| Cefoxitin | 13/21 (61.9%) | 11/14 (78.6%) |
| Cefuroxime | 486/989 (49.1%) | 5/7 (71.4%) |
| 3rd Generation Cephalosporins: | ||
| Cefadizime | NR | NR |
| Cefotaxime (Cefatam) | 19/20 (95.0%) | 6/7 (85.7%) |
| Ceftazidime | 140/1082 (12.9%) | 18/18 (100%) |
| Ceftibuten | NR | NR |
| Ceftriaxone (Rocephin/Epicephin) | 37/990 (3.7%) | 5/8 (62.5%) |
| 4th Generation Cephalosporins: | ||
| Cefepime | 71/1007 (1.7%) | 8/14 (57.1%) |
| Monobactams: | ||
| Aztreonam | 58/989 (5.9%) | 5/5 (100%) |
| Nitrofurans: | ||
| Nitrofurantoin | 6/6 (100%) | NR |
| Penicillins: | ||
| Amoxicillin | 68/72 (94.4%) | NR |
| Amoxicillin-Clavulanic Acid (Augmentin) | 6/6 (100%) | 5/6 (83.3%) |
| Ampicillin | 851/994 (85.6%) | 3/3 (100%) |
| Ampicillin-Sulbactam | 4/4 (100%) | 8/12 (66.7%) |
| Piperacillin/Tazobactam | 33/1002 (3.3%) | 16/18 (88.9%) |
| Pivmecillinam | NR | NR |
| Ticarcillin | 12/12 (100%) | NR |
| Quinolones: | ||
| Ciprofloxacin | 716/1071 (66.9%) | 12/12 (100%) |
| Fluoroquinolone | 11/11 (100%) | NR |
| Levofloxacin | 14/15 (93.3%) | 2/8 (25.0%) |
| Lomefloxacin | NR | NR |
| Nalidixic Acid | 18/18 (100%) | NR |
| Norfloxacin | NR | NR |
| Ofloxacin | NR | NR |
| Sulfonamides: | ||
| Trimethoprim-sulfamethoxazole (Co-trimoxazole) | 445/1068 (41.7%) | 2/3 (66.7%) |
| Polymyxins: | ||
| Colistin (Polymyxin E) | 4/4 (100%) | 15/15 (100%) |
| Polymyxin B | 11/11 (100%) | NR |
| Tetracyclines: | ||
| Tetracycline | 74/74 (100%) | NR |
| Glycylcyclines: | ||
| Tigecycline | NR | 6/10 (60.0%) |
| Dichloroacetic Acid Derivatives: | ||
| Chloramphenicol | 74/74 (100%) | NR |
a Compiled results for 1098 isolates from thirteen separate studies.
b Complied results for 25 isolates from eight separate studies.
NR=not reported
What's New
None
Guided Medline Search For:
Reviews
Baron EJ. Flow Diagram for Gram Neg Rods on BAP & MacConkey (NOT for stool isolates)
Review Article: Bush K, et al. MiniReview: Updated Functional Classification of β-lactamases. Antimicrob Agents Chemother 2010;54:969-976.
Review Article: Pitout JD. Enterobacteriaceae Producing ESBLs in the Community: Are They a Real Threat? Infect Med 2007;24:57-65.