Providencia Infections

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Providencia Infections

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The genus Providencia includes urease-producing gram-negative bacilli that are responsible for a wide range of human infections. Although most Providencia infections involve the urinary tract, they are also associated with gastroenteritis and bacteremia. [1] Providencia infections are uncommon and are usually nosocomial. They represent an emerging problem because of the increasing prevalence of antibiotic resistance secondary to extended-spectrum beta-lactamase (ESBL).

The first species of the genus now known as Providencia was isolated by Rettger in 1904. The bacterium was initially seen in chickens in what was believed to be an epidemic of fowl cholera. The bacterium was not further characterized until 1918, when it was named Bacterium rettgerii by Hadley et al. Organisms belonging to the genus Providencia have undergone many taxonomic changes since their first description, with frequent confusion and overlap between organisms of the closely related genera Providencia,Proteus, and Morganella.

Kauffmann first proposed the genus name Providencia in 1951, referring to a group of organisms studied by Stuart and colleagues at Brown University in Providence, Rhode Island. By 1983, the 4 species in the Providencia genus at that time were fully differentiated with DNA hybridization and urea hydrolyzation. In 1986, Providencia heimbachae was the fifth species discovered. [2]

The 5 species currently in the genus Providencia, in descending order of prevalence, include Providencia stuartii, Providencia rettgeri, Providencia alcalifaciens, Providencia rustigianii, and P heimbachae. [3]

Providencia species are found in multiple animal reservoirs, including flies, birds, cats, dogs, cattle, sheep, guinea pigs, and penguins, and are resident oral flora in reptiles such as pythons, vipers, and boas. Providencia species are also found commonly in soil, water, and sewage. Examples of Providencia infections in animals include neonatal diarrhea due to P stuartii infection in dairy cows and enteritis caused by P alcalifaciens infection in dogs. P rettgeri has been isolated in crocodiles with meningitis/septicemia and in chickens with enteritis. [4] P heimbachae has been isolated in penguin feces and an aborted bovine fetus. [5]

In humans, Providencia species have been isolated from urine (most common), stool, and blood, as well as from sputum, skin, and wound cultures. P stuartii septicemia is primarily of urinary origin. One case study has described P stuartii as the etiology of infective endocarditis. [6] Another case report found P rettgeri to be a cause of ocular infections, including keratitis, conjunctivitis, and endophthalmitis. [7]

P stuartii is frequently isolated in patients with indwelling urinary catheters and is known to persist in the urinary tract after bladder access is attained. In one study, the mean duration of bacterial colonization was 6.4 months. [8] The persistence of bacteria in the urinary tract is thought to be due to an adhesin, mannose-resistant/Klebsiella -like (MR/K) hemagglutinin, which allows bacteria to adhere to urinary catheters (mediated by 3 fimbriae). [8, 9] In a 1994 study by Rahav et al, persistence patterns in males and females were found to differ, with P stuartii showing more persistence in females. Reasons theorized include different receptor characteristics in male and female urinary tracts and a bacterial predilection for Foley catheters over condom catheters, which are used more commonly in males. [8]

ESBL-positive P stuartii is an increasing problem in hospitalized patients. In one study, 52% of 223 P stuartii isolates were found to be positive for ESBL in a hospital population that included ICU, medical, and surgical wards over a 4-year span. [10]

P alcalifaciens, P rettgeri, and P stuartii have been implicated in gastroenteritis. In one study, P rettgeri and P stuartii were found to be highly invasive using in vivo testing with Caco-2, a human colon carcinoma cell line. However, a common virulence plasmid was not identified in Providencia species. [11, 12] Providencia species, most commonly P agalactiae, have been demonstrated in the stool of symptomatic patients, although testing protocols used to identify diarrheagenic bacterial pathogens do not generally include Providencia.

United States

P stuartii and, to a lesser extent, P rettgeri are the most common Providencia species that cause human infection. While uncommon in most clinical settings, these organisms tend to cause cystitis in patients with bladder catheters and are primarily associated with complicated urinary tract infections. In a Canadian study in 2001, Providencia species were isolated in 18% of complicated urinary tract infections. [13] In contrast, Providencia bacteriuria in acute hospital settings is rare (0.3-1%). [8]

The prevalence of Providencia infections are generally low, although it is increasing. More significantly, Providencia infections with antimicrobial resistance patterns are increasing. In 2003, a study at an Italian university hospital with medical, surgical, and intensive care units found that the prevalence of ESBL-producing P stuartii in the general patient population increased from 31% in 1999 to 62% in 2002. Over a 4-year span, P stuartii was isolated in 0.08% of patients. Of these isolates, 87% were found in urine, 10% in blood, and 3% in respiratory tract secretions. [10]

P stuartii is most often found in complicated urinary tract infections in patients with chronic indwelling urinary catheters or condom catheters. Providencia species are rarely a cause of uncomplicated urinary tract infections. In a study of patients with urinary catheters living in a retirement home, P stuartii was the most commonly isolated bacteria, found in 59% of urine specimens. (The next most common was Escherichia coli, at 32%.) [8]

Providencia species, specifically P alcalifaciens and P rettgeri, have also been shown to be an infrequent cause of foodborne gastroenteritis. In 1996, a large outbreak of foodborne P alcalifaciens infections occurred in Japan at multiple schools, affecting student and teacher populations. [14] This was the first reported outbreak of foodborne P alcalifaciens gastroenteritis. Providencia species, especially P rettgeri, have also been implicated as cause of traveler’s diarrhea. In a Japanese study, 130 patients with diarrhea were evaluated at the Kansai Airport quarantine station, and Providencia species were isolated in 15.4% of stool samples. Most travelers who reported diarrhea had traveled to Southeast Asia. [11]

International

Providencia species are found worldwide. A study that examined ESBL-producing Enterobacteriaceae distribution worldwide (including Providencia species) found that the prevalence of ESBL-positive bacteria varied across geographical boundaries. The highest percentage of ESBL-positive isolates as found in Latin America (44%) and the lowest in Netherlands and Germany (2% and 2.6%, respectively). [15] . Another multidrug-resistant outbreak of Providencia stuartii was reported in Greece in 2012. [16]

The mortality rate in patients with Providencia bloodstream infection ranges from 6-33%. The rate is greater in polymicrobial infection.

All races appear to be equally susceptible to Providencia infection.

Males and females appear to be equally susceptible to Providencia infection. In one study, however, a significant difference was seen in the persistence pattern of bacteriuria in women versus men among nursing-home patients with long-term urinary catheterization (88.25% vs 50.5%). [8]

Elderly persons are at much greater risk of P stuartii or P rettgeri infection, most likely because these infections are associated with the use of indwelling urinary catheters, which are more common used in elderly populations.

P alcalifaciens gastroenteritis has been documented in children and adults. In a 2005 study, a large outbreak of gastroenteritis was found to be attributable to P alcalifaciens infection. The outbreak involved students and teachers of two kindergartens and one high school. The prevalence of infection was higher in children (53% of kindergartners affected vs 36% of adult teachers). [14] Another study demonstrated that P rettgeri infection is a potential cause of traveler’s diarrhea in adults. [11]

Armbruster CE, Smith SN, Yep A, Mobley HL. Increased incidence of urolithiasis and bacteremia during Proteus mirabilis and Providencia stuartii coinfection due to synergistic induction of urease activity. J Infect Dis. 2014 May 15. 209(10):1524-32. [Medline]. [Full Text].

O’Hara CM, Brenner FW, Miller JM. Classification, identification, and clinical significance of Proteus, Providencia, and Morganella. Clin Microbiol Rev. 2000 Oct. 13(4):534-46. [Medline].

Ovchinnikova OG, Rozalski A, Liu B, Knirel YA. O-antigens of bacteria of the genus providencia: structure, serology, genetics, and biosynthesis. Biochemistry (Mosc). 2013 Jul. 78(7):798-817. [Medline].

Janda, J. Michael, Abbott, Sharon. Enterobacteria 2nd edition. 2006. ASM Press:

Mohr O’Hara C, Steigerwalt AG, Green D, McDowell M, Hill BC, Brenner DJ, et al. Isolation of Providencia heimbachae from human feces. J Clin Microbiol. 1999 Sep. 37(9):3048-50. [Medline].

Krake PR, Tandon N. Infective endocarditis due to Providenca stuartii. South Med J. 2004 Oct. 97(10):1022-3. [Medline].

Koreishi AF, Schechter BA, Karp CL. Ocular infections caused by Providencia rettgeri. Ophthalmology. 2006 Aug. 113(8):1463-6. [Medline].

Rahav G, Pinco E, Silbaq F, Bercovier H. Molecular epidemiology of catheter-associated bacteriuria in nursing home patients. J Clin Microbiol. 1994 Apr. 32(4):1031-4. [Medline].

Darouiche RO. Device-associated infections: a macroproblem that starts with microadherence. Clin Infect Dis. 2001 Nov 1. 33(9):1567-72. [Medline].

Tumbarello M, Citton R, Spanu T, et al. ESBL-producing multidrug-resistant Providencia stuartii infections in a university hospital. J Antimicrob Chemother. 2004 Feb. 53(2):277-82. [Medline].

Yoh M, Matsuyama J, Ohnishi M, Takagi K, Miyagi H, Mori K, et al. Importance of Providencia species as a major cause of travellers’ diarrhoea. J Med Microbiol. 2005 Nov. 54:1077-82. [Medline].

Arpin C, Thabet L, Yassine H, Messadi A, Boukadida J, Dubois V, et al. 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 2-year Outbreak in a Tunisian Burn Unit. Antimicrob Agents Chemother. 2011 Dec 12. [Medline].

Nicolle LE. Urinary tract pathogens in complicated infection and in elderly individuals. J Infect Dis. 2001 Mar 1. 183 Suppl 1:S5-8. [Medline].

Murata T, Iida T, Shiomi Y, Tagomori K, Akeda Y, Yanagihara I, et al. A large outbreak of foodborne infection attributed to Providencia alcalifaciens. J Infect Dis. 2001 Oct 15. 184(8):1050-5. [Medline].

Luzzaro F, Mezzatesta M, Mugnaioli C, Perilli M, Stefani S, Amicosante G, et al. Trends in production of extended-spectrum beta-lactamases among enterobacteria of medical interest: report of the second Italian nationwide survey. J Clin Microbiol. 2006 May. 44(5):1659-64. [Medline].

Giakkoupi P, Tryfinopoulou K, Polemis M, Pappa O, Miriagou V, Vatopoulos A. Circulation of a multiresistant, conjugative, IncA/C plasmid within the nosocomial Providencia stuartii population in the Athens area. Diagn Microbiol Infect Dis. 2015 May. 82 (1):62-4. [Medline].

Asakura H, Momose Y, Ryu CH, Kasuga F, Yamamoto S, Kumagai S, et al. Providencia alcalifaciens causes barrier dysfunction and apoptosis in tissue cell culture: potent role of lipopolysaccharides on diarrheagenicity. Food Addit Contam Part A Chem Anal Control Expo Risk Assess. 2013. 30(8):1459-66. [Medline].

Mataseje LF, Boyd DA, Lefebvre B, Bryce E, Embree J, Gravel D, et al. Complete sequences of a novel blaNDM-1-harbouring plasmid from Providencia rettgeri and an FII-type plasmid from Klebsiella pneumoniae identified in Canada. J Antimicrob Chemother. 2014 Mar. 69(3):637-42. [Medline].

Prentice B, Robinson BL. A review of Providencia bacteremia in a general hospital, with a comment on patterns of antimicrobial sensitivity and use. Can Med Assoc J. 1979 Sep 22. 121(6):745-9. [Medline].

Albert MJ, Faruque AS, Mahalanabis D. Association of Providencia alcalifaciens with diarrhea in children. J Clin Microbiol. 1998 May. 36(5):1433-5. [Medline].

Hawkey PM. Providencia stuartii: a review of a multiply antibiotic-resistant bacterium. J Antimicrob Chemother. 1984 Mar. 13(3):209-26. [Medline].

Haynes J, Hawkey PM. Providencia alcalifaciens and travellers’ diarrhoea. BMJ. 1989 Jul 8. 299(6691):94-5. [Medline].

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 Jun. 17(6):1057-60. [Medline].

Kaslow RA, Lindsey JO, Bisno AL, Price A. Nosocomial infection with highly resistant, Proteus rettgeri. Report of an epidemic. Am J Epidemiol. 1976 Sep. 104(3):278-86. [Medline].

Krake PR, Tandon N. Infective endocarditis due to Providenca stuartii. South Med J. 2004 Oct. 97(10):1022-3. [Medline].

Matsuda T, Beppu T, Hirota M, et al. [A long-term surviving case of multiple metastatic liver tumors from rectal cancer treated with microwave coagulation therapy (MCT)]. Gan To Kagaku Ryoho. 1999 Oct. 26(12):1921-4. [Medline].

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 Mar. 14(3):647-54. [Medline].

Stock I, Wiedemann B. Natural antibiotic susceptibility of Providencia stuartii, P. rettgeri, P. alcalifaciens and P. rustigianii strains. J Med Microbiol. 1998 Jul. 47(7):629-42. [Medline].

Warren JW. Providencia stuartii: a common cause of antibiotic-resistant bacteriuria in patients with long-term indwelling catheters. Rev Infect Dis. 1986 Jan-Feb. 8(1):61-7. [Medline].

Wenzel RP, Hunting KJ, Osterman CA, Sande MA. Providencia stuartii, a hospital pathogen: potential factors for its emergence and transmission. Am J Epidemiol. 1976 Aug. 104(2):170-80. [Medline].

Woods TD, Watanakunakorn C. Bacteremia due to Providencia stuartii: review of 49 episodes. South Med J. 1996 Feb. 89(2):221-4. [Medline].

Edward Charbek, MD Fellow in Pulmonary/Critical Care Medicine, St Louis University Hospital

Disclosure: Nothing to disclose.

Nirav Patel, MD Assistant Professor of Internal Medicine, Division of Infectious Diseases, Allergy and Immunology, and Division of Pulmonary, Critical Care, and Sleep Medicine, St Louis University School of Medicine; Chief Medical Officer, Director of Antibiotic Stewardship, Infection Control Officer, St Louis University Hospital

Nirav Patel, MD is a member of the following medical societies: American Medical Association, Infectious Diseases Society of America, Infectious Diseases Society of St Louis, Missouri State Medical Association, Society for Healthcare Epidemiology of America

Disclosure: Nothing to disclose.

Francisco Talavera, PharmD, PhD Adjunct Assistant Professor, University of Nebraska Medical Center College of Pharmacy; Editor-in-Chief, Medscape Drug Reference

Disclosure: Received salary from Medscape for employment. for: Medscape.

Charles V Sanders, MD Edgar Hull Professor and Chairman, Department of Internal Medicine, Professor of Microbiology, Immunology and Parasitology, Louisiana State University School of Medicine at New Orleans; Medical Director, Medicine Hospital Center, Charity Hospital and Medical Center of Louisiana at New Orleans; Consulting Staff, Ochsner Medical Center

Charles V Sanders, MD is a member of the following medical societies: American College of Physicians, Alliance for the Prudent Use of Antibiotics, The Foundation for AIDS Research, Southern Society for Clinical Investigation, Southwestern Association of Clinical Microbiology, Association of Professors of Medicine, Association for Professionals in Infection Control and Epidemiology, American Clinical and Climatological Association, Infectious Disease Society for Obstetrics and Gynecology, Orleans Parish Medical Society, Southeastern Clinical Club, American Association for the Advancement of Science, Alpha Omega Alpha, American Association of University Professors, American Association for Physician Leadership, American Federation for Medical Research, American Geriatrics Society, American Lung Association, American Medical Association, American Society for Microbiology, American Thoracic Society, American Venereal Disease Association, Association of American Medical Colleges, Association of American Physicians, Infectious Diseases Society of America, Louisiana State Medical Society, Royal Society of Medicine, Sigma Xi, Society of General Internal Medicine, Southern Medical Association

Disclosure: Received royalty from Baxter International for other.

Mark R Wallace, MD, FACP, FIDSA Clinical Professor of Medicine, Florida State University College of Medicine; Clinical Professor of Medicine, University of Central Florida College of Medicine

Mark R Wallace, MD, FACP, FIDSA is a member of the following medical societies: American College of Physicians, American Medical Association, American Society for Microbiology, Infectious Diseases Society of America, International AIDS Society, Florida Infectious Diseases Society

Disclosure: Nothing to disclose.

Joshua S Hawley-Molloy, MD Staff Physician, Infectious Disease Service, Associate Program Director, Internal Medicine Residency, Department of Medicine, Tripler Army Medical Center

Joshua S Hawley-Molloy, MD is a member of the following medical societies: American College of Physicians, Infectious Diseases Society of America, Phi Beta Kappa, Armed Forces Infectious Diseases Society

Disclosure: Nothing to disclose.

Evan G Brown, DO Resident Physician, Department of Internal Medicine, Tripler Army Medical Center

Evan G Brown, DO is a member of the following medical societies: American College of Physicians and American Osteopathic Association

Disclosure: Nothing to disclose.

Kenneth C Earhart, MD Deputy Head, Disease Surveillance Program, United States Naval Medical Research Unit #3

Kenneth C Earhart, MD is a member of the following medical societies: American College of Physicians, American Society of Tropical Medicine and Hygiene, Infectious Diseases Society of America, and Undersea and Hyperbaric Medical Society

Disclosure: Nothing to disclose.

Leanne B Gasink, MD, MSc Assistant Professor, Department of Medicine and Faculty-Fellow, Center for Clinical Epidemiology and Biostatistics at the University of Pennsylvania School of Medicine; Associate Hospital Epidemiologist, Hospital of the University of Pennsylvania

Disclosure: Johnson and Johnson Salary Employment

Joshua S Hawley-Molloy, MD Staff Physician, Infectious Disease Service, Associate Program Director, Internal Medicine Residency, Department of Medicine, Tripler Army Medical Center

Joshua S Hawley-Molloy, MD is a member of the following medical societies: American College of Physicians, Armed Forces Infectious Diseases Society, Infectious Diseases Society of America, and Phi Beta Kappa

Disclosure: Nothing to disclose.

Ebbing Lautenbach, MD, MPH Director of Infection Control, Presbyterian Medical Center, Assistant Professor, Department of Medicine, Division of Infectious Disease, University of Pennsylvania School of Medicine

Ebbing Lautenbach, MD, MPH is a member of the following medical societies: American College of Epidemiology, American College of Physicians, Infectious Diseases Society of America, Society for Epidemiologic Research, and Society for Healthcare Epidemiology of America

Disclosure: Nothing to disclose.

Providencia Infections

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