Morganella species
Authors: Te-Yu Lin,M.D. Vivek Kak, M.D., Feng Yee Chang, Ph.D., M.D.
MICROBIOLOGY
Morganella is the third member of the tribe Proteeae. Proteus and Providencia are the other members of this tribe and share some of the biochemical and clinical characteristics (8, 9).
In 1906 Morgan described a non-lactose fermenting organism in children with summer infantile diarrhea. This bacterium came to be known as Morgan’s bacillus and was later classified as Bacillus morganii (55). Independently Castellani isolated a bacterium while studying a case of fever in 1905 in Colombo, Sri Lanka. In 1914 he described this bacteria along with two others as Bacterium Columbense (12). Later in 1943 Fulton would classify these strains into the genus Morganella (27). In 1992 using DNA hybridization Jensen et al. defined two subspecies of Morganella (33).
Morganella are motile, non-lactose fermenting gram-negative bacteria, which share with Proteus the capacity for urease production and presence of phenylalanine deaminase. They can be separated from Proteus species by the lack of swarming activity or gelatin liquefaction or H2S production. Morganella species can ferment mannose and have the enzyme ornithine decarboxylase which Proteus lack (24). Two subspecies, M. morganii subsp. Morganii and M. morganii subsp. Siboniiwith four and three biogroups respectively can be differentiated based on biochemical and genetic features (60).
EPIDEMIOLOGY
Morganella species are infrequent causes of disease in healthy individuals. Morganella morganii was originally thought to be a cause of summer diarrhea. The organism has been isolated along with Proteus mirabalis more frequently in patients with diarrhea than in healthy controls (57). M. morganii is found in the environment and in the intestinal tracts of humans, mammals, and reptiles as part of the normal flora (23). Therefore, most M. morganii bacteremia cases were opportunistic community-acquired infections. M. morganii bacteremia is not common and only accounts for 0.69% of bacteremia reported by Lee et al (41). Custovic et al found 3.6% of M. morganii bacteremia among nosocomial infections in newborns (17).
CLINICAL MANIFESTATIONS
Clinical infections due to M. morganii often involve the urinary tract, skin and soft tissue and hepatobiliary tract (42). Urinary tract infection is the most common clinical infection site. Most often these occur in elderly patients in nursing homes with long-term indwelling catheters (84). Morganella is the fifth leading cause of UTIs in nursing home patients (59). In a study of 20 patients with chronic indwelling urinary catheters, Warren et al. found Morganella bacteriuria in 19% of weekly specimens with a mean duration of bacteriuria of 3.3 weeks (83). In a prospective monitoring of all Morganella cultures in a VA microbiology laboratory 60% of isolates were from the urine, 18% from wounds and the remaining 22% from a variety of body fluids or tube drainage (49).
Morganella usually causes skin and soft tissue infections. Falagas reported 13 patients (54%) suffered from skin and soft tissue infections in a 4-year period at Greece hospital (23). In a retrospective review of 19 cases of Morganella bacteremia McDermott found that 37% were related to wound infections (49).
Morganella could also cause intra-abdominal infections. The portals of entry of M. morganii bacteremia involved hepatobiliary tract was 22% by Lee report during one-year period (41). In a retrospective review of 61 cases of M. morganii bacteremia, Kim found that 64% were related to intra-abdominal infections (included biliary infection, liver abscess and peritonitis) (38).
Morganella may rarely cause bacteremia. In a multicenter study of 2084 cases of bacteremia in Britain, Morganella accounted for 1% of cases and 4 deaths (46). Morganella has been reported as the cause of up to 3% of bacteremias in a nursing home, arising primarily from either the urinary tract or soft tissue infections (56).
Morganella species have been isolated in diabetic foot infections (65), necrotizing fasciitis (40), decubitus ulcer infections (56), septic arthritis (39, 75), meningitis (30, 47, 74), otitis media (29), gastroenteritis (2), peritonitis and bacteremia (28, 33), chorioamnionitis (11, 34), pericarditis (58) and neonatal sepsis (33, 71, 73). Isolated case reports have implicated Morganella species in pyomyostis (3), and tubo-ovarian abscess (13, 68). A case of Morganella pericarditis in a bone marrow transplant patient has also been reported (77).
LABORATORY DIAGNOSIS
Definitive diagnosis of Morganella infections requires isolation of the bacteria in the clinical laboratory. Morganella grow as flat, colorless 2- to 3-mm colonies on MacConkey’s and sheep-blood agar. However current commercial database systems used in subspecies identification have only M. morganii subsp. morganii listed in their database so far. The phenotypic separation of the Morganella subspecies can be done by the inability of M. morganii subsp. sibonii to ferment the sugar trehalose (60).
The matrix-assisted laser desorption ionization time-of- flight mass spectrometry (MALDI-TOF MS) is a rapid, accurate, and cost-effective method of microbial characterization and identification (15, 22).This technology generates characteristic mass spectral fingerprints, that are unique signatures for each microorganism and are thus ideal for an accurate microbial identification at the genus and species levels and has a potential to be used for strain typing and identification.
PATHOGENESIS
The ability of Morganella to cause infections in the urinary tract may be due to the MR/K hemagglutinin that enhances adherence to urinary catheters (53). Additionally, Morganella produces a urease that predisposes to encrustation of urinary catheters (78). The Morganella urease also can be activated at a low pH, which may enhance the bacterial survival at low pH (90). Morganella species may also produce a hemolysin, which enhances virulence by lysing erythrocytes due to the formation of hydrophilic pores in the cell wall (86).
SUSCEPTIBILITY IN VITRO AND IN VIVO
Beta-Lactam Antibiotics
Resistance to β-lactam antibiotics in Morganella species is usually mediated by the presence of chromosomally encoded β-lactamases belonging to the AmpC β-lactamase family. These β-lactamases are typically inducible in the presence of β-lactam antibiotics (10), with only trace amounts being produced in the absence of antibiotics. In the presence of enzyme-inducing antibiotics these enzymes may lead to expression of high-level resistance. As a result, agents such as ampicillin, amoxicillin, and "first-generation" cephalosporins are ineffective. "Second-generation" cephalosporins such as cefuroxime are also ineffective against Morganella with MIC90s ranging from 16 to 64 mg/mL (6, 46, 79, 85). Cefoxitin, though a potent beta-lactamase inducer appears more stable against Morganella than Enterobacter (44).
A second mechanism of β-lactam resistance in Morganella is the chromosomally mediated hyperproduction of β-lactamases. These strains have mutations at the ampD locus leading to stable derepression of the β-lactamase gene and permanent production of excessive enzyme levels. These derepressed strains continuously produce β-lactamase without a need for an inducing antibiotic (89). The sequence of the gene encoding one of these β-lactamases has been published (4). The extended-spectrum penicillins and "third-generation" cephalosporins are generally not active against Morganella strains that are constitutive hyperproducers of β-lactamases. Addition of clavulanic acid or sulbactam to these agents fails to enhance their activity against derepressed organisms. Thus the MICs of ticarcillin and ticarcillin-clavulanate against Morganella are the same (25). Tazobactam, on the other hand, enhances the activity of piperacillin against derepressed strains. Hence, the combination of piperacillin plus tazobactam is five times more active than piperacillin alone (44).
The third-generation cephalosporins ceftriaxone, cefotaxime, and ceftazidime are more active against Morganella, with MIC90s ranging from 0.03 to 32 mg/mL (7). The MICs for cefotaxime and ceftazidime are 0.015 and 0.06 mg/mL for inducible strains but 4 and 8 mg/mL for constitutive hyperproducers, respectively (44).
The most active β-lactam antibiotics against the derepressed and inducible isolates are cefipime and cefpirome. These agents are the most β-lactamase stable and have MICs against the derepressed isolates of 1 to 4 mg/mL versus more than 64 mg/mL for cefotaxime (44). Cefipime appears to be the most active cephalosporin (MIC90s, 0.03-0.25 mg/mL). Washington found MIC90s to cefipime below 1mg/mL for all isolates (85); Kessler found that 100% of isolates had MICs below 8 mg/mL and that cefipime was more active than ceftazidime, ceftriaxone, or imipenem (37). This increase in cefipime activity is due to an increased resistance to enzymatic hydrolysis compared to the other cephalosporins. MICs for aztreonam range between 0.06 and 0.12 mg/mL (61). Jean found remarkably high imipenem-non-susceptible rates were documented for M. morganii in 2009 (32). Meropenem appears to be the most active of the carbapenems, and is active even against some imipenem-resistant isolates (67). The new carbapenem ertapenem at a concentration of 4mg/mL inhibited 100% of isolates of AmpC-producing Morganella morganii (54).
A third mechanism of resistance of β-lactam resistance in Morganella strains is due to extended-spectrum β-lactamase (ESBL) production. ESBLs are plasmid-mediated enzymes that can confer resistance to third generation cephalosporins such as cefotaxime, ceftriaxone, ceftazidime as well as the monobactamaztreonam but are generally susceptible to β-lactam + β-lactamase inhibitor combinations. The carbapenems however still maintain their activity against ESBL-producing strains of Morganella. The occurrence of ESBLs in Morganella morganii has been reported (16, 69), and a few have been characterized at the molecular level (5, 81). Since 1990,Morganella isolates possessing the extended spectrum TEM-13, TEM-10, TEM-21 and TEM-72 enzymes have been reported (5, 50, 64, 81). In a 1992 survey of 1000 isolates of Enterobacteriaceae, Liu found several Morganella isolates possessing SHV, TEM, or OXA plasmid-mediated β-lactamases (43).
Non β- Lactam Antibiotics
Aminoglycosides are usually active against Morganella (19). Between 71 and 100% of Morganella isolates from the Medical College of Virginia remained susceptible to aminoglycosides (45). At the Mayo Clinic, 91 and 98% of 163 isolates of M. morganii were reported susceptible to less than 2 mg/mL of gentamicin and less than 8 mg/mL of amikacin, respectively (20). Aminoglycoside resistance among Morganella is rare and mediated by a variety of complex combinations of enzymes, the most frequent of which is the modifying enzyme ANT(2")- I which confers resistance to gentamicin, tobramycin, and kanamycin (52).
The fluroquinolones are highly active against Morganella, with the MIC90s for most isolates below 0.25 mg/mL (26, 46, 79). Ciprofloxacin is twice as active as ofloxacin in vitro (46). In a study of 390 clinical isolates, 97% were ciprofloxacin susceptible (1). Decreased quinolone uptake has been described in laboratory mutants of Morganella, due to enhanced efflux as well as decreased permeability of the quinolones in those strains (18).
Trimethoprim-sulfamethoxazole is also active against some Morganella (MIC50s-0.06 mg/mL; MIC90s 16 mg/mL) (46).
ANTIMICROBIAL THERAPY
Therapeutic choices for infections due to Morganella are primarily based upon in vitro susceptibility data, since little information is available from clinical trials. The antibiotic of choice depends upon the site of infection, the nature of the host and the local pattern and prevalence of resistance.
Specific Infections
Bacteremia
Initial therapy for patients with suspected bacteremia due to Morganella should be selected on the basis of local susceptibility patterns. A third-generation cephalosporin has been suggested as the drug of choice for Morganella infections (51). This recommendation certainly holds for initial empirical treatment for Morganella infections in areas where local susceptibility patterns indicate absence of ESBL producing strains. However, while using these drugs, clinicians need to be aware of a potential drug resistance to emerge in vivo due to the constitutive production of the AmpC β-lactamase as has been seen in Enterobacter (14). Addition of an aminoglycoside to a cephalosporin may decrease the potential of emergence of resistance to broad-spectrum cephalosporins (36). In areas where bacteremia may be due to presence of an ESBL producing strain, the carbapenems should be regarded as drugs of choice (62). The published experience in using carbapenems against ESBL producing organisms is most with imipenem though meropenem appears to be more active than it in-vitro (67). Ertapenem also has good in vitro activity against Morganella (54). In addition to a cell wall active agent, some physicians would recommend combination therapy with the addition of an aminoglycoside active against Morganella in cases of bacteremia.
For patients with allergy to β-lactams and or carbapenems an attractive option would be the use of quinolones such as ciprofloxacin. In general the newer quinolones offer no therapeutic advantage over ciprofloxacin for treatment of Morganella infections. In the future though, increasing in-vitro resistance to the quinolones by ESBL producing organisms may limit this option. Another option for susceptible strains would be the use of high dose trimethoprim-sulfamethoxazole and aminoglycosides.
The exact duration of treatment for these infections has not been studied but a course of at least 2 weeks appears reasonable.
Urinary Tract Infection
UTI’s due to Morganella should be treated with oral quinolones like ciprofloxacin. The absence of high levels of resistance so far to this class of drugs in Morganella makes this an attractive choice. Other options include the third generation cephalosporins and trimethoprim-sulfamethoxazole.
For UTI’s caused by ESBL-producing strains of Morganella a quinolone still is probably the drug of choice, though there have been several reports of urinary tract infection due to ESBL-producing organisms being successfully treated with cephalosporins, despite the results of in-vitro susceptibility tests (24). Other treatment options for these infections include trimethoprim-sulfamethoxazole (for susceptible strains) or carbapenems.
In cases of uncomplicated UTI’s due to Morganella a course of 3 to 5 days of therapy should be adequate; however Morganella UTI’s are generally associated with complicating features such as indwelling catheters. In such cases the duration of therapy should be at least 2 to 3 weeks.
Wound Infection
Nosocomial wound infections can often be due to Morganella species (28, 49, 87). These infections can be polymicrobial or monobacterial in origin. An important caveat in management of these infections is adequate debridement of the infected tissues. In general these infections should be treated with the use of a broad-spectrum agent such as piperacillin-tazobactam. Other options include the use of third generation cephalosporins like ceftriaxone, cefipime or a quinolone with an antianaerobic drug. For infections caused by an ESBL-producing strain, the drug of choice is generally a carbapenem. The once daily administered, ertapenem is an attractive option in severe wound infections caused by ESBL producing strains of Morganella morganii.
Intra-abdominal Infection
Morganella species are often involved in intra-abdominal infections (41). These infections can be polymicrobial or mixed with anaerobic bacteria. Treatment emphasizes the importance of adequate drainage or removal of the infected tissues. Broad-spectrum antibiotic such as piperacillin-tazobactam was the first choice; other options include the use of third generation cephalosporins like ceftriaxone, cefipime or a fluoroquinolone. Carbapenem, especially meropenem or ertapenem was indicated if ESBL-producing strain was considered.
Neonatal Infections
Though Morganella species are an extremely rare cause of neonatal infections, recently increasing case reports have implicated this organism as a cause of neonatal brain abscess (82), neonatal sepsis, as well as necrotising fascitis (40). It is thought that the neonate acquires the infection probably from overt or subtle chorioamnionitis in the mother. The other risk factor of acquisition of these bacteria in a neonate may be use of ampicillin as prophylactic therapy during pregnancy. Antibiotic therapy of these infections in a neonate should be with a combination of a third generation cephalosporin such as cefotaxime and an aminoglycoside.
Underlying Diseases
The majority of infections caused by Morganella are in patients who have been hospitalized and may have urinary catheters or intravenous lines or wounds that can get infected (8, 61, 63, 80). Other cases have been reported in individuals with underlying immune defects due to diabetes, AIDS, splenectomy, Hodgkin’s disease, cirrhosis of liver, solid organ malignancy and autoimmune disease (42).
Alternative Therapy
In general use of alternative drugs for treatment of Morganella infections must be guided by the isolated organisms in-vitro susceptibility pattern. The use of combination therapy using a β-lactam antibiotic with an aminoglycoside has been traditionally used in serious Morganella infections although no data exists from controlled studies supporting such a practice.
ADJUNCTIVE THERAPY
Besides optimal antibiotics, adjunctive therapy is important for treatment of Morganella infections. The urinary catheter should be replaced in urinary tract infections. Intravenous lines should also be replaced in cases of bacteremias and wounds should be adequately debrided. In cases of diabetic foot infections due to Morganella the vascular supply of the infected areas should be assessed to determine the presence of any arterial insufficiency.
ENDPOINTS OF THERAPY
In general once appropriate therapy is initiated against Morganella infections, patients, if febrile initially, should defervesce in 48-72 hours. In cases of urinary tract infections failure to defervesce should prompt an evaluation of the kidney to exclude any obstruction to the collecting system and or any abscesses. Deep wound infections should also be evaluated for any underlying osteomyelitis. Generally there is little need for follow-up cultures to document bacteriological cure if the patient responds clinically.
VACCINES
There are no vaccines in development against Morganella.
PREVENTION OR INFECTION CONTROL MEASURES
Over the last few years the antibiotic susceptibility of Morganella species has gradually shown a trend towards increased resistance, with certain strains also showing the presence of ESBLs. In areas where ESBL-producing organisms have been recently documented, infection control methods should be implemented to limit spread of these organisms. These may include checking for rectal colonizers of these organisms, vigorous handwashing practices, use of contact isolation for infected or colonized patients. If there are multiple different clones of ESBL producing organisms in a hospital, changes in antibiotic use policy in the hospital may have a role in decreasing the number of these organisms (70).
REFERENCES
1. Acar JF, Goldstein FW. Trends in bacterial resistance to fluoroquinolones.Clin Infect Dis 1997;24 (Suppl 1):S67-732. [PubMed]
2. Ahren CM, Jertborn M, Herclik L, Kaijser B, Svennerholm AM. Infection with bacterial enteropathogens in Swedish travellers to Southeast Asia -a prospective study.Epidemiol Infect 1990; 105:325-333. [PubMed]
3. Arranz-Caso JA, Cuadrado-Gomez LM, Romanik-Cabrera J, Garcia-Tena J. Pyomyositis caused by Morganella morganii in a patient with AIDS. Clin Infect Dis 1996;22:372-373. [PubMed]
4. Barnaud G, Arlet G, Danglot C, Philippon A. Cloning and sequencing of the gene encoding the AmpC β-lactamase of Morganella morganii. FEMS Micrbiol Letters 1997;148:15-20. [PubMed]
5. Barroso H, Freitas-Vieira A, Duarte A. Molecular characterization of a Ceftazidime- Resistant Morganella morganii isolate producing a TEM-10 β-lactamase. Antimicrob Agents Chemother 1999;43:434-435. [PubMed]
6. Biedenbach DJ, Jones RN, Erwin ME. Interpretive accuracy of the disk diffusion method for testing newer orally administered cephalosporins against Morganellamorganii. J ClinMicrobiol 1993;31:2828-2830. [PubMed]
7. Binfiglio G, Stefani S, Nicoletti G. In vitro activity of cefpirome against beta-lactamase- inducible and stably derepressed Enterobacteriaceae.Chemotherapy 1994; 40: 311-316. [PubMed]
8. Braunstein H, Tomasulo M. Identification of Proteus morganii and distinction from other Proteus species. Am J ClinPathol 1975;69:905-908. [PubMed]
9. Brenner DJ, Farmer JJ 3rd, Fanning GR, Steigerwalt AG, Klykken P, Wathen HG, Hickman FW, Ewing WH. Deoxyribonucleic acid relatedness of Proteus andProvidencia. Int J SystBacteriol 1978;28:269-282.
10. Bush K, Jacoby GA, Medeiros AA. A functional classification scheme for beta-lactamases and its correlation with molecular structure.Antimicrob Agents Chemother 1995;39:1211- 1233. [PubMed]
11. Carmona F, Fabregues F, Alvarez R, Vila J, Cararach V. A rare case of chorioamnionitis by Morganella morganii complicated by sepsis and ARDS.Eur J ObstetGynecolReprodBioI 1992;45:67-70. [PubMed]
12. Castellani A. Notes on cases of fever due to Bacterium Columbense. Zentbl Bakteriol Parasitenkd Infektionskr Hyg I Org. 1914;74:197-200.
13. Chou YY, Chiu SK, Lai HC, Chang FY. Tubo-ovarian abscess with Morganella morganii bacteremia. J Microbiol Immunol Infect. 2009;42:357-9. [PubMed]
14. Chow JW, Fine MJ, Shlaes DM, Quinn JP, Hooper DC, Johnson MP, Ramphal R, Wagener MM, Miyashiro DK, Yu VL. Risk factors for emergence of resistance to broad-spectrum cephalosporins among Enterobacter spp. Ann Intern Med 1991 Oct 15;115:585-90. [PubMed]
15. Croxatto A, Prod'hom G, Greub G. Applications of MALDI-TOF mass spectrometry in clinical diagnostic microbiology. FEMS Microbiol Rev. 2012;36:380-407. [PubMed]
16. Coudron PE, Moland ES, Sanders CC. Occurrence and detection of extended-spectrum β- lactamases in members of the family Enterobacteriaceae at a veterans affair medical center: seek and you may find. J ClinMicrobiol 1997;35:2593-2597. [PubMed]
17. Custović A, Hadzić S. Epidemiology of bacterial intrahospital infections in newborns]. Med Arh. 2008;62(5-6):294-7. [PubMed]
18. del Mar Tavio M, Vila J, Ruiz J, Manuel Martin Sanchez A, Teresa Jimenez de Anta M. Decreased permeability and enhanced proton-dependent active efflux in the development of resistance to quinolones in Morganella morganii. Int J Antimicrob Agents 2000;14:157- 160. [PubMed]
19. DiPersio JR, Krafczyk TL. In vitro activity of netilmicin, gentamicin, tobramycin and amikacin against glucose fermenting and nonfermenting bacteria. Chemotherapy 1980;26:323. [PubMed]
20. Edson RS, Terrell CL. The aminoglycosides. Mayo ClinProc 1991;66:1158. [PubMed]
21. Emery CL, Weymouth LA. Detection and clinical significance of extended-spectrum β- lactamases in a tertiary-care medical center. J ClinMicrobiol 1997;35:2061-2067. [PubMed]
22. Emonet S, Shah HN, Cherkaoui A, Schrenzel J. Application and use of various mass spectrometry methods in clinical microbiology. Clin Microbiol Infect. 2010;16:1604-13. [PubMed]
23. Falagas ME, Kavvadia PK, Mantadakis E, Kofteridis DP, Bliziotis IA, Saloustros E, Maraki S, Samonis G Morganella morganii infections in a General Tertiary Hospital. Infection 2006;34:315-321. [PubMed]
24. Farmer JJ III. Enterobacteriaceae: introduction and identification. In: Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH, eds. Manual of clinical microbiology. 6th ed. Washington, DC: American Society for Microbiology, 1995:438-449.
25. Fuchs PC, Barry AL, Jones RN. In vitro activity and disk susceptibility of Timentin: Current status. Am J Med 1985;(Suppl 5B):25-32. [PubMed]
26. Fuchs PC, Barry AL, Sewell DL. Antibacterial activity of WY- 49605 compared with those of the other oral agents and selection of disk content for disk diffusion and susceptibility testing. Antimicrob Agents Chemother 1995;39:1472-1479. [PubMed]
27. Fulton M. The identity of Bacterium columbensis Castellani. J Bacteriol 1943;46:79-82.
28. Gebhart-Mueller Y, Mueller P, Nixon B. Unusual case of postoperative infection caused by Morganella morganii. J Foot Ankle Surg 1998;37:145-147. [PubMed]
29. Haddad J Jr, Inglesby TV Jr, Addonizio L. Head and neck infections in pediatric cardiac transplant patients. Ear Nose Throat J 1995;74:422-425. [PubMed]
30. Isaacs RD, Ellis-Pegler RB. Successful treatment of Morganella morganii meningitis with pefloxacinmesylate. J AntimicrobChemother 1987;20:769-770. [PubMed]
31. Isobe H, Motomura K, Kotou K, Sakai H, Satoh M, Nawata H. Spontaneous bacterial empyema and peritonitis caused by Morganella morganii. J ClinGastroenterol 1994;18:87- 88. [PubMed]
32. Jean SS, Hsueh PR, Lee WS, Yu KW, Liao CH, Chang FY, Ko WC, Wu JJ, Chen YH, Chen YS, Liu JW, Lu MC, Liu CY, Lam C, Chen RJ. Carbapenem susceptibilities and non-susceptibility concordance to different carbapenems amongst clinically important Gram-negative bacteria isolated from intensive care units in Taiwan: results from the Surveillance of Multicentre Antimicrobial Resistance in Taiwan (SMART) in 2009. Int J Antimicrob Agents. 2013;41:457-62. [PubMed]
33. Jensen KT, Frederiksen W, Hickman-Brenner FW, Steigerwalt AG, Riddle CG, Brenner DJ. Recognition of Morganella subspecies, with proposal of of Morganella morganii subsp.morganii subspnov. andand Morganella morganii subsp. Sibonii subsp. Nov. Int J SystBacteriol 1992;42:613-620. [PubMed]
34. Johnson JR, Feingold M. Case of chorioamnionitis in an immunocompetent woman caused by Morganella morganii. J Maternal-fetal Med 1998;7:13-14. [PubMed]
35. Katz LM, Lewis RJ, Borenstein DG. Successful joint arthroplasty following Proteus morganii (Morganella morganii) septic arthritis: a four-year study. Arthritis Rheum 1987;30:583-585. [PubMed]
36. Kaye KS, Cosgrove S, Harris A, Eliopoulos GM, Carmeli Y. Risk factors for emergence of resistance to broad-spectrum cephalosporins among Enterobacter spp.Antimicrob Agents Chemother 2001;45:2628-30. [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(SuppI 6A):13S-19S. [PubMed]
38. Kim BN, Kim NJ, Kim MN, Kim YS, Woo JH, Ryu J. Bacteremia due to tribe Proteeae: a review of 132 cases during a decade (1991-2000). Scand J Infect Dis 2003;35:98-103. [PubMed]
39. Koyuncu Ş, Ozan F. Morganella morganii osteomyelitis complicated by secondaryseptic knee arthritis: a case report. Acta Orthop Traumatol Turc.2012;46:464-7. [PubMed]
40. Krebs VL, Koga KM, Diniz EM, Ceccon ME, Vaz FA. Necrotizing fasciitis in a newborn infant: a case report. Rev HospClinFac Med Sao Paulo 2001;56:59-62. [PubMed]
41. Lee IK, Liu JW. Clinical characteristics and risk factors for mortality in Morganella morganii bacteremia. J Microbial Immunol Infect 2006;39:328-334. [PubMed]
42. Lin TY, Chan MC, Yang YS, Lee Y, Yeh KM, Lin JC, Chang FY. Clinical manifestations and prognostic factors of Morganella morganii bacteremia. Eur J Clin Microbiol Infect Dis. 2014 Aug 9. [PubMed]
43. Liu PY, Gur D, Hall LM, Livermore DM. Survey of the prevalence of beta-lactamases amongst 1000 gram-negative bacilli isolated consecutively at the Royal London Hospital. J AntimicrobChemother 1992;30:429-447. [PubMed]
44. Livermore DM. Beta-lactamases in laboratory and clinical resistance. ClinMicrobiol Rev 1995;8:557-584. [PubMed]
45. Markowitz SM. Urinary tract specimens. In: Dalton HP, Nottebart HC, eds. Interpretive medical microbiology. New York: Churchill Livingstone, 1986:564-570.
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. Mastroianni A, Coronado O, Chiodo F. Morganella morganii meningitis in a patient with AIDS. J Infect 1994;29:356-357. [PubMed]
48. Maheshwari A, Dutta S, Kumar P, Narang A. Early onset mixed Morganella and Klebsiella sepsis In a neonate. Indian J Pediatr 2001;68:671-672. [PubMed]
49. McDermott C, Mylotte JM. Morganella morganii: epidemiology of bacteremic disease. Infect Control 1984;5:131-137. [PubMed]
50. Medeiros AA. Evolution and dissemination of beta-lactamases accelerated by generations of beta-lactam antibiotics.Clin Infect Dis 1997;24(SI)SI9-45. [PubMed]
51. Medical Letter. The choice of antibacterial drugs. Med Lett 1996;38:25-30. [PubMed]
52. Miller GH, Sabatelli FJ, Hare RS, Glupczynski Y, Mackey P, Shlaes D, Shimizu K, Shaw KJ. The most frequent aminoglycoside resistance mechanisms-changes with time and geographic area: a reflection of aminoglycoside usage patterns? Clin Infect Dis 1997;24(Suppl 1):S46-62. [PubMed]
53. Mobley HL, Chippendale GR, Tenney JH, Mayrer A, Crisp LJ, 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;151: 264-271. [PubMed]
54. Moland ES, Thomson KS. In vitro activity of MK-0826 against well characterized strains of enterobacteriaceae which produce ESBLs and/or AmpC beta-lactamases. 40th Interscience Conference on Antimicrobial Agents and Chemotherapy 2000; Abstract 383.
55. Morgan HR. Upon the bacteriology of the summer diarrhea of infants. Br Med J 1906;1:908-912. [PubMed]
56. 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]
57. Muller HE. Occurrence and pathogenic role of Morganella-Proteus-Providentia group bacteria in human feces. J Clin Microbiol 1986;23:404-405. [PubMed]
58. Nakao T, Yoshida M, Kanashima H, Yamane T. Morganella morganii Pericarditis in a Patient with Multiple Myeloma. Case Rep Hematol. 2013;2013:452730. [PubMed]
59. Nicolle LE, Strausbaugh LJ, Garibaldi RA. Infections and antibiotic resistance in nursing homes. Rev Clin Microbiol 1996;9:1-17. [PubMed]
60. O’Hara CM, Brenner FW, Miller JM. Classification, Identification, and clinical significance of Proteus, Providentia and Morganella. Clin Microbiol Rev 2000; 13(4):534- 546. [PubMed]
61. Parry MF. Aztreonam susceptibility testing.A retrospective analysis. Am J Med 1990;88(3C);7S-11S. [PubMed]
62. Paterson DL. Recommendation for treatment of severe infections caused by enterobacteriaceae producing extended-spectrum β-lactamases (ESBLs).Clin Microbiol Infect 2000;6:460-463. [PubMed]
63. Penner JL, Hennessy JN. O-antigen grouping of Morganella morganii (Proteus morganii) by slide agglutination. J Clin MicrobioI 1979;10:8-13. [PubMed]
64. Perilli M, Segatore B, de Massis MR, Riccio ML, Bianchi C, Zollo A, Rossolini GM, Amicosante G. TEM-72, a new extended-spectrum beta-lactamase detected in Proteus mirabilis and Morganella morganii in Italy. Antimicrob Agents Chemother2000;44:2537-2539. [PubMed]
65. Pereira A, Monteagudo J, Mazzara R, Reverter JC, Castillo R. Anti-KI of the IgA class associated with Morganella morgariii infection. Transfusion 1989;29:549-551. [PubMed]
66. Piddock LJ, Walters RN, Jin YF, Turner HL, Gascoyne-Binzi DM, Hawkey PM. Prevalence and mechanism of resistance to 'third-generation' cephalosporins in clinically relevant isolates of Enterobacteriaceae from 43 hospitals in the U.K., 1990-1991 J Antimicrobial Chemother 1997;39:177-187. [PubMed]
67. 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]
68. Pomeranz A, Korzets Z, Eliakim A, Pomeranz M, Uziel Y, Wolach B. Relapsing Henoch- Schonleinpurpura associated with a tubo-ovarian abscess due to Morganellamorganii. Am J Nephrol 1997;17:471-473. [PubMed]
69. Power P, Radice M, Barberis C, de Mier C, Mollerach M, Maltagliatti M, Vay C, Famigletti A, Gutkind G. Cefotaxime-hydrolysing Beta lactamases in Morganellamorganii. Eur J Clin Microbiol Infect Dis 1999;18:743-747. [PubMed]
70. Rahal JJ, Urban C, Horn D. Class restriction of cephalosporins use to control total cephalosporins resistance in nosocomial Klebsiella. JAMA 1998;280:1233-1237. [PubMed]
71. Ranu SS, Valencia GB, Piecuch S. Fatal early onset infection in an extremely low birth weight infant due to Morganella morganii. J Perinatal 1999;19:533-535. [PubMed]
72. Riess G, Andres J, Thornber D, Wise R. In vitro activity of RU 29246, the active compound of the cephalosporin prodrug HR 916.Antimicrob Agents Chemother 1992;36:2360-2364. [PubMed]
73. Salen PN, Eppes S. Morganella morganii, a newly reported rare cause of neonatal sepsis. Acad Emerg Med 1997;4:711-714. [PubMed]
74. Samonis G, Anatoliotaki M, Apostolakou H, Souglakos J, Georgoulias V. Fatal septicemia and meningitis due to Morganella morganii in a patient with Hodgkin’s disease. Scand J Infect Dis 2001;33:553-555. [PubMed]
75. Schonwetter RS, Orson FM. Chronic Morganella morganii arthritis in an elderly patient. J ClinMicrobiol 1988;26:1414-1415. [PubMed]
76. Sewell D, Barry A, Allen S, Fuchs P, McLaughlin J, Pfaller M. Comparative antimicrobial activities of the penem WY -49605 (SUN5555) against recent clinical isolates from five US medical centers. Antimicrob Agents Chemother 1995;39:1591-1595. [PubMed]
77. Sica S, Di Mario A, Salutari P, d’Onofrio G, Antinori A, Chiusolo P, Leone G. Morganella morganii pericarditis after resolventsplenectomy for immune pancytopenia following allogenic bone marrow transplantation for acute lymphoblastic leukaemia. Clin Infect Dis 1995;21:1052-1053. [PubMed]
78. Stamm W. Catheter-associated urinary tract infections: Epidemiology, pathogenesis, and prevention. Am J Med 1991; (3B):65S-71S.[PubMed]
79. Stock I, Wiedemann B. Identification and natural antibiotic susceptibility of Morganella morganii. DiagnMicrobiol Infect Dis 1998;30:153-165. [PubMed]
80. Tucci V, Isenberg HD. Hospital cluster epidemic with Morganella morganii. J ClinMicrobiol 1981;14:563-566. [PubMed]
81. Tessier F, Arpin C, Allery A, Quentin C. Molecular characterization of a TEM-21 β- lactamase in a clinical isolate of Morganella morganii. Antimicrob Agents Chemother 1998;42:2125-2127. [PubMed]
82. Verboon-Maciolek M, Vandertop WP, Peters AC, Roord JJ, Geelen SP. Neonatal brain abscess caused by Morganella morganii. Clin Infect Dis 1995;20:471. [PubMed]
83. 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]
84. Warren JW. Catheter-associated bacteriuria in long term care facilities. Infect Control Hosp EpidemioI 1994;15:557-562. [PubMed]
85. Washington JA, Jones RN, Gerlach EH, Murray PR, Allen S, Knapp CC. Multicenter comparison of in vitro activities of FK037, cefepime, ceftriaxone, ceftazidime, and cefuroxime. Antimicrob Agents Chemother 1993;37:1696-1700. [PubMed]
86. Welch RA. Identification of two different hemolysin determinants in uropathogenic Proteus isolates. Infect Immun 1987;55:2183-2190. [PubMed]
87. Williams EW, Hawkey PM, Penner JL, Senior BW, Barton LJ. Serious nosocomial infection caused by Morganella morganii and Proteus mirabilis in a cardiac surgery unit. J Clin Microbiol 1983;18;5-9. [PubMed]
88. 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]
89. Yang Y, Livermore DM. Chromosomal β-lactamase expression and resistance to β-lactam antibiotics in Proteus vulgaris and Morganella morganii. Antimicrob Agents Chemother 1988;32:1385-1391. [PubMed]
90. Young GM, Amid D, Miller VL. A bifunctional urease enhance survival of pathogenic Yersinaenterocolitica and Morganella morganii at low pH. J Bacteriol 1996;178:6487- 6495. [PubMed]
Tables
TABLE 1. Comparative Activity of Antibiotic Against Morganella morganii
| Antibiotic | No. Isolates | MIC50 | MIC90 |
|---|---|---|---|
| Amoxicillin | 9 | 128 | 128 |
| Amoxicillin-clavulanate | 39 16 | 64 >64 | >64 >64 |
| Ticarcillin | 165 | <1 | 16 |
| Ticarcillin-clavulanate | 165 | <1 | 16 |
| Cefaclor | 16 39 | >64 >64 | >64 >64 |
| Cefuroxime | 39 39 62 | >64 >64 >16 | >64 >64 >16 |
| Cefoxitin | 9 39 | 16 8 | 512 >64 |
| Cefixime | 19 16 | 0.008 2 | 0.008 32 |
| Cefpodoxime | 19 | 0.06 | 0.5 |
| Ceftriaxone | 39 33 | 0.5 <0.03 | 8 2 |
| Cefotaxime | 9 33 | 8 0.06 | 16 2 |
| Ceftazidime | 9 62 33 | 8 <0.25 0.25 | 32 <0.25 2 |
| Cefipime | 62 33 | <0.25 0.03 | <0.25 0.12 |
| Cefoperazone | 33 | 1 | 16 |
| Imipenem | 33 | 2 | 4 |
| TMP-SMXa | 39 | 0.06 | 16 |
| Fleroxacin | 39 | 0.06 | 0.12 |
| Ciprofloxacin | 39 | 0.06 | 0.06 |
| Ofloxacin | 39 | 0.12 | 0.25 |
| Lomefloxacin | 39 | 0.12 | 0.25 |
a TMP-SMX, trimethoprim-sulfamethoxazole.
Adapted from references 9, 20,29,34,52,58,62,70 by Orenstein R, Wong ES. Morganella Species- In: Yu VL, MerriganJr TC, Barriere SL. Antimicrobial Therapy and Vaccines. Wilkins and Wilkins .1999.
TABLE 2. Recommendation For Treatment Of Infections Caused By Morganella.
| Site of Infection | Non-ESBL-Producing | ESBL-Producing | ||
|---|---|---|---|---|
| 1st Line | 2nd Line | 1st Line | 2nd Line | |
| Bacteremia | III Generation Cephalosporin a | Ciprofloxacinb | Carbapenemsc | Ciprofloxacin |
| Urinary Tract Infection | Ciprofloxacin | III Generation Cephalosporin a | Ciprofloxacin | III Generation Cephalosporin a |
| Adult Dose | |
|---|---|
| aIII Generation Cephalosporin | |
| Cefotaxime | 1-2 gm I.V q. 8h. |
| Ceftriaxone | 1-2 gm/ I.V q. day |
| bCiprofloxacin | |
| 500-750 mg orally b.i.d. | |
| 400 mg I.V b.i.d. | |
| cCarbapenem | |
| Meropenem | 0.5-1 gm I.V q8-12h. |
| Imepenem | 0.5-1 gm I.V q.6-8h |
| Ertapenem | 0.5-1 gm I.V qd |
| Doripenem | 0.25-0.5 gm I.V q.8-12h |
*In vitro data showed ESBL producing strain more susceptible to meropenem; in vivo data was not available.
What's New
Lin TY, et al. Clinical manifestations and prognostic factors of Morganella morganii bacteremia. Eur J Clin Microbiol Infect Dis 2014 Aug 9 [Epub ahead of print].
Guided Medline Search For:
Reviews
Cennimo DJ, Koo H, Mohamed JA, Huang DB, Chiang T. Enteroaggregative Escherichia coli: A Review of Trends, Diagnosis, and Treatment. Infect in Med 2007;24:100-110.
Pitout JD. Enterobacteriaceae Producing ESBLs in the Community: Are They a Real Threat? Infect Med 2007;24:57-65.