INTRODUCTION

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The genus Leminorella consists of gram-negative bacilli belonging to the family Enterobacteriaceae and was first described as enteric group 57 in 1982. The generic name is derived from Leon Le Minor, a French microbiologist who has made many contributions to enteric bacteriology as the head of the National Salmonella Center of France. Although strains of Leminorella spp. share the general properties of Enterobacteriaceae, they exhibit only 3 to 16% DNA homology to other bacteria in this family. Based on genetic differences, they are divided into three taxa: Leminorella grimontii, L. richardii, and Leminorella sp. strain 3 (2).

Strains of Leminorella spp. are easy to culture and identify. They are facultative anaerobes which grow on sheep blood and MacConkey agar and are negative for D-mannose fermentation and positive for tyrosine hydrolysis, hydrogen sulfide production, and L-arabinose fermentation.

The clinical significance of Leminorella spp. is not clear. There are no reports of infections caused by Leminorella spp., and their incidence in clinical specimens is unknown. We initiated this study to investigate the occurrence, clinical significance, infection spectrum, and antimicrobial susceptibility of Leminorella spp. in a tertiary care hospital.

	MATERIALS AND METHODS

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The study was conducted in the Tel Aviv Sourasky Medical Center, a 1,150-bed tertiary care teaching hospital with approximately 70,000 patient admissions per year. The microbiology laboratory processes over 82,500 clinical specimens annually. Identification of gram-negative organisms (including Leminorella spp.) and susceptibility testing were performed by an automated system (Microscan; Dade Behring Inc., West Sacramento, Calif.) using a combined gram-negative identification panel and an automated microbroth dilution method (Neg/Urine Combo Panel; Microscan). Criteria for identification acceptance were >85% agreement (in accordance with manufacturer recommendations). Identification of blood isolates was also confirmed by API 20. Criteria for resistance were evaluated in accordance with National Committee for Clinical Laboratory Standards guidelines. Records of the Microbiology Laboratory for the period spanning 1 January 1997 to 30 April 1999 were searched retrospectively for recovery of Leminorella spp. from clinical specimens. The medical records of patients identified by this search were reviewed, and data were entered into a prepared questionnaire. To define infections, we used a modification of Centers for Disease Control and Prevention guidelines (modified to include community-acquired infections and exclude asymptomatic bacteriuria) (1). An isolate was classified as a definite pathogen if the patient had symptoms and signs of infection at the site of isolation and no other pathogen was isolated from that site, as a probable pathogen if the patient had symptoms and signs of infection at the site of isolation but the culture yielded polymicrobial growth or if the Leminorella sp. was a single isolate but the signs and symptoms of infection were not definitely related to the site of isolation, as a possible pathogen if signs and symptoms of infection were evident but not clearly related to the site of isolation, and as a nonpathogen if there was no evidence of infection at the time of isolation.

	RESULTS

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During the 28 months surveyed, Leminorella spp. were identified in clinical specimens from 18 patients, representing an incidence of 11 cases per 100,000 patient admissions. There was no clustering of cases by time or place. The medical records of 14 of the patients were available for review. The mean age was 67 (range, 10 to 88) years, and 78% of the patients were male. In 12 of 14 cases, Leminorella spp. were isolated after more than 72 h (average, 11 days) in the hospital. In one case, they were isolated from a patient undergoing chemotherapy who had intensive contact with the health care system, and in one case, the isolate appeared to have been community acquired.

Patients' characteristics and clinical syndromes are summarized in Table 1. Signs and symptoms of infection were evident in 13 of the 14 patients studied. Site-specific signs and symptoms included dysuria in patients with urinary tract infections (UTI), purulent sputum production, rales on physical examination of patients with lower respiratory tract infections, and purulent drainage, localized tenderness, and redness in patients with soft tissue infections. The systemic signs and symptoms of infection were as follows: fever in 57% leukocytosis in 43%, and leukopenia in 7% of the patients at the time that the Leminorella sp. was present. In 43% of the cases, Leminorella spp. were isolated from polymicrobial cultures. Three patients had an additional focus of infection other than the site of isolation of Leminorella sp. Using clinical criteria, Leminorella sp. was classified as a definite pathogen in six (43%) cases, a probable pathogen in four (29%) cases, and a possible pathogen in three (21%) cases. In one case (7%), Leminorella spp. had no clinical significance.

Urine was the most common site of isolation. In all cases, urine colony counts were >100,000 CFU/ml. In six of the seven patients, pyuria was present (>25 erythrocytes per high-power field). In three of the seven cases, Leminorella sp. was classified as a definite pathogen. Three patients had an indwelling urinary catheter, and two had recurrent UTI. Indeed, the most common clinical syndrome caused by Leminorella spp. was UTI, which occurred in six patients (43%). In five cases, it was the only pathogen isolated from urine and one patient had a polymicrobial UTI in which the copathogen was Acinetobacter baumanii.

In four patients, Leminorella sp. was isolated from wounds. Three of these patients had undergone surgical procedures prior to isolation of the organism. Two had surgical site infections following orthopedic surgery (not in a cluster). The first was a 43-year-old man who developed a wound infection with Leminorella spp. 7 days following repair of a fractured tibia. The second was an 85-year-old female who developed a wound infection 18 days after repair of a fractured hip. In the latter case, both Leminorella spp. and coagulase-negative staphylococci were isolated from the wound. The other two patients with wound infections were a 59-year-old man with post coronary artery bypass graft Staphylococcus epidermidis sternal osteomyelitis who developed a superinfection with Leminorella spp. and a 56-year-old man with pyoderma gangrenosum who had a soft tissue infection of a lower limb ulcer. In this case, Leminorella spp., S. aureus, and a group A beta-hemolytic streptococcus were isolated from the wound and the Leminorella sp. was classified as a possible pathogen.

The only case of bacteremia was that of a 10-year-old boy with acute myeloid leukemia who had postchemotherapy neutropenia and fever. No other pathogen was isolated at that time, and no localizing signs or symptoms were present. Leminorella sp. was isolated from two out of the three sets of blood samples drawn. We defined this case as primary bacteremia, and Leminorella sp. was classified as a definite pathogen.

A case of secondary peritonitis occurred in a 75-year-old male with diabetes mellitus who had been operated on for a mesenteric vascular event and had a leak from the anastomotic site. The patient developed signs and symptoms of peritonitis and underwent a "second-look" laparotomy. Leminorella sp. was the only organism isolated from the peritoneal fluid.

A case of lower respiratory tract infection involved a 79-year-old female with anoxic brain damage after a myocardial infarction. The patient was mechanically ventilated for a prolonged time. She produced copious amount of purulent sputum in association with fever and leukocytosis. Her chest radiograph was clear, and her sputum grew Leminorella spp., Klebsiella pneumoniae, and coagulase-negative staphylococci.

Antimicrobial susceptibility. The susceptibilities of the 18 isolates to 15 antimicrobial agents are summarized in Table 2. The isolates were uniformly susceptible to imipenem. Beta-lactam agents (with the exception of imipenem) had poor activity against Leminorella sp. isolates. One-half of the isolates or fewer were susceptible to the following agents: ampicillin, piperacillin (and their combination with a beta-lactamase inhibitor), expanded- and broad-spectrum cephalosporins (62% were susceptible to ceftazidime), and aztreonam. Similarly, the two fluoroquinolones which were tested (levofloxacin and ciprofloxacin) had poor activity. Over half of the isolates were resistant to gentamicin. In contrast, amikacin showed very good activity with intermediate susceptibility in only one isolate.

	DISCUSSION

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Automated systems identify microorganisms based on multiple biochemical tests and computer analysis. Such systems are gaining popularity because of their ease of use and their ability to process a large number of specimens in a relatively short time. Taxa which were not identified to the species level in the past are now more frequently identified. For some of these "new" organisms, the lack of clinical correlates poses a clinical dilemma for the physician. Leminorella spp. are such species.

To date, Leminorella spp. have been recovered from stool and urine only, with no clinical correlates (2). Our study establishes Leminorella spp. as clinically relevant organisms causing primarily UTI, surgical site infection, peritonitis, bacteremia, soft tissue infection, and probably also lower respiratory tract infection.

Leminorella sp. was cultured almost exclusively after the patients were hospitalized for over 72 h, suggesting that it be considered a nosocomial pathogen. The organisms exhibited resistance to multiple antibiotic agents, with uniform susceptibility only to imipenem and amikacin.

Leminorella sp. infections tended to affect patients compromised by underlying conditions or those with invasive devices and procedures. Seventy-one percent of the patients from whose urine Leminorella spp. were isolated had an indwelling urinary catheter or recurrent UTI. Three of four patients from whose wounds Leminorella spp. were isolated had undergone a surgical procedure a few days before the culture was taken. Leminorella spp. were isolated from the sputum of only one patient. This patient has been mechanically ventilated for a long time before the isolation of Leminorella spp.

Retrospective study data should be viewed with caution. Isolates were not available for further investigation and identification to the species level. However, given the unique phenotypic profile of Leminorella spp. (hydrogen sulfide and L-arabinose positive, urea and lipase negative), errors in identification were very unlikely. Moreover, all of the isolates but one shared a typical antibiotic susceptibility pattern. Salmonella sp. is the only organism reported to be misidentified as a Leminorella sp. (3), but the clinical setting of our patients is not compatible with Salmonella sp. infection. Another limitation of a retrospective design is difficulty in distinguishing between infecting and colonizing organisms. To overcome this obstacle, we employed a set of suitable predefined criteria.

We conclude that Leminorella spp. should be considered significant nosocomial pathogens capable of causing a variety of clinical syndromes which could prove refractory to routine antimicrobial therapy.