Primary Shewanella alga Septicemia in a Patient on Hemodialysis

Abstract

We report the first Japanese case of primary septicemia with Shewanella alga and also describe the bacteriological characteristics of and results of antibiotic susceptibility tests of the isolate. S. alga was repeatedly isolated, at times simultaneously with Escherichia coli, from the blood of a 64-year-old female undergoing hemodialysis. The isolated organism was determined to be S. alga based on recently published identification criteria, such as hemolysis on sheep blood agar, no acid production from carbohydrates, and growth on agar containing 6.5% NaCl. Results of antibiotic susceptibility tests demonstrated that the isolate was sensitive to levofloxacin and cefpirome (MICs, ≤0.063) but resistant to cefazolin, ceftizoxime, and imipenem (MICs, >128, 64, and 8 μg/ml, respectively). Although the role of S. alga as a human pathogen has not been fully determined, accumulating data suggest that this organism may be a potential pathogen, especially in compromised hosts.

CASE REPORT

We report here a case of primary Shewanella alga septicemia and describe the bacteriological characteristics of and antibiotic susceptibility results for the organism. A 64-year-old female patient on hemodialysis for 5 years was admitted to the hospital because of a 5-day history of general fatigue and high-grade fever. Her symptoms progressively deteriorated despite the use of oral cefpodoxime proxetil. The patient denied having been exposed to any fresh or salt water, insect bites, or trauma or having traveled recently. Body temperature on admission was 39.4°C, and severe malaise was observed. Physical examination demonstrated no specific signs of infections or skin manifestations. Laboratory tests on admission showed a level of C-reactive protein of 4.2 mg/dl (normal range, 0 to 0.2 mg/dl), a leukocyte count of 6,300/mm³ (normal range, 4,000 to 9,000/mm³), a platelet count of 80,000/mm³ (normal range, 150,000 to 400,000/mm³), and no signs of liver damage. Blood cultures were collected, and then cefazolin (2 g/day), gentamicin (40 mg/day), and levofloxacin (100 mg/day) were empirically started. On the second and third days after admission, S. alga and Escherichia coli were separately or concurrently isolated from multiple blood culture bottles. No other pathogenic organisms were isolated from several other specimens, including urine, stool, and sputum. The level of C-reactive protein in serum increased to 20.9 mg/dl on the third day, but clinical symptoms and laboratory results returned to normal thereafter. On day 7, antibiotics were changed to minocycline (100 mg/day), cefpirome (1 g/day), and levofloxacin (100 mg/day) based on the results of broth microdilution antibiotic sensitivity testing (Table 1). The patient was discharged from the hospital 25 days after admission.

TABLE 1.

Results of antibiotic susceptibility testing against isolates in this study

Antibiotic	MIC (μg/ml) for:
	S. alga	E. coli
Piperacillin	1	1
Imipenem	8	0.125
Cefazolin	>128	1
Ceftizoxime	64	≦0.063
Cefpirome	≦0.063	≦0.063
Gentamicin	2	2
Minocycline	0.125	1
Levofloxacin	≦0.063	≦0.063

The blood culture isolate was a nonfermentative gram-negative rod that was motile and oxidase positive. The organism was identified with 99% certainty as Shewanella putrefaciens with the VITEK System (bioMerieux Vitek, Inc., Hazelwood, Mo.). Recent changes in taxonomy have suggested that several strains of previously reported S. putrefaciens probably were S. alga since general identification systems, such as the VITEK and the API 20NE systems, cannot distinguish between S. alga and S. putrefaciens (3). Therefore, additional biochemical and bacteriological tests were performed to correctly identify the organism. Species identification as S. alga in this report was based on the criteria of Nozue et al. (11), and the results are shown in Table 2.

TABLE 2.

Bacteriological characteristics of the Shewanella organism isolated from our patient

Bacteriological or biochemical test	Result
Gram staining	− (bacilli)
Oxidase test	+
Hemolysis on sheep blood agar	+
Production of H2S	+
Growth at or on:
4°C	−
42°C	+
Agar with 6.5% NaCl	+
SSa agar	+
Acid productionb from:
Arabinose	−
Maltose	−
Sucrose	−
Ribose	−

^aSS, salmonella-shigella agar. 

^bFinal results were determined 72 h after inoculation of bacteria. 

Several investigators have reported the results of antibacterial susceptibility tests of S. putrefaciens (including S. alga), in which gentamicin, piperacillin, and cefotaxime were recommended as effective agents (1, 8). Recently, Vogel et al. (13) have reported differences between S. alga and S. putrefaciens with respect to their susceptibilities to certain antimicrobial agents, including penicillin, ampicillin, and tetracycline (13). Although the present report includes only one strain of S. alga, our data suggest the therapeutic potential of levofloxacin, cefpirome, and minocycline, since an excellent clinical response was observed in our patient after administration of these agents.

Shewanella spp. are widely distributed in nature, and their natural habitats are water and soil (10). Shewanella putrefaciens is an uncommon cause of human disease, and isolates from clinical specimens usually indicate colonization. On the other hand, several reports have demonstrated the association of this organism with otitis media, infected ulcers of the lower limbs, and systemic infections in patients with severe debility, liver disease, or malignancy (1, 2, 4, 6, 8).

Although S. putrefaciens is the predominant human pathogen within the genus, several investigators have reported the genetic heterogeneity of this organism. Gilardi (5) recognized three distinct biovars within S. putrefaciens, while Weyant et al. recognized two biotypes based upon biochemical and phenotypic characteristics (14). In 1990, Simidu et al. (12) proposed the name S. alga for a tetrodotoxin-producing isolate recovered from red algae. Later, this strain was shown to be genetically related to S. putrefaciens, and it was subsequently determined that some strains previously reported to be S. putrefaciens were S. alga (11). In 1996, the first two Danish patients with S. alga bacteremia and lower leg ulcers were reported (3).

Since S. putrefaciens was first isolated from humans by King in 1964 (9), the number of case reports describing this organism as a human pathogen has increased in recent years. However, most human isolates of S. putrefaciens occur as part of a mixed bacterial flora, which may overshadow the clinical significance of infections caused by this organism. With our patient, E. coli was isolated concurrently with S. alga, and both organisms were considered pathogenic because of the serial isolation of these organisms from the blood. Recently, Khashe and Janda (7) demonstrated that S. alga was more virulent than S. putrefaciens in an experimental study using mice and suggested that S. alga may be the predominant human pathogen among Shewanella species.

Further studies, including determination of bacterial virulence factors, risk factors of the host, and response to antibacterial therapy, are necessary to define the pathogenic role of this organism in humans.