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REVIEW 10.1111/j.1469-0691.2005.01108.x

Shewanella algae and Shewanella putrefaciens: clinical and microbiological characteristics H. M. Holt1, B. Gahrn-Hansen1 and B. Bruun2

1Department of Clinical Microbiology, Odense University Hospital, Odense and 2Department of Clinical Microbiology, Hillerød Hospital, Hillerød, Denmark

ABSTRACT The occurrence of the two Shewanella species found in clinical specimens, Shewanella algae and Shewanella putrefaciens, correlates with the temperature and salinity of seawater. This means that Shewanella infections occur in warm climates or during especially warm summers in temperate climates. The infections described most commonly involve ears, skin and soft tissue, with or without bacteraemia. Primary bacteraemia with a fulminant course is also seen in immunocompromised patients. Important differential characteristics between the two species include the ability of S. algae to produce mucoid colonies with b-haemolysis on sheep blood agar, to grow at 42C and in NaCl 6% w ⁄ v, and to reduce nitrite, and an inability to produce acid from maltose, all of which are in contrast to the characteristics of S. putrefaciens. Automated identification systems fail to differentiate between S. algae and S. putrefaciens, as S. algae is not included in the databases of these systems. Presumably for this reason, most Shewanella infections reported during recent years have been attributed to S. putrefaciens. However, when extensive phenotypic characterisation is performed, most human infections are seen to be caused by S. algae.As the two species seem to have different pathogenic potential for humans, correct identification is important, and this is possible in routine clinical microbiology laboratories. Keywords Antibiotic susceptibility, identification, infections, review, Shewanella spp., taxonomy Accepted: 2 January 2005 Clin Microbiol Infect 2005; 11: 347–352

Since the publication of Nozue et al. [34], it has INTRODUCTION become increasingly clear that most reports of Human infections with members of the genus human infections attributed to Shewanella putre- Shewanella are rare, being reported mainly from faciens have been caused by the species now geographical areas with warm climates, e.g., the named Shewanella algae [34–36]. Despite this, most USA [1–8], Australia [9–13], Asia [14–22], South infections caused by Shewanella spp. that have Africa [23,24] and southern Europe [25–30]. How- been reported in the literature have been attrib- ever, in recent years, cases from countries with uted to S. putrefaciens [9,11,12,14,15,17,30]. This temperate climates have also been reported [31– review describes the characteristics of S. algae and 33]. Although the clinical significance of these S. putrefaciens, and the bacteriological and clinical organisms has often been obscured by their differences between these two species. occurrence as part of a mixed bacterial flora, a number of monomicrobial infections have been HISTORY AND TAXONOMY reported, thereby documenting the pathogenic potential of Shewanella spp. [1,6,12,14,15,24,25, Shewanella spp. are Gram-negative, motile bacilli, 28–31]. whose most important phenotypic characteristic is the production of hydrogen sulphide. The first description of the species was provided in 1931 by Corresponding author and reprint requests: H. M. Holt, Derby and Hammer [37], who isolated a hitherto Department of Clinical Microbiology, Odense University Hospital, Winsløvparken 21.2, DK 5000 Odense C, Denmark unknown bacterial taxon from putrefied butter E-mail: [email protected] and water supplies of dairies, and named it

2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases 348 Clinical Microbiology and Infection, Volume 11 Number 5, May 2005

Achromobacter putrefaciens. In 1941, Long and EPIDEMIOLOGY AND Hammer [38] proposed that this species should PATHOGENICITY be transferred to the genus Pseudomonas under the name Pseudomonas putrefaciens. During the next Shewanella spp. are found throughout the world, three decades, these organisms were placed in mainly in marine environments. They are import- Pseudomonas group IV, according to Shewan et al. ant in the turnover of organic material, and are [39], and they became known as some of the most capable of dissimilatory reduction of various important spoilage bacteria of fish [40–43]. metals and other substances, such as nitrate, In the 1974 edition of Bergey’s Manual of nitrite, thiosulphate and trimethylamine-N-oxide. Systematic Bacteriology, P. putrefaciens was classi- In Denmark, S. putrefaciens and S. algae can be fied as ‘species incertae sedis’, mainly because the isolated from seawater with a salinity of 15–20% G + C content of 43–55% was below the range for [32], with the frequency of occurrence being Pseudomonas spp. (58–70%). However, several correlated with the temperature of the seawater studies agreed that isolates of P. putrefaciens could [55]. These organisms are detected in Denmark be separated into at least two different taxa on the only during the months of July–October, when basis of differences in salt tolerance, growth the water temperature is > 13C [55]. This obser- temperatures and saccharolytic activity [44–46]. vation accords with the fact that most Shewanella In 1978, Owen et al. [47] divided isolates into four infections occur in countries with a warm climate, DNA homology groups, I–IV, a division that or during especially warm summers in countries supported the results of other investigators with temperate climates. [34,36,48]. In 1985, phylogenetic studies resulted The only Shewanella spp. found in clinical in a reclassification of these organisms to the specimens are S. putrefaciens and S. algae, and it family Vibrionaceae, and the description of a new seems likely that > 80% of isolates from humans genus, Shewanella [49], named after James Shewan are S. algae [32,34–36]. Of 164 clinical isolates in honour of his work in marine microbiology. examined by Holt et al. [56], mostly from ear Included in this new genus was S. putrefaciens and swabs, only five were identified as S. putrefaciens. the related species Shewanella hanedai and Shewa- As these organisms are frequently isolated to- nella benthica. gether with other bacteria, the pathogenic poten- In the early 1990s, DNA homology group IV of tial of Shewanella has been controversial. In a Owen et al. [47] was reclassified as a new species, study of mice in which 1 mL of seawater was Shewanella alga (sic), by Simidu et al. [50], emen- inoculated into surgical wounds, 30% of the mice ded subsequently by Nozue et al. [34] on the basis developed a wound infection from which of genomic and phenotypic studies. S. alga was ‘P. putrefaciens’ isolates were cultured. Three of found to have a G + C content of 52–54 mol%, these isolates were then inoculated intraperiton- compared with 46% for the type strain of eally into rats. This procedure resulted in bacter- % S. putrefaciens, while DNA homology between aemia in three of ten rats, with an LD50 of 50 the type strains of S. alga and S. putrefaciens was [57]. It is not known whether the isolates used found to be < 10%. Other studies confirmed the were S. algae or S. putrefaciens. Saxe and Levin [58] significant genomic differences between the two found no difference in pathogenicity between species by ribotyping, 16S rRNA analysis, gyrB strains of S. putrefaciens ‘biotype I’ and ‘biotype II’ gene sequencing, and DNA–DNA hybridisation (equivalent to S. algae). However, another mouse [36,51]. In 1997, the name of this new species was pathogenicity study performed by Khashe and corrected to S. algae [52]. On the basis of small- Janda [35] indicated that S. algae was the more subunit rDNA sequencing, the genus Shewanella virulent species, and it was speculated that the was shown to be a robust monophyletic taxon haemolytic activity of S. algae could be an import- within the gamma subgroup of the phylum ant virulence factor [35]. An ability to form Proteobacteria [53]. Recent results of 16S rRNA biofilms has been described in detail for Shewa- gene sequence analyses of genera from this group nella oneidensis and S. putrefaciens [59,60]. In a led to a proposal for a new family, Shewanella- Danish study of ear infections involving S. algae, ceae [54], containing about 30 Shewanella spp., 49% of patients had ear tubes, and biofilm most of which are psychrophilic and therefore of formation could be a pathogenicity factor in such little interest to clinical microbiologists. cases [32]. S. algae is tolerant to bile salts, and

2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 347–352 Holt et al. Infections with Shewanella 349 produces extracellular virulence factors such as Table 1. Summary of biochemical characteristics of Shewa- siderophores and other exoenzymes [61]. Produc- nella algae and Shewanella putrefaciens (type strains and results taken from different studies [32,34–36,50,56,66]) tion of tetrodotoxin, the pufferfish toxin, has been reported [50], but this finding could not be S. algaeT S. putrefaciensT (IAM 14159) S. algae (ATCC 8071) S. putrefaciens reproduced by other investigators [61,62]. Intra- peritoneal inoculation in mice has given rise to Oxidase + + + + Catalase + + + + specific antibodies against S. putrefaciens [63]. Indole production – – – – Arginine dihydrolase – –– – The most obvious source for human infection is Lysine decarboxylase – –– – exposure to seawater. Such contact has been Ornithine decarboxylase + + + + H2S production + + + + reported in some of the case reports in the Urea hydrolysis – –– – literature [5,8,11,15,16,31,56] and in a Danish Gelatine hydrolysis + + + + DNA hydrolysis + + + + study of ear infections, where > 80% of patients Nitrate reduction + + + + Nitrite reduction + + – – had been swimming in the sea shortly before Acid from symptoms developed [32]. In Denmark, environ- Arabinose – – + d Ribose (+) (+) + d mental and clinical isolates of S. algae demonstrate Glucose (+) (+) + d Fructose ())(+)– d great clonal variability, as determined by ribo- Mannitol – –– – typing and random amplified polymorphic DNA Lactose – –– – Maltose – –– d profiling, but no systematic differences distin- Sucrose – –– d Growth guishing environmental and clinical isolates have 4C––++ been found [64]. Furthermore, a Danish seawater 42C++–– NaCl 6–6.5% w ⁄ v+ + – – isolate was found to be identical to one of the Haemolysis ++–– clinical isolates by all typing methods [64], sup- (sheep blood, 48 h) Mucoid colony ++–– porting the theory of a marine source of infection. consistency

Parentheses indicate delayed ⁄ weak reactions; d, variable results. PHENOTYPIC CHARACTERISATION AND IDENTIFICATION S. algae by Nozue et al. [34]. A number of reports S. algae and S. putrefaciens are non-fermentative of human infections allegedly caused by S. putre- bacilli with a single polar flagellum. They grow faciens do not supply sufficient data to show well on conventional solid media, including Mac- whether or not the isolates were actually S. algae Conkey agar, with 1–2-mm yellowish-brown col- [9,11,12,14,15,17,30]. This problem is caused by onies after incubation for 18–24 h. Table 1 the fact that the semi-automated and automated summarises the main differences between S. algae identification systems used for identification in and S. putrefaciens found by different investigators these reports (API 20E and 20NE; API ID 32 GN [32,34–36,50,56,65]. Characteristic traits include and Vitek) include S. putrefaciens, but not S. algae, production of hydrogen sulphide, decarboxylation in their databases. It also appears that these of ornithine, and hydrolysis of gelatine. S. putre- identifications as S. putrefaciens were not con- faciens is the more saccharolytic of the two species, firmed by reference laboratories. with S. algae producing acid only from ribose, and sometimes from glucose and fructose, while CLINICAL MANIFESTATIONS S. putrefaciens produces acid from maltose and glucose, and sometimes sucrose and arabinose. In The clinical syndromes reported to be caused by contrast to S. putrefaciens, S. algae shows weak S. algae and S. putrefaciens (hereafter called Shewa- b-haemolysis on sheep blood agar after incubation nella infections unless the species designation is for 48 h, as well as growth at 42C and in NaCl 6% clearly justified) are generally the same as those w ⁄ v. Holt et al. [32,56] also found that S. algae was caused by various species of the other marine distinguished from S. putrefaciens by a mucoid halophilic genus Vibrio [11,66,67]. colony consistency and an ability to reduce nitrite. In Denmark, the most common Shewanella Automated identification systems are unable to infection is infection of the ear with S. algae. This distinguish between S. putrefaciens and S. algae. can take the form of acute infection or acute A large number of clinical isolates identified exacerbation in chronic otitis media in predis- tentatively as S. putrefaciens were shown to be posed individuals. In a study of 67 ear infections

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[32], all Shewanella infections were caused by erythromycin and quinolones, but resistant to S. algae, with this organism being isolated in pure penicillin [6,16,32,36,45,56]. Susceptibility to culture in 50% of cases. Outside Denmark, only a ampicillin and cephalosporins is variable, with few such ear infections have been reported, and more isolates being susceptible to third- and these date from the 1970s [2–4,22,44]. fourth- than to first- and second-generation The most common clinical syndrome described cephalosporins [6,32,45,56]. All Danish S. algae in the literature is infection of skin and soft tissue, isolates were susceptible to piperacillin, amino- associated with breaches in the skin such as ulcers glycosides, ciprofloxacin, erythromycin and tet- or following trauma [10,11,15,16,24,30,31,68,69]. racycline, while susceptibility to ampicillin and Bacteraemia is often present, but the course is cephalosporins varied [56]. All isolates of S. algae usually benign. In approximately 40 published were resistant to colistin, while six clinical iso- reports, c.40% of cases have involved pure lates of S. putrefaciens were all susceptible. Thus cultures of Shewanella. Two cases of S. alga (sic) polymyxin susceptibility can be used to differen- bacteraemia, one with myonecrosis, involving tiate between the two species. The six cases patients with chronic ulcers have been reported involving S. putrefaciens were regarded as coloni- in Denmark [31]. Primary bacteraemia, associated sations and were consequently not treated with with severe hepatobiliary disease and malignancy specific antibiotics. In contrast, many cases with with an often fulminant course, has also been S. algae were treated with local or systemic described [6,16,24]. A distinction between these antibacterial agents [32,56]. According to the two syndromes is not always possible, as cases literature, most Shewanella infections are treated involving both cellulitis and underlying debilita- easily by a combination of surgical therapy ⁄ drain- ting diseases have been described. age and antibiotics [14,15,29,31,32,56,69]. Poor Another clinical syndrome, hitherto described outcome is associated most often with under- only in South Africa, is paediatric bacteraemia in lying disease [6,16,24]. Treatment options include underweight babies [24], with 19 cases occurring b-lactams (provided that the strain is susceptible), in two hospitals during 1990–1993. Of 16 neo- aminoglycosides and quinolones. nates, all suffered from respiratory distress at birth, and six subsequently died. In 12 cases, the CONCLUSIONS organism was isolated shortly after birth, thereby indicating the possibility of intrapartum infection. The increasing number of reports of Shewanella Respiratory colonisation, and possibly infec- infections in which the organism has been isola- tion, has been seen in a peritoneal dialysis patient ted in pure culture indicates the pathogenic with bacteraemia [13], in a patient after near- potential of this genus. Most human infections drowning [8], in patients with tuberculosis [70], are caused by S. algae. Automated identification and in patients with pleural empyema as a systems are unable to distinguish between complication of biliary tract infection [16]. There S. putrefaciens and S. algae. Important differences are also anecdotal reports of Shewanella bone and between the two species exist regarding genotypic joint infections [2,7,10,28], meningitis [26], cere- and phenotypic characteristics, pathogenicity and bellar abscess [14], endocarditis [17], an infected susceptibility to antimicrobial agents. A prere- aortic aneurysm [29] and eye infections [1,16]. quisite for further study in this field is correct Among the clinical isolates examined by Holt identification, which is possible in routine clinical et al. [56], only 3% were identified as S. putrefaciens. microbiological laboratories with careful conven- The organism was not detected in blood cultures, tional phenotypic characterisation. and evidence of its pathogenic role in Danish The epidemiology and clinical symptoms of clinical cases is lacking. This is in agreement with S. algae infections are similar to those of infec- the findings of other investigators [34–36]. tions involving Aeromonas and halophilic Vibrios. The most common S. algae infections involve ears and soft tissue, but serious infections such ANTIBIOTIC SUSCEPTIBILITY AND as bacteraemia, meningitis and endocarditis TREATMENT have also been described. Marine environments S. algae and S. putrefaciens are characteristically can often be implicated as the source of infec- susceptible to aminoglycosides, carbapenems, tion.

2005 Copyright by the European Society of Clinical Microbiology and Infectious Diseases, CMI, 11, 347–352 Holt et al. Infections with Shewanella 351

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