• 1.

    Vogel BF, Jorgensen K, Christensen H, Olsen JE, Gram L, 1997. Differentiation of Shewanella putrefaciens and Shewanella alga on the basis of whole-cell protein profiles, ribotyping, phenotypic characterization, and 16S rRNA gene sequence analysis. Appl Environ Microbiol 63: 21892199.

    • Search Google Scholar
    • Export Citation
  • 2.

    Khashe S, Janda JM, 1998. Biochemical and pathogenic properties of Shewanella alga and Shewanella putrefaciens. J Clin Microbiol 36: 783787.

    • Search Google Scholar
    • Export Citation
  • 3.

    Gram L, Bundvad A, Melchiorsen J, Johansen C, Fonnesbech Vogel B, 1999. Occurrence of Shewanella algae in Danish coastal water and effects of water temperature and culture conditions on its survival. Appl Environ Microbiol 65: 38963900.

    • Search Google Scholar
    • Export Citation
  • 4.

    Derby H, Hammer B, 1931. Bacteriology of butter. Part IV. Bacteriological studies on surface tainted butter. Iowa Agric Exp Stn Res Bull 145: 389416.

    • Search Google Scholar
    • Export Citation
  • 5.

    Holt HM, Gahrn-Hansen B, Bruun B, 2005. Shewanella algae and Shewanella putrefaciens: clinical and microbiological characteristics. Clin Microbiol Infect 11: 347352.

    • Search Google Scholar
    • Export Citation
  • 6.

    Kueh CS, Kutarski P, Brunton M, 1992. Contaminated marine wounds: the risk of acquiring acute bacterial infection from marine recreational beaches. J Appl Bacteriol 73: 412420.

    • Search Google Scholar
    • Export Citation
  • 7.

    Tsai MS, You HL, Tang YF, Liu JW, 2008. Shewanella soft tissue infection: case report and literature review. Int J Infect Dis 12: e119e124.

    • Search Google Scholar
    • Export Citation
  • 8.

    Oh HS, Kum KA, Kim EC, Lee HJ, Choe KW, Oh MD, 2008. Outbreak of Shewanella algae and Shewanella putrefaciens infections caused by a shared measuring cup in a general surgery unit in Korea. Infect Control Hosp Epidemiol 29: 742748.

    • Search Google Scholar
    • Export Citation
  • 9.

    von Graevenitz A, Simon G, 1970. Potentially pathogenic, nonfermentative, H2S-producing gram-negative rod (1 b). Appl Microbiol 19: 176.

    • Search Google Scholar
    • Export Citation
  • 10.

    Gilardi GL, 1972. Infrequently encountered Pseudomonas species causing infection in humans. Ann Intern Med 77: 211215.

  • 11.

    Riley PS, Tatum HW, Weaver RE, 1972. Pseudomonas putrefaciens isolates from clinical specimens. Appl Microbiol 24: 798800.

  • 12.

    Holmes B, Lapage SP, Malnick H, 1975. Strains of Pseudomonas putrefaciens from clinical material. J Clin Pathol 28: 149155.

  • 13.

    Rosenthal SL, Zuger JH, Apollo E, 1975. Respiratory colonization with Pseudomonas putrefaciens after near-drowning in salt water. Am J Clin Pathol 64: 382384.

    • Search Google Scholar
    • Export Citation
  • 14.

    Debois J, Degreef H, Vandepitte J, Spaepen J, 1975. Pseudomonas putrefaciens as a cause of infection in humans. J Clin Pathol 28: 993996.

    • Search Google Scholar
    • Export Citation
  • 15.

    Thong ML, 1976. Pseudomonas putrefaciens from clinical material. Southeast Asian J Trop Med Public Health 7: 363366.

  • 16.

    Appelbaum PC, Bowen AJ, 1978. Opportunistic infection of chronic skin ulcers with Pseudomonas putrefaciens. Br J Dermatol 98: 229231.

    • Search Google Scholar
    • Export Citation
  • 17.

    Vandepitte J, Debois J, 1978. Pseudomonas putrefaciens as a cause of bacteremia in humans. J Clin Microbiol 7: 7072.

  • 18.

    Schmidt U, Kapila R, Kaminski Z, Louria D, 1979. Pseudomonas putrefaciens as a cause of septicemia in humans. J Clin Microbiol 10: 385387.

    • Search Google Scholar
    • Export Citation
  • 19.

    Eschete ML, Williams F, West BC, 1980. Pseudomonas putrefaciens and group A beta-hemolytic Streptococcus septicemia. Arch Intern Med 140: 15331534.

    • Search Google Scholar
    • Export Citation
  • 20.

    Pope TL, Teague WG, Kossack R, Bray ST, Flannery DB, 1982. Pseudomonas sacroiliac osteomyelitis: diagnosis by gallium citrate Ga 67 scan. Am J Dis Child 136: 649650.

    • Search Google Scholar
    • Export Citation
  • 21.

    Laudat P, Audurier A, Loulergue F, Legros B, Lapierre F, 1983. Pseudomonas putrefaciens meningitis. J Infect 7: 281283.

  • 22.

    Marne C, Pallares R, Sitges-Serra A, 1983. Isolation of Pseudomonas putrefaciens in intra-abdominal sepsis. J Clin Microbiol 17: 11731174.

    • Search Google Scholar
    • Export Citation
  • 23.

    Kim JH, Cooper RA, Welty-Wolf KE, Harrell LJ, Zwadyk P, Klotman ME, 1989. Pseudomonas putrefaciens bacteremia. Rev Infect Dis 11: 97104.

    • Search Google Scholar
    • Export Citation
  • 24.

    Heller HM, Tortora G, Burger H, 1990. Pseudomonas putrefaciens bacteremia associated with shellfish contact. Am J Med 88: 8586.

  • 25.

    Chen SC, Lawrence RH, Packham DR, Sorrell TC, 1991. Cellulitis due to Pseudomonas putrefaciens: possible production of exotoxins. Rev Infect Dis 13: 642643.

    • Search Google Scholar
    • Export Citation
  • 26.

    Roger SD, Chen SC, Lawrence S, Sorrell TC, 1991. Pseudomonas putrefaciens bacteraemia in a peritoneal dialysis patient. Nephrol Dial Transplant 6: 73.

    • Search Google Scholar
    • Export Citation
  • 27.

    Dan M, Gutman R, Biro A, 1992. Peritonitis caused by Pseudomonas putrefaciens in patients undergoing continuous ambulatory peritoneal dialysis. Clin Infect Dis 14: 359360.

    • Search Google Scholar
    • Export Citation
  • 28.

    Brink AJ, van Straten A, van Rensburg AJ, 1995. Shewanella (Pseudomonas) putrefaciens bacteremia. Clin Infect Dis 20: 13271332.

  • 29.

    Dominguez H, Vogel BF, Gram L, Hoffmann S, Schaebel S, 1996. Shewanella alga bacteremia in two patients with lower leg ulcers. Clin Infect Dis 22: 10361039.

    • Search Google Scholar
    • Export Citation
  • 30.

    Butt AA, Figueroa J, Martin DH, 1997. Ocular infection caused by three unusual marine organisms. Clin Infect Dis 24: 740.

  • 31.

    Chen YS, Liu YC, Yen MY, Wang JH, Wang JH, Wann SR, Cheng DL, 1997. Skin and soft-tissue manifestations of Shewanella putrefaciens infection. Clin Infect Dis 25: 225229.

    • Search Google Scholar
    • Export Citation
  • 32.

    Holt HM, Sogaard P, Gahrn-Hansen B, 1997. Ear infections with Shewanella alga: a bacteriologic, clinical and epidemiologic study of 67 cases. Clin Microbiol Infect 3: 329334.

    • Search Google Scholar
    • Export Citation
  • 33.

    Yohe S, Fishbain JT, Andrews M, 1997. Shewanella putrefaciens abscess of the lower extremity. J Clin Microbiol 35: 3363.

  • 34.

    Dhawan B, Chaudhry R, Mishra BM, Agarwal R, 1998. Isolation of Shewanella putrefaciens from a rheumatic heart disease patient with infective endocarditis. J Clin Microbiol 36: 2394.

    • Search Google Scholar
    • Export Citation
  • 35.

    Levy PY, Tessier JL, 1998. Arthritis due to Shewanella putrefaciens. Clin Infect Dis 26: 536.

  • 36.

    Papanaoum K, Marshmann G, Gordon LA, Lumb R, Gordon DL, 1998. Concurrent infection due to Shewanella putrefaciens and Mycobacterium marinum acquired at the beach. Australas J Dermatol 39: 9295.

    • Search Google Scholar
    • Export Citation
  • 37.

    Bhandari S, Pan TL, Horvath J, Tiller D, 2000. CAPD, swimming in Shewanella. Nephrol Dial Transplant 15: 14841485.

  • 38.

    Leong J, Mirkazemi M, Kimble F, 2000. Shewanella putrefaciens hand infection. Aust N Z J Surg 70: 816817.

  • 39.

    Liao WY, Liaw YS, Wang HC, Chen KY, Luh KT, Yang PC, 2000. Bacteriology of infected cavitating lung tumor. Am J Respir Crit Care Med 161: 17501753.

    • Search Google Scholar
    • Export Citation
  • 40.

    Paccalin M, Grollier G, le Moal G, Rayeh F, Camiade C, 2001. Rupture of a primary aortic aneurysm infected with Shewanella alga. Scand J Infect Dis 33: 774775.

    • Search Google Scholar
    • Export Citation
  • 41.

    Krsnik I, Arribalzaga K, Romanyk J, 2002. Shewanella alga bacteremia and associated cellulitis in a patient with multiple myeloma. Haematologia (Budap) 32: 7980.

    • Search Google Scholar
    • Export Citation
  • 42.

    Pagani L, Lang A, Vedovelli C, Moling O, Rimenti G, Pristera R, Mian P, 2003. Soft tissue infection and bacteremia caused by Shewanella putrefaciens. J Clin Microbiol 41: 22402241.

    • Search Google Scholar
    • Export Citation
  • 43.

    Bulut C, Ertem GT, Gokcek C, Tulek N, Bayar MA, Karakoc E, 2004. A rare cause of wound infection: Shewanella putrefaciens. Scand J Infect Dis 36: 692694.

    • Search Google Scholar
    • Export Citation
  • 44.

    Clement LF, Gallet C, Perron J, Lesueur A, 2004. Infectious cellulitis and Shewanella alga septicemia in an immunocompetent patient [in French]. Ann Dermatol Venereol 131: 10951097.

    • Search Google Scholar
    • Export Citation
  • 45.

    Jorens PG, Goovaerts K, Ieven M, 2004. Shewanella putrefaciens isolated in a case of ventilator-associated pneumonia. Respiration 71: 199201.

    • Search Google Scholar
    • Export Citation
  • 46.

    Suzuk S, Yetener V, Ergungor F, Balaban N, 2004. Cerebellar abscess caused by Shewanella putrefaciens. Scand J Infect Dis 36: 621622.

  • 47.

    Botelho-Nevers E, Gouriet F, Rovery C, Paris P, Roux V, Raoult D, Brouqui P, 2005. First case of osteomyelitis due to Shewanella algae. J Clin Microbiol 43: 53885390.

    • Search Google Scholar
    • Export Citation
  • 48.

    Tsai TH, You HY, 2006. Necrotizing fasciitis caused by Shewanella putrefaciens in a uremic patient. J Microbiol Immunol Infect 39: 516518.

    • Search Google Scholar
    • Export Citation
  • 49.

    Park HJ, Tuli SS, Downer DM, Gohari AR, Shah M, 2007. Shewanella putrefaciens keratitis in the lamellar bed 6 years after LASIK. J Refract Surg 23: 830832.

    • Search Google Scholar
    • Export Citation
  • 50.

    Grocholski AS, Delage M, Samimi M, Maruani A, 2009. Acute dermohypodermitis of the right leg (S. putrefaciens) after sea bathing [in French]. Ann Dermatol Venereol 136: 5960.

    • Search Google Scholar
    • Export Citation
  • 51.

    Bhalerao DS, Kinikar AG, Roushani SB, Franklin VX, 2010. Shewanelia putrefaciens: a rare microbial agent associated with a non-healing ulcer in a leprosy patient. Indian J Lepr 82: 205207.

    • Search Google Scholar
    • Export Citation
  • 52.

    Gressier M, Mbayo D, Deramond H, Grados F, Eb F, Canarelli B, 2010. First case of human spondylodiscitis due to Shewanella algae. Int J Infect Dis 14 (Suppl 3): e261e264.

    • Search Google Scholar
    • Export Citation
  • 53.

    Sharma KK, Kalawat U, 2010. Emerging infections: Shewanella - a series of five cases. J Lab Physicians 2: 6165.

  • 54.

    Tucker C, Baroso G, Tan P, 2010. Ventilator-associated pneumonia due to Shewanella putrefaciens. Am J Health Syst Pharm 67: 10071009.

    • Search Google Scholar
    • Export Citation
  • 55.

    Goyal R, Kaur N, Thakur R, 2011. Human soft tissue infection by the emerging pathogen Shewanella algae. J Infect Dev Ctries 5: 310312.

    • Search Google Scholar
    • Export Citation
  • 56.

    Finkelstein R, Oren I, 2011. Soft tissue infections caused by marine bacterial pathogens: epidemiology, diagnosis, and management. Curr Infect Dis Rep 13: 470477.

    • Search Google Scholar
    • Export Citation
  • 57.

    Heritier C, Poirel L, Nordmann P, 2004. Genetic and biochemical characterization of a chromosome-encoded carbapenem-hydrolyzing ambler class D beta-lactamase from Shewanella algae. Antimicrob Agents Chemother 48: 16701675.

    • Search Google Scholar
    • Export Citation
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Human Infection with Shewanella putrefaciens and S. algae: Report of 16 Cases in Martinique and Review of the Literature

Nicolas VignierDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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Morgane BarreauDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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Claude OliveDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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Emilie BaubionDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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Rafaelle ThéodoseDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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Patrick HochedezDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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André CabiéDepartment of Tropical and Infectious Diseases, Bacteriology Laboratory, INSERM CIE802, and Department of Dermatology, University Hospital of Fort-de-France, Fort-de-France, Martinique

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Shewanella spp. are saprophytic bacteria that are part of the marine microflora in warm climates and are rarely pathogenic. However, Shewanella spp. infections are being increasingly reported, and there has been no comprehensive review of the literature describing these infections. This article reports 16 cases of Shewanella spp. infections in Martinique since 1997 and reviews another 239 cases reported in the literature since 1973. Patients experienced soft tissue infections, ear infection, or abdominal and biliary tract infections. A skin or mucosal portal of entry was found for 53% of the patients and exposure to the marine environment was reported for 44%; 79% of patients had an underlying condition. Bacteriema were frequent (28%). Most (87%) patients recovered, although ear infections can become chronic. Death occurred in 13% of the patients. Most Shewanella spp. isolates are susceptible to cefotaxime (95%), piperacillin and tazobactam (98%), gentamicin (99%), and ciprofloxacin (94%).

Introduction

Shewanella spp. are Gram-negative bacteria widely distributed worldwide; they are saprophytes and rarely pathogenic.1 Their natural habitats are all forms of water and soil, but they have also been isolated from diverse sources including dairy products, oil, and carcasses.2 They belong to the microflora of the marine environment (with Vibrio paraheamolyticus, Aeromonas hydrophila, Plesiomonas, and various enteric bacteria). In Denmark, Shewanella spp. have been isolated from sea water at temperatures > 13°C.3

The bacterium was first isolated in 1931 from putrefied butter and was successively called Achromobacter putrefaciens, Pseudomonas putrefaciens, Alteromonas putrefaciens, and finally Shewanella spp., of which 30 species have now been identifed.4 The only species that have been isolated from clinical specimens are S. putrefaciens and S. algae. Important differential characteristics between the two species include the ability of S. algae to produce mucoid colonies with beta-hemolysis on sheep blood agar, grow at 42°C and in 6% NaCl (w/v), reduce nitrite, and an inability to produce acid from maltose, all of which are in contrast to the characteristics of S. putrefaciens.5

The pathogenicity of these species remains unclear, partly because they are found in polymicrobial infections, but there is now enough evidence to conclude that some Shewanella spp. are pathogenic for humans.6 Most cases have been reported from areas with warm climates. Shewanella infections are sometimes acquired after exposure to seawater. The most common clinical manifestations seem to be otitis, soft tissue infection,7 bacteremia, and hepatobiliary infection. Some argue than S. algae could be more virulent species.2 Shewanella spp. have in rare cases been found associated with medical devices and can lead to health–care-associated infections and outbreaks.8

Infections with Shewanella spp. are rare, and there have been no systematic studies. Therefore, we report a review of Shewanella spp. infections reported to our Caribbean reference center and of other cases and series reported in the literature.

Patients and Methods

We reviewed all cases over a 14-year period, for which cultures were positive for Shewanella spp. in the Bacteriology laboratory of the University Hospital of Fort-de-France in Martinique. Patient files for 1997–2010 were reviewed retrospectively and those for 2011–2012 were included prospectively. Medical records were analyzed by physicians specialized in infectious disease from our university hospital. Shewanella spp. were cultured on Uriselect® medium (Biorad Laboratories, Hercules, CA) and identified by using the API® 20NE standardized system (Biomérieux, Marcy l'Etoile, France).

We searched for articles reporting cases of Shewanella spp infections in the PubMed database by using the following terms: Achromobacter putrefaciens, Pseudomonas putrefaciens, Alteromonas putrefaciens, Shewanella, Shewanella putrefaciens, Shewanella alga, and Shewanella algae. We included series and case reports. No prevalence or incidence studies were found. Standardized environmental, clinical, and bacteriologic data were collected and entered into a database. Data for patients from Martinique were added to the global case report database. Thus, global analysis includes all cases from Martinique, case reports, and series. Not all relevant data were available for each case, and consequently the number of observations is systematically specified in the results section. Stata version 10 (StataCorp LP, College Station, TX) was used for statistical analyses.

Results

Martinique.

In Martinique, we found 21 Shewanella spp.-positive clinical specimens isolated from 21 patients (7 women, 13 men, and 1 newborn). Their mean age was 61 years. The specimens were blood (3 specimens), pus (12), joint fluid (1), leg surgical site (1), bronchial aspiration (2), and gastric liquid (1). Five isolates were likely not pathogenic after review of patient file (specimens from skin, ulcer, or lung without clinical arguments for infection; one grows from joint fluid in only one specimen and other specimens remained negative). Sixteen of the 21 isolates were considered to be pathogens.

The clinical characteristics of these cases are summarized in Table 1. Half (8 of 16) of the infections were polymicrobial, and most often involved marine or gastrointestinal flora. Soft tissue infection was the most frequent clinical presentation (11 of 16) and in some cases was complicated with abscess (3), osteoarthritis (1), or bacteremia (3). Other infections included superinfection of an open fracture (3 of 16), peritonitis (1 of 16), pneumonia (1 of 16), and neonatal infection (1 of 16). Four patients died. Three died secondarily from the infection (skin and soft tissue infection with bacteremia in two patients and osteitis with renal failure in one patient). Among the 11 patients with skin and soft tissue infections, nine had underlying conditions. A portal of entry was found in most (9 of 11) patients: chronic venous ulcers (4), post-traumatic ulcers (2), or wounds (3). We found history of sea water exposure for three patients. All isolates were susceptible to ceftazidime, piperacillin, and ciprofloxacin. None were susceptible to fosfomycin, 4 of 8 to amoxicillin, 13 of 15 to cefotaxime, 15 of 15 to cotrimoxazole, and 15 of 15 to gentamicin.

Table 1

Clinical characteristics of 16 patients with Shewanella spp. infection isolated in Martinique, 1997–2012

Year Age, years Sex Underlying condition Portal of entry Type of infection Bacteremia Outcome Co-isolates
1998 84 M Prostatic cancer, venous insufficiency Leg ulcer Cellulitis No Citrobacter freundii and Aeromonas sobria
1998 27 M No Open fracture Superinfection of open fracture with arthritis No Monomicrobial
1999 35 M No Open fracture Superinfection of finger open fracture with necrosis No Death Aeromonas hydrohila, Enterobacter Cloacae, and Streptococcus D
1999 73 M Diabetes, heart failure Blister Cellulitis and abscess No Aeromonas sobria, Staphylococcus aureus, and Group B Streptococcus
2000 78 M No Open fracture Superinfection of finger open fracture No Aeromonas hydrophila, Enterobacter cloacae, and Enterococcus faecalis
2002 78 M Arteritis Blister Superinfection of blister No Escherichia coli
2005 66 F Diabetes, amputated foot, renal failure Amputation Osteitis and erysipelas No Death Gram-negative and -positive rods
2006 76 M Diabetes, obesity, heart and renal failure Leg ulcer Superinfection of ulcer No Staphylococcus aureus
2007 83 F Hypertension Leg ulcer Cellulitis Yes Death Monomicrobial
2008 85 M Arthritis, heart failure, chronic bronchitis Leg ulcer Cellulitis and leg abscess No Monomicrobial
2008 < 1 F Newborn Birth Neonatal respiratory distress No Monomicrobial
2009 89 F Cecal tumor, heart failure, diverticulosis Digestive Stercoral peritonitis No Death unrelated Monomicrobial
2010 39 M Osteosynthesis Wound Late abscess on osteosynthesis No Staphylococcus lugdenensis
2011 76 F Heart failure Leg ulcer Cellulitis Yes Monomicrobial
2011 79 M No Wound Cellulitis Yes Monomicrobial
2012 63 M Chronic respiratory failure Lung Pneumonia No Monomicrobial

Review of the literature.

We identified 56 articles published on PubMed search during 1973–2011, which reported 239 cases of Shewanella spp. infection or colonization.755 Including the cases in Martinique, we analyzed a total of 260 cases. Twenty reported cases and five cases from Martinique were likely colonization (25 of 244). The mean age of the patients was 50 years (range = 0–90 years, n = 154) and 49 (39%) of 127 patients were women. Some neonatal cases were reported (one study in South Africa and one case in Martinique)28 but the elderly were overrepresented (Table 2). The origins of the cases are shown in Table 2. Series have been reported in some countries, and these countries were thus overrepresented: Denmark (76),32 South Korea (33),8 South Africa (28),28 United States (26),13,23,31 Taiwan (19),31 Belgium (9),14 and India (5).53

Table 2

Characteristics of patients with Shewanella spp. infection (case report database)

Variable No. positive/no. tested (%)
Age
 Premature 9/154 (6)
 Neonate 8/154 (5)
 Child 9/154 (6)
 Adult 85/154 (55)
 Senior (> 65 years of age) 43/154 (28)
Residence
 Europe (Belgium, Denmark, France, Italy, Spain, Great Britain) 98/242 (40)
 Australia 4/242 (2)
 Caribbean (Martinique) 20/242 (8)
 Pacific area (Hawaii) 1/242 (< 1)
 Asia (Turkey, Japan, Korea, Taiwan, India) 64/242 (26)
 Africa (South Africa) 28/242 (12)
 North America (United States, Mexico) 27/254 (11)

Eleven percent of patients were immunocompromised (Table 3) because of cancer with chemotherapy (15), steroid use (4), splenectomy (2), neutropenia (2), human immunodeficiency virus HIV infection (1), and immunosuppressive drugs (1). Two-thirds had other underlying conditions: chronic ear disease (55), biliary tract lithiasis (8), cirrhosis (6), or other hepatobilary disease (21), heart failure (15), venous incompetence (9), renal failure (7), hypertension (7), arterial insufficiency (6), diabetes (6), gut surgery (6), peritoneal dialysis (6), chronic obstructive pulmonary disease (3), and obesity (3).

Table 3

Condition and portal of entry of patients with Shewanella spp. infection (case report database)

Variable No. positive/no. tested (%)
Condition
 None 45/216 (21)
 Immunocompromised 24/216 (11)
Underlying condition 147/216 (68)
Portal of entry
 None 116/249 (47)
 Skin or mucosal injury 133/249 (53)
Water exposure
 None 65/168 (42)
 Salt water 67/168 (44)
 Fresh water 36/168 (24)

A skin or mucosal portal of entry was found for 53% of the cases (Table 3). The portals of entry were chronic leg ulcers (31), burns (4), wounds (32), rupture of the tympanic membrane (52), near drowning (1), mechanical ventilation (1), and loco-regional tumor (1). Exposure to the marine environment was reported for 44% of the cases, for which relevant information was available (Table 3).

The clinical spectrum of the disease is shown in Table 4. Ear infections were the most commonly reported infections, particularly in the series in Denmark. There were 53 cases of otitis media, 1 case of with cerebral abscess, 15 cases of chronic otitis, and eight cases of otitis externa. Skin and soft tissue infections were common (27%), comprising 19 cases of cellulitis, 6 cases of abscesses, 1 case of empyema, 3 cases of necrotizing fasciitis, 1 case of tonsillitis, 1 case of extensive myonecrosis, 3 cases of infections or colonizations of an open fracture, 5 cases of colonizations or chronic infections of a non-healing ulcer, and 3 cases of non-healing wounds. Abdominal and biliary tract infections were also reported: 10 biliary tract infections, 2 with cholecystitis, five with peritonitis, 1 with abdominal wall abscess, and 1 with paracolic abscess. For these case-patients, the portal of entry was digestive. The last common type of infection was respiratory infection: 10 cases of pneumonia, 2 cases of acute exacerbations of COPD, 1 case of bronchitis, 2 cases of ventilator-associated pneumonia, 17 cases of neonatal respiratory distress, 1 case of pulmonary abscess, and 1 case of acute exacerbation of bronchiectasis. Other sporadic clinical presentations are shown in Table 4.

Table 4

Clinical characteristics of patients with Shewanella spp. infection (case report database)

Type of infection* No. positive (%)
Skin and soft tissue 70 (27)
Bacteremia 71 (28)
Abdominal or biliary tract 43 (17)
Respiratory 34 (13)
Ear 84 (33)
Other 17 (7)
 Bone 2 (1)
 Urinary tract 4/256 (2)
 Eye infection 3/256(1)
 Endocarditis 1/256 (< 1)
 Meningitis 1/256 (< 1)
 Aneurysm infection 1/256 (< 1)
 Cerebral abscess 2/256 (1)

Some patients had more than one infection.

Bacteremia was the most common complication (71 of 256, 28%). It was associated with skin and soft tissue infection (23 of 71, 33%), abdominal or biliary tract infection (13 of 71, 19%), or respiratory infection (21 of 71, 30%). Bacteremia was not associated with ear infection in any case.

The infection was considered serious (hypotension, secondarily organ failure, or death) in 21% (50 of 242) of cases. Fifty (19%) of 259 cases were described as possible healthcare-associated infections. An outbreak of 31 abdominal and biliary tract infections, or bacteremia, caused by exposure to a shared measuring cup was reported in a general surgery unit in South Korea.8 Other infections in this group were two cases of ventilator-associated pneumonia,45,54 five cases of peritonitis in patients undergoing peritoneal dialysis,26,27,31 eight cases of skin and soft tissue infections,24,31 one case of keratitis,49 one case of bacteremia caused by endoscopic therapy of gastric varices,31 one case of meningitis after trepanation,21 and one case of urinary tract infection associated with catheterization.14

Most (87%, 195 of 223) patients recovered, although some cases of ear infection became chronic. Death occurred in 26 (13%) of 208 case-patients. Death was related to the infection in 18 (86%) of 21 cases for which information was available.

Bacteria isolated were Pseudomonas putrefaciens (19%, 49 of 253), Shewanella putrefaciens (37%, 93 of 253), and Shewanella algae (44%, 112 of 253). However, 16S rRNA analysis was not performed systematically to confirm the identification.

Bacteria was isolated from pus (49%, 112 of 230), blood (30%, 69), bile (7%, 16), or other specimens (17%: ascitic fluid [7], peritoneal dialysate [5], bronchoalveolar lavage fluid [2], sputum [7], urine: > 104 bacteria/mL [4]), corneal stroma and vitreous fluid [2], feces [2], bone [1], disc biopsy specimen [1], cerebral abscess [1], pulmonary abscess [1], pleural effusion [1], neonatal gastric liquid and anus [1], bronchic aspiration [2], articular fluid [1], and tonsilar pus [1]). The culture was polymicrobial in 99 (53%) of 188 cases. Co-isolates were gram-negative rods in 64% and gram-positive cocci in 30%. Associated bacteria from marine flora were reported in some cases (Aeromonas hydrophila and A. sobria [8], Vibrio alginolyticus [3], Vibrio vulnificans [1], and Mycobacterium marinum [1]). Antibiotic susceptibility of Shewanella spp. isolates is shown in Table 5.

Table 5

Antibiotic susceptibility of clinical Shewanella spp. isolates (case report database)

Antibiotic No. positive/no. tested (%)
Penicillin G 0/8 (0)
Amoxicillin 25/114 (22)
Amoxicillin/clavulanic acid 9/12 (75)
Cefazolin 5/15 (33)
Cefotaxime 128/135 (95)
Ceftriaxone 51/54 (94)
Ceftazidime 69/73 (95)
Cefepime 19/20 (95)
Ticarcillin 36/47 (77)
Ticarcillin/clavulanic acid 15/18 (83)
Piperacillin 51/54 (94)
Piperacillin/tazobactam 54/55 (98)
Imipenem 103/125 (82)
Gentamicin 144/146 (99)
Tobramycin 18/18 (100)
Netilmicin 14/14 (100)
Amikacin 76/76 (100)
Colistin 16/30 (53)
Trimethoprim/sulfamethoxazole 62/143 (43)
Ofloxacin 14/16 (88)
Ciprofloxacin 121/129 (94)
Fosfomycin 0/19 (0)
Erythromicin 91/94 (97)
Chloramphenicol 115/116 (99)
Tetracycline 104/117 (89)
Polymyxin B 5/73 (7)

Discussion

Shewanella spp. infections have been reported worldwide. The cases include soft tissue infections, ear infections, abdominal infections, and biliary tract infections. Infections involving these species are frequently associated with underlying conditions and complications.

Although we intended to provide a comprehensive overview of the state of the knowledge of Shewanella spp. infections, our review has several limitations. In particular, many of the cases are single-case reports or small series. Thus, reporting bias is plausible. Furthermore, all relevant information that could be expected was not available from all publications.

There is substantial heterogeneity between cases reports and series, and they do not appropriately reflect the distribution of Shewanella spp. infections worldwide. Other than small series reported in Taiwan,31 South Africa,28 and Belgium,14 the healthcare-associated epidemic in South Korea,8 a larger series of otitis cases in Denmark,32 and our retrospective study in Martinique, there have been no epidemiologic studies, either retrospective or prospective. We therefore compiled case reports to generate a description of the clinical and bacteriologic spectrum of this infection. Shewanella spp. infection seems to be ubiquitous: it has been observed in temperate regions during summer but is more common in intertropical areas.

Most of the clinical isolates are Shewanella putrefaciens, but recent data suggest that many of these isolates should be classified as the genetically distinct species Shewanella algae.5 Some argue that S. algae may be a more virulent species.2 This misclassification is largely caused by the use of conventional systems that are unable to identify S. algae (API® 20 NE system, ID 32 GN, or VITEK® 2 GN; Biomérieux). Accurate bacteriologic identification requires the use of molecular typing (16S rRNA sequence analysis). In our 21 cases, we performed 16S rRNA only three times for the three most recent isolates initially identified as S. putrefaciens by biochemical methods. All three isolates were identified as S. algae by molecular analysis. As has been suggested elsewhere, some of the S. putrefaciens infections reported during recent years were probably caused by S. algae.5

The clinical spectrum of human Shewanella spp. infections is wide; otitis, skin and soft-tissue infection,31 hepatobiliary infection, and peritonitis32 are the most frequent. This spectrum is similar to those of infections involving other marine bacteria (Aeromonas spp., Vibrio spp.).56 This bacterium can be involved in neonatal infections as shown by a study in South Africa (respiratory distress with bacteremia) and one case in Martinique.28 Serious infections and bacteremia are common.18,28 Chronic infection of the legs, liver disease, and neonatal infections have been identified as possible risk factors for bloodstream infection by S. putrefaciens.18,23,28 The death rate is high, although this finding may be partially explained by the high frequency of underlying conditions and bacteremia.

Shewanella putrefaciens was often isolated from cases of polymicrobial infection. Most of the strains co-isolated from such polymicrobial infections were enterobacteriaceae, but bacteria of marine flora were also found.31,36 This pattern of co-isolates is consistent with portals of entry (gastrointestinal in most cases) and environmental flora.

Our study confirms that exposure to the marine environment is a risk factor for Shewanella spp. infection. The frequency of skin disease among patients with chronic ulcers or breaks in the skin and hepatobiliary infections suggest that Shewanella spp. may also be a commensal of the skin and present in gastrointestinal flora. Chronic diseases facilitate the occurrence of infection. Patients with lower leg ulcers should be advised to avoid exposure to the marine environment.

Shewanella spp. can show resistance to penicillins initially used to treat soft tissue infection. However, treatment of Shewanella spp. infections is straightforward once the antibiogram is available. Shewanella spp. are susceptible to commonly used antimicrobial agents, particularly third-generation cephalosporins, piperacillin, ciprofloxacin, and gentamicin. Because Shewanella spp. are oxidase positive, laboratories tend to test broad-spectrum antibiotics. However, it may be of value to test narrow-spectrum antibiotics because many Shewanella spp. isolates are susceptible to amoxicillin and third-generation cephalosporins. It is important to note that Shewanella can show resistance to imipenem by secreting an oxacillinase.57

Infection with Shewanella spp. infections should be considered in a suggestive environmental context (tropical area, sea water exposure). The use of molecular typing should be encouraged when Shewanella spp. are isolated. Epidemiologic studies are required to confirm these observations.

  • 1.

    Vogel BF, Jorgensen K, Christensen H, Olsen JE, Gram L, 1997. Differentiation of Shewanella putrefaciens and Shewanella alga on the basis of whole-cell protein profiles, ribotyping, phenotypic characterization, and 16S rRNA gene sequence analysis. Appl Environ Microbiol 63: 21892199.

    • Search Google Scholar
    • Export Citation
  • 2.

    Khashe S, Janda JM, 1998. Biochemical and pathogenic properties of Shewanella alga and Shewanella putrefaciens. J Clin Microbiol 36: 783787.

    • Search Google Scholar
    • Export Citation
  • 3.

    Gram L, Bundvad A, Melchiorsen J, Johansen C, Fonnesbech Vogel B, 1999. Occurrence of Shewanella algae in Danish coastal water and effects of water temperature and culture conditions on its survival. Appl Environ Microbiol 65: 38963900.

    • Search Google Scholar
    • Export Citation
  • 4.

    Derby H, Hammer B, 1931. Bacteriology of butter. Part IV. Bacteriological studies on surface tainted butter. Iowa Agric Exp Stn Res Bull 145: 389416.

    • Search Google Scholar
    • Export Citation
  • 5.

    Holt HM, Gahrn-Hansen B, Bruun B, 2005. Shewanella algae and Shewanella putrefaciens: clinical and microbiological characteristics. Clin Microbiol Infect 11: 347352.

    • Search Google Scholar
    • Export Citation
  • 6.

    Kueh CS, Kutarski P, Brunton M, 1992. Contaminated marine wounds: the risk of acquiring acute bacterial infection from marine recreational beaches. J Appl Bacteriol 73: 412420.

    • Search Google Scholar
    • Export Citation
  • 7.

    Tsai MS, You HL, Tang YF, Liu JW, 2008. Shewanella soft tissue infection: case report and literature review. Int J Infect Dis 12: e119e124.

    • Search Google Scholar
    • Export Citation
  • 8.

    Oh HS, Kum KA, Kim EC, Lee HJ, Choe KW, Oh MD, 2008. Outbreak of Shewanella algae and Shewanella putrefaciens infections caused by a shared measuring cup in a general surgery unit in Korea. Infect Control Hosp Epidemiol 29: 742748.

    • Search Google Scholar
    • Export Citation
  • 9.

    von Graevenitz A, Simon G, 1970. Potentially pathogenic, nonfermentative, H2S-producing gram-negative rod (1 b). Appl Microbiol 19: 176.

    • Search Google Scholar
    • Export Citation
  • 10.

    Gilardi GL, 1972. Infrequently encountered Pseudomonas species causing infection in humans. Ann Intern Med 77: 211215.

  • 11.

    Riley PS, Tatum HW, Weaver RE, 1972. Pseudomonas putrefaciens isolates from clinical specimens. Appl Microbiol 24: 798800.

  • 12.

    Holmes B, Lapage SP, Malnick H, 1975. Strains of Pseudomonas putrefaciens from clinical material. J Clin Pathol 28: 149155.

  • 13.

    Rosenthal SL, Zuger JH, Apollo E, 1975. Respiratory colonization with Pseudomonas putrefaciens after near-drowning in salt water. Am J Clin Pathol 64: 382384.

    • Search Google Scholar
    • Export Citation
  • 14.

    Debois J, Degreef H, Vandepitte J, Spaepen J, 1975. Pseudomonas putrefaciens as a cause of infection in humans. J Clin Pathol 28: 993996.

    • Search Google Scholar
    • Export Citation
  • 15.

    Thong ML, 1976. Pseudomonas putrefaciens from clinical material. Southeast Asian J Trop Med Public Health 7: 363366.

  • 16.

    Appelbaum PC, Bowen AJ, 1978. Opportunistic infection of chronic skin ulcers with Pseudomonas putrefaciens. Br J Dermatol 98: 229231.

    • Search Google Scholar
    • Export Citation
  • 17.

    Vandepitte J, Debois J, 1978. Pseudomonas putrefaciens as a cause of bacteremia in humans. J Clin Microbiol 7: 7072.

  • 18.

    Schmidt U, Kapila R, Kaminski Z, Louria D, 1979. Pseudomonas putrefaciens as a cause of septicemia in humans. J Clin Microbiol 10: 385387.

    • Search Google Scholar
    • Export Citation
  • 19.

    Eschete ML, Williams F, West BC, 1980. Pseudomonas putrefaciens and group A beta-hemolytic Streptococcus septicemia. Arch Intern Med 140: 15331534.

    • Search Google Scholar
    • Export Citation
  • 20.

    Pope TL, Teague WG, Kossack R, Bray ST, Flannery DB, 1982. Pseudomonas sacroiliac osteomyelitis: diagnosis by gallium citrate Ga 67 scan. Am J Dis Child 136: 649650.

    • Search Google Scholar
    • Export Citation
  • 21.

    Laudat P, Audurier A, Loulergue F, Legros B, Lapierre F, 1983. Pseudomonas putrefaciens meningitis. J Infect 7: 281283.

  • 22.

    Marne C, Pallares R, Sitges-Serra A, 1983. Isolation of Pseudomonas putrefaciens in intra-abdominal sepsis. J Clin Microbiol 17: 11731174.

    • Search Google Scholar
    • Export Citation
  • 23.

    Kim JH, Cooper RA, Welty-Wolf KE, Harrell LJ, Zwadyk P, Klotman ME, 1989. Pseudomonas putrefaciens bacteremia. Rev Infect Dis 11: 97104.

    • Search Google Scholar
    • Export Citation
  • 24.

    Heller HM, Tortora G, Burger H, 1990. Pseudomonas putrefaciens bacteremia associated with shellfish contact. Am J Med 88: 8586.

  • 25.

    Chen SC, Lawrence RH, Packham DR, Sorrell TC, 1991. Cellulitis due to Pseudomonas putrefaciens: possible production of exotoxins. Rev Infect Dis 13: 642643.

    • Search Google Scholar
    • Export Citation
  • 26.

    Roger SD, Chen SC, Lawrence S, Sorrell TC, 1991. Pseudomonas putrefaciens bacteraemia in a peritoneal dialysis patient. Nephrol Dial Transplant 6: 73.

    • Search Google Scholar
    • Export Citation
  • 27.

    Dan M, Gutman R, Biro A, 1992. Peritonitis caused by Pseudomonas putrefaciens in patients undergoing continuous ambulatory peritoneal dialysis. Clin Infect Dis 14: 359360.

    • Search Google Scholar
    • Export Citation
  • 28.

    Brink AJ, van Straten A, van Rensburg AJ, 1995. Shewanella (Pseudomonas) putrefaciens bacteremia. Clin Infect Dis 20: 13271332.

  • 29.

    Dominguez H, Vogel BF, Gram L, Hoffmann S, Schaebel S, 1996. Shewanella alga bacteremia in two patients with lower leg ulcers. Clin Infect Dis 22: 10361039.

    • Search Google Scholar
    • Export Citation
  • 30.

    Butt AA, Figueroa J, Martin DH, 1997. Ocular infection caused by three unusual marine organisms. Clin Infect Dis 24: 740.

  • 31.

    Chen YS, Liu YC, Yen MY, Wang JH, Wang JH, Wann SR, Cheng DL, 1997. Skin and soft-tissue manifestations of Shewanella putrefaciens infection. Clin Infect Dis 25: 225229.

    • Search Google Scholar
    • Export Citation
  • 32.

    Holt HM, Sogaard P, Gahrn-Hansen B, 1997. Ear infections with Shewanella alga: a bacteriologic, clinical and epidemiologic study of 67 cases. Clin Microbiol Infect 3: 329334.

    • Search Google Scholar
    • Export Citation
  • 33.

    Yohe S, Fishbain JT, Andrews M, 1997. Shewanella putrefaciens abscess of the lower extremity. J Clin Microbiol 35: 3363.

  • 34.

    Dhawan B, Chaudhry R, Mishra BM, Agarwal R, 1998. Isolation of Shewanella putrefaciens from a rheumatic heart disease patient with infective endocarditis. J Clin Microbiol 36: 2394.

    • Search Google Scholar
    • Export Citation
  • 35.

    Levy PY, Tessier JL, 1998. Arthritis due to Shewanella putrefaciens. Clin Infect Dis 26: 536.

  • 36.

    Papanaoum K, Marshmann G, Gordon LA, Lumb R, Gordon DL, 1998. Concurrent infection due to Shewanella putrefaciens and Mycobacterium marinum acquired at the beach. Australas J Dermatol 39: 9295.

    • Search Google Scholar
    • Export Citation
  • 37.

    Bhandari S, Pan TL, Horvath J, Tiller D, 2000. CAPD, swimming in Shewanella. Nephrol Dial Transplant 15: 14841485.

  • 38.

    Leong J, Mirkazemi M, Kimble F, 2000. Shewanella putrefaciens hand infection. Aust N Z J Surg 70: 816817.

  • 39.

    Liao WY, Liaw YS, Wang HC, Chen KY, Luh KT, Yang PC, 2000. Bacteriology of infected cavitating lung tumor. Am J Respir Crit Care Med 161: 17501753.

    • Search Google Scholar
    • Export Citation
  • 40.

    Paccalin M, Grollier G, le Moal G, Rayeh F, Camiade C, 2001. Rupture of a primary aortic aneurysm infected with Shewanella alga. Scand J Infect Dis 33: 774775.

    • Search Google Scholar
    • Export Citation
  • 41.

    Krsnik I, Arribalzaga K, Romanyk J, 2002. Shewanella alga bacteremia and associated cellulitis in a patient with multiple myeloma. Haematologia (Budap) 32: 7980.

    • Search Google Scholar
    • Export Citation
  • 42.

    Pagani L, Lang A, Vedovelli C, Moling O, Rimenti G, Pristera R, Mian P, 2003. Soft tissue infection and bacteremia caused by Shewanella putrefaciens. J Clin Microbiol 41: 22402241.

    • Search Google Scholar
    • Export Citation
  • 43.

    Bulut C, Ertem GT, Gokcek C, Tulek N, Bayar MA, Karakoc E, 2004. A rare cause of wound infection: Shewanella putrefaciens. Scand J Infect Dis 36: 692694.

    • Search Google Scholar
    • Export Citation
  • 44.

    Clement LF, Gallet C, Perron J, Lesueur A, 2004. Infectious cellulitis and Shewanella alga septicemia in an immunocompetent patient [in French]. Ann Dermatol Venereol 131: 10951097.

    • Search Google Scholar
    • Export Citation
  • 45.

    Jorens PG, Goovaerts K, Ieven M, 2004. Shewanella putrefaciens isolated in a case of ventilator-associated pneumonia. Respiration 71: 199201.

    • Search Google Scholar
    • Export Citation
  • 46.

    Suzuk S, Yetener V, Ergungor F, Balaban N, 2004. Cerebellar abscess caused by Shewanella putrefaciens. Scand J Infect Dis 36: 621622.

  • 47.

    Botelho-Nevers E, Gouriet F, Rovery C, Paris P, Roux V, Raoult D, Brouqui P, 2005. First case of osteomyelitis due to Shewanella algae. J Clin Microbiol 43: 53885390.

    • Search Google Scholar
    • Export Citation
  • 48.

    Tsai TH, You HY, 2006. Necrotizing fasciitis caused by Shewanella putrefaciens in a uremic patient. J Microbiol Immunol Infect 39: 516518.

    • Search Google Scholar
    • Export Citation
  • 49.

    Park HJ, Tuli SS, Downer DM, Gohari AR, Shah M, 2007. Shewanella putrefaciens keratitis in the lamellar bed 6 years after LASIK. J Refract Surg 23: 830832.

    • Search Google Scholar
    • Export Citation
  • 50.

    Grocholski AS, Delage M, Samimi M, Maruani A, 2009. Acute dermohypodermitis of the right leg (S. putrefaciens) after sea bathing [in French]. Ann Dermatol Venereol 136: 5960.

    • Search Google Scholar
    • Export Citation
  • 51.

    Bhalerao DS, Kinikar AG, Roushani SB, Franklin VX, 2010. Shewanelia putrefaciens: a rare microbial agent associated with a non-healing ulcer in a leprosy patient. Indian J Lepr 82: 205207.

    • Search Google Scholar
    • Export Citation
  • 52.

    Gressier M, Mbayo D, Deramond H, Grados F, Eb F, Canarelli B, 2010. First case of human spondylodiscitis due to Shewanella algae. Int J Infect Dis 14 (Suppl 3): e261e264.

    • Search Google Scholar
    • Export Citation
  • 53.

    Sharma KK, Kalawat U, 2010. Emerging infections: Shewanella - a series of five cases. J Lab Physicians 2: 6165.

  • 54.

    Tucker C, Baroso G, Tan P, 2010. Ventilator-associated pneumonia due to Shewanella putrefaciens. Am J Health Syst Pharm 67: 10071009.

    • Search Google Scholar
    • Export Citation
  • 55.

    Goyal R, Kaur N, Thakur R, 2011. Human soft tissue infection by the emerging pathogen Shewanella algae. J Infect Dev Ctries 5: 310312.

    • Search Google Scholar
    • Export Citation
  • 56.

    Finkelstein R, Oren I, 2011. Soft tissue infections caused by marine bacterial pathogens: epidemiology, diagnosis, and management. Curr Infect Dis Rep 13: 470477.

    • Search Google Scholar
    • Export Citation
  • 57.

    Heritier C, Poirel L, Nordmann P, 2004. Genetic and biochemical characterization of a chromosome-encoded carbapenem-hydrolyzing ambler class D beta-lactamase from Shewanella algae. Antimicrob Agents Chemother 48: 16701675.

    • Search Google Scholar
    • Export Citation

Author Notes

* Address correspondence to Nicolas Vignier, Department of Infectious and Tropical Diseases, University Hospital of Fort-de-France, 97200 Fort-de-France, Martinique. E-mail: vigniernicolas@yahoo.fr

Authors' addresses: Nicolas Vignier, Morgane Barreau, and Patrick Hochedez, Department of Infectious and Tropical Diseases, University Hospital of Fort-de-France, 97200 Fort-de-France, Martinique, E-mails: vigniernicolas@yahoo.fr, morgane-barreau@orange.fr, and patrick.hochedez@chu-fortdefrance.fr. Claude Olive and Rafaelle Théodose, Bacteriology Laboratory, University Hospital of Fort-de-France, 97200 Fort-de-France, Martinique, E-mails: claude.olive@chu-fortdefrance.fr and rafaelle.theodose@chu-fortdefrance.fr. Emilie Baubion, Department of Dermatology, University Hospital of Fort-de-France, 97200 Fort-de-France, Martinique, E-mail: emilie.baubion@chu-fortdefrance.fr. André Cabié, Department of Infectious and Tropical Diseases and INSERM CIE802, University Hospital of Fort-de-France, 97200 Fort-de-France, Martinique, E-mail: andre.cabie@chu-fortdefrance.fr.

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