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Emerging causes of superficial and invasive infections following marine injuries and exposures.

Soft tissue bacterial infections following aquatic animal bites, stings, and minor injuries occur commonly and usually on the extremities in fishermen and beachgoers worldwide after freshwater and saltwater exposures. Although Louisiana's shorelines are rapidly retreating today from levee projects, saltwater intrusions, and hurricane storm surges, Louisiana has more tidal, saltwater, and brackish water shorelines (more than 7,000 miles) than any other state, including Alaska and Hawaii. As a result, Louisiana residents are often exposed to marine pathogens when fishing or working offshore or when enjoying Louisiana's miles of shorelines.

Although many species of bacteria have been isolated from marine wounds, superficial soft tissue and invasive infections following marine injuries and exposures are most commonly caused by a small number of bacterial species, including Aeromonas hydrophila, Edwardsiella tarda, Erysipelartx rhusiopathiae, Mycobacterium marinurn, and Vibrio vulnificus. Of the causative marine pathogens, the most serious and often fatal invasive infections are caused by Vibrio vulnificus. In addition to these species, several other aquatic bacteria have recently been identified as emerging causes of superficial and invasive infections following marine injuries and exposures, including marine mammal (dolphins and seals) Brucella species, Chromobacterium violaceum, Comamonas species, Shewanella algae, and Streptococcus iniae. The objectives of this review are to describe the epidemiology, presenting clinical manifestations, diagnostic and treatment strategies, and outcomes of both the superficial and the deeper invasive infections caused by the newly emerging marine bacterial pathogens.

MATERIALS AND METHODS

Initially, several search engines were queried for references using all keywords listed as medical subject heading (MESH) words for searches. The keywords included: marine injuries, marine animal injuries, marine infections, aquatic infections; marine bacteria; fish pathogens; aquaculture-related fish infections; marine mammal pathogens. The sources of US cases of superficial and invasive infections following marine injuries and exposures were provided by peer-reviewed, published case reports and series, descriptive studies, case-control studies, and Morbidity Mortality Weekly Reports (MMWR) published by the United States (US) Centers for Disease Control and Prevention (CDC). Infections were classified as superficial (abscess), spreading (cellulitis, lymphangitis), and invasive (arthritis, tenosynovitis, osteomyelitis, metastatic abscesses, e.g., neurobrucellosis). Bacterial species were classified by Gram staining status, antibiotic susceptibilities, and biochemical and molecular signatures (Table 1).

[FIGURE 1 OMITTED]

NEWLY EMERGING CAUSES OF MARINE INFECTIONS

Marine Mammal Brucella Species

Brucellosis, or undulant fever, is a zoonotic infectious disease caused by several species-specific strains of Brucella, which are small, gram-negative, non-motile, non-spore-forming, rod-shaped coccobacilli. Brucellosis is rare in the United States, with an average of 113 cases reported to the CDC annually over the period 2000-2009. (1) Most cases in the United States are caused by consuming unpasteurized milk or cheese from infected cattle (B. abortus) or goats (B. melitensis), hunting feral swine (B. suis), and occupational exposures among laboratory workers handling Brucella species. (1,2) New zoonotic reservoirs of Brucella strains have now been identified in pinnipeds (seals, sea lions, and walruses) and cetaceans (dolphins, porpoises, and whales), collectively referred to as marine mammal Brucella species and tentatively classified as B. pinnepediae and B. cetaceae, respectively. (2) Seroprevalence studies have now identified marine mammal Brucella species strains in both seals and porpoises stranded and dying along the New England Coast. (3) In humans, brucellosis can cause fever, febrile sweating, headache, weakness, myalgia, back pain, and rarely, invasive granulomatous disease in bone, liver, and the central nervous system (neurobrucellosis). (2) Four human cases of marine mammal brucellosis have been reported since 2001 with two cases in males from coastal Peru treated in the United States for neurobrucellosis with granulomatous intracerebral lesions; one patient in New Zealand with spinal osteomyelitis; and one veterinary laboratory worker with a mild form of brucellosis. (2,4)

The diagnosis of brucellosis can be by slow-growing culture from blood or biopsies, serological demonstration of Brucella antibodies (ELISA) for the more commonly encountered strains, and PCR assays for separation and speciation of the terrestrial and marine mammal strains. Invasive brucellosis and neurobrucellosis will require prolonged treatment (2-12 months) with a combination of intravenous rifampin, doxycycline, and gentamicin for a week or more followed by six or more weeks of oral doxycycline and rifampin. (1) For persons exposed to stranded marine mammals or their carcasses, a three-week course of antimicrobial prophylaxis with oral doxycycline and rifampin has been recommended by the CDC in addition to symptom surveillance with daily fever checks for 24 weeks. (1) For children and others who cannot take doxycycline, a three-week course of trimethoprim-sulfamethoxazole and rifampin is recommended. (1)

On October 27, 2011, six months after the Deepwater Horizon BP oil spill off the Louisiana coast in April 2010, the National Oceanic and Atmospheric Administration (NOAA) confirmed that 5 of the 21 tested bottle-nosed dolphins among the 580 dolphins that died in the northern Gulf of Mexico in 2010-2011 had marine mammal brucellosis. (5) NOAA scientists concluded that severe environmental stress, including crude oil exposures, could have compromised the animal's immune systems, making them more susceptible to a zoonotic infectious disease common in marine mammals. (5) As a result, the NOAA advises that anyone who encounters a stranded or dead dolphin in the Gulf of Mexico region not touch the animal, keep all pets away from the animal, and notify the NOAA immediately at 1-877-942-5343. (5) All persons who handle stranded marine mammals or who participate in autopsies on their carcasses should be educated as to the potential risks of marine mammal brucellosis and use personal protective equipment, including respirators. (1,5)

Chromobacterium violaceum

Chromobacterium violaceum is an aerobic, gram-negative bacillus, and a saprophyte found in soil and water in tropical and subtropical regions worldwide. (6) The organism grows rapidly on ordinary culture media and is typically first identified by the violet-color of its colonies. (6) Non-pigmented strains of C. violaceum are less commonly found than pigmented strains, but do co-exist with pigmented strains and can cause mixed infections. (7) Although widely distributed, C. violaceum is a low-grade pathogen and causes few infections, with most reported from the southeastern US with high case fatality rates, especially in the immunocompromised. (8) In 1982, Macher and colleagues reported 12 cases of C. violaceum infections in the United States in patients with chronic granulomatous disease--seven of whom died of invasive septicemia 7 days to 15 months after initial infections. (9) The portal of entry for C. violaceum is typically a break in the skin from an insect bite, laceration, or fish bite, followed by exposure to brackish or stagnant water. An ulcerated skin lesion with a bluish purulent discharge develops at the initial injury site with regional swelling usually on an extremity. Within days, invasive septicemia may occur, especially in the immunocompromised, with high fevers and disseminated macular skin lesions that progress to abscesses. Abscesses may also occur in bone and in the liver. The organism is susceptible to aminoglycosides, quinolones, tetracyclines, imipenem, and trimethoprim-sulfamethoxazole but resistant to penicillins and cephalosporins. (8) Due to high case fatalify rates, treatment of suspected C. violaceum infections should begin immediately with drainage of all purulent abscess collections and combined intravenous antibiotic therapy. A high index of suspicion for C. violaceum infections should be maintained in all cases with a rapid progression from an ulcerated lesion in a soil- or water-contaminated minor wound followed by sepsis, widespread cutaneous involvement, and liver abscesses. Rapidly growing violet-pigmented colonies on blood or MacConkey agar are diagnostic of the pigmented strains of C. violaceum.

Comamonas species

Comamonas species are flagellated, gram-negative, rod-shaped bacteria that form characteristic pink-pigmented colonies on ordinary culture media. (10) Like C. violaceum, Comamonas species are widely distributed in nature in soil and water but rarely cause human infections, with 24 cases reported to date and a case fatality rate of 12.5%. (10) Of the 24 reported human cases, eight cases were associated with appendicitis or perforated appendix, suggesting that Comamonas species could be human gastrointestinal tract commensals. (10) In seven cases, there were no predisposing factors, with the exception of one case following a tiger bite. (10) Comamonas peritonitis occurred in eight cases, endocarditis in two cases, and one in an intravenous drug abuser. (10)

Smith and Gradon reported a case of Comamonas sepsis in a previously healthy 89-year-old man who slept next to a tropical fish tank in which fish had started to die rapidly, turning the tank water opaque and malodorous. (10) The patient presented with sore throat, myalgia, fever, and had two sequential positive blood cultures for Comamonas species sensitive to all antibiotics tested. (10) The patient was treated with levofloxacin, and his condition rapidly stabilized without sequelae. (10) Since the patient denied any physical contact with his son's fish tank, the authors concluded that the most likely source of infection was by inhalation and recommended that Comamonas bacteremia be considered in the differential diagnosis of sepsis in patients who are tropical fish tank enthusiasts. (10)

Shewanella species

Shewanella species are saprophytic gram-negative bacteria that are distributed in temperate regions worldwide and are part of the normal microflora of the marine environment. like Aeromois hyhrophila, Erysipelothrix rhusiopathiae, and Vibrio vulnificus. (11-13) There are more than 50 species of Shewanella, all of which produce yellowish-brown mucoid colonies that emit hydrogen sulfide in culture. (11-13) Several Shewanella species have been recently recognized as emerging causes of soft tissue and invasive infections after seawater exposures, including S. algae, S. haliotis, S. putrefaciens, and S. xiamenensis. (13) The most common clinical manifestations of Shewanella infections are deep ulcers associated with hemorrhagic bullae, usually on the lower extremities, otitis externa, otitis media, and bacteremia. (11-13) Non-healing ulcers have resulted in necrotizing fasciitis, compartment syndromes requiring decompressive fasciotomies, and osteomyelitis (Figure 1). (11-13) Shewanella septicemia has been associated with endocarditis and meningitis. (11-13) Shewanella pneumonia, cholecystitis, and peritonitis have been reported following aspiration or ingestion of seawater. (12) Besides seawater exposure and ingestion of raw seafood, other common risk factors for Shewanella infections have included minor trauma or lacerations in marine environments, pre-existing lower extremity ulcers, and immunocompromise. (13) Wagner and colleagues reported a case of S. algae-infected chronic leg ulcers in a 52-year-old female with autoimmune vasculitis and myasthenia gravis seven months after returning from a Mediterranean vacation during which she reported frequently bathing in the surf. (11) Poovorawan and colleagues reported another recent case of severe S. haliotis soft tissue infection in the left lower leg with compartment syndrome in a 52-year-old female from Bangkok who had undergone orthotopic liver transplantation six months previously and reported frequent handling of fresh saltwater fish in a seafood market (Figure 1). (13) In a descriptive analysis of 16 Shewanella cases in Martinique and another 239 cases reported in the literature over a 14-year period, 1997-2012, Vignier and co-investigators noted that 79% of patients had predisposing risk factors for Shewanella infections--53% of patients had a skin or mucosal portal of entry, and 44% of cases reported prior marine exposures. (12) The case fatality rate was 13% in their case series. (12)

The diagnosis of Shewanella infections can be established by positive blood or lesion aspirate cultures, but the speciation of Shewanella causative strains will require molecular characterization by PCR. (12) Most species are sensitive to a broad range of antibiotics, including aminoglycosides, third-generation cephalosporins, and quinolones. S. algae is resistant to penicillins and first- and second-generation cephalosporins. (11,12) For invasive infections, especially in immunosuppressed patients, most authorities recommend two weeks of intravenous antibiotic therapy with third-generation cephalosporins combined with either aminoglycosides or quinolones, followed by two to three weeks of oral antibiotic therapy. (11-13) Early surgical consultation is also recommended for drainage of bullous lesions, debridement of ulcers, and monitoring for potential extremity compartment syndromes requiring decompressive fasciotomies (Figure 1).

Streptococcus iniae

Streptococcus iniae, a gram-positive, B-hemolytic streptococcus unassigned to a Lancefield Group, was first identified in 1976 as the cause of subcutaneous abscesses in Amazon freshwater dolphins in US aquariums. (14) Often misidentified as S. viridians, S. iniae has emerged as a major fish pathogen capable of causing epizootic outbreaks of invasive streptococcal disease in farm-raised fish. (15) S. iniae initially colonizes the surface of the fish, causing cellulitis which can be complicated by invasive meningoencephalitis with 30%-50% mortality in affected aquaculture ponds. (15) Commercially devastating outbreaks have now been reported worldwide in other farm-raised fresh and saltwater fish species, including coho salmon, rainbow trout, tilapia, and yellowtail. (15)

The first human cases of S. iniae invasive infections were reported from the Toronto area in 1996, when a cluster of four cases in patients of Asian descent who had recently prepared fresh, whole farm-raised fish was reported to public health authorities. (15) Three of these patients had bacteremic cellulitis of the hands secondary to soft tissue injuries that occurred during the preparation of fresh fish obtained from wet markets; and the fourth patient had S. iniae sepsis with arthritis, meningitis, and endocarditis. (15) During a follow-up, one-year surveillance investigation, Weinstein and colleagues identified 11 patients with invasive S. iniae infections with cellulitis of the hands in eight cases, endocarditis in one case, and either arthritis or cellulitis in the remaining cases. (15) All of the patients had recently handled live or freshly killed fish, and eight patients suffered percutaneous injuries while preparing the fish and developed cellulitis within 16-24 hours of their injuries. (15) Most of the fish species identified were tilapia commonly used in Asian cuisine. (15) The median age of the case-patients was 67 years (range 40-80 years); the female-to-male ratio was 2:1; and all patients were of Asian descent. (15) Four patients had chronic underlying diseases, including diabetes, chronic renal failure, rheumatic heart disease, and osteoarthritis. (15) In all 11 cases, invasive S. iniae infection was culture-confirmed; and S. iniae isolates from nine of these cases were identical by pulsed-field gel electrophoresis (PFGE) and also matched PFGE-identified S. iniae isolates obtained from the surface and brains of infected tilapia from local aquaculture farms. (15) In all cases, the S. iniae isolates were sensitive to a broad range of antibiotics, including aminoglycosides, cephalosporins, macrolides, penicillins, and trimethoprim-sulfamethoxazole. (15) All patients were admitted to hospitals, treated with parenteral antibiotics, and responded to antibiotic therapy within two to four days. (15) The investigators concluded that most patients had been inoculated with S. iniae in association with minor injuries received during preparation of fresh fish, especially tilapia, and recommended that precautionary measures be taken, especially by immunocompromised elderly patients, when handling whole, uncooked fish to prevent S. iniae infections. (15)

GENERAL MANAGEMENT OF MARINE INJURIES

Even minor abrasions and lacerations sustained in marine environments should be considered potentially contaminated with common marine microbes, such as Vibrio species. Following any specific detoxification measures, such as hot water immersion for stingray injuries or topical acetic acid for fire coral and jellyfish stings, all wounds should be irrigated with a sterile diluent solution, if possible, such as normal saline. Crushed or devitalized tissues should be excised by sharp dissection under local anesthesia or peripheral nerve blocks. Foreign bodies should be removed. Diagnostic imaging is often indicated, especially in puncture wounds, to exclude retained foreign bodies. Potential constriction bands, such as bracelets, rings, and watches, should be removed from the injured extremity and baseline extremity circumference measurements taken in the event of swelling from necrotizing fasciitis and compartment syndromes. Sequential surgical debridements will be indicated in many cases--in all cases of necrotizing fasciitis --and following fasciotomies for compartment syndromes. Most wounds should be left open or packed open to heal by secondary intention. Delayed primary closures may be indicated for potentially disfiguring facial wounds. Tetanus prophylaxis is indicated for all marine wounds.

GENERAL MANAGEMENT OF CONTAMINATED MARINE WOUNDS

Grossly contaminated or infected wounds and all puncture wounds should be cultured, and the microbiology laboratory should be notified in advance that special culture media and stains will likely be required, such as sodium-enriched media for Vibrio species and acid-fast stains/cultures for marine aquatic mycobacteria. With the exception of minor marine wounds demonstrating localized cellulitis or spreading erysipeloid-type reactions, most other marine infections and all gram-negative and mycobacterial marine infections will require therapy with antibiotic combinations. (1) Streptococcus iniae infections are characterized by impetigo and cellulitis, and Erysipelothrix rhusthopathiae infections cause erysipeloid manifestations. These infections may be treated empirically with single antibiotics, specifically penicillins or macrolides in cases of penicillin allergy, until culture and antibiotic susceptibility results are reported.

In all suspected cases of M. marinum infection, clinicians will need to pursue confirmation by culture and begin combined antibiotic therapy with clarithromycin and ethambutol. (11,12) Persons who are immunosuppressed or have cirrhosis, hepatitis, uremia, hemosiderosis, or other iron-retaining conditions, are at higher risks for invasive Vibrio infections with the highest case fatality rates. They also should be empirically covered with combinations of third-generation cephalosporins (ceftazidime) and tetracyclines (doxycycline), fluoroquinolones and tetracyclines, or aminoglycosides and trimethroprim-sulfamethoxazole. The clinical microbiology laboratory should be consulted frequently, and all definitive antibiotic therapy should be based on precise pathogen identification by culture or molecular signature and antibiotic susceptibility testing.

CONCLUSIONS AND RECOMMENDATIONS

Clinicians should maintain a high index of suspicion regarding potentially catastrophic bacterial infections, especially Vibrio vulnificus and Chromobacterium violaceum infections, following marine injuries and exposures. Patients with well-known risk factors for marine infections, including those with suppressed immune response mechanisms, liver disease, alcoholism, diabetes, chronic renal disease, AIDS, and cancer, should be cautioned about the risks of marine infections through exposures to marine animals, seawater, the preparation of freshly-killed seafood, and the ingestion of seawater or consumption of raw or undercooked seafood, especially oysters. All persons who handle stranded marine mammals, such as bottle-nose dolphins common in the northern Gulf of Mexico, or who participate in necropsies on their carcasses should be educated as to the potential risks of marine mammal brucellosis and the use of personal protective equipment, including respirators.

REFERENCES

(1.) United States Centers for Disease Contiol and Prevention (CDC). Human exposures to marine Brucella isolated from a harbor porpoise-Maine, 2012. Morb Mort Week Rep 61: 461-463.

(2.) Sohn AH, frobert WS Glaser CA, et al. Human neurobrucellosis with intracerebral granuloma caused by marine mammal Brucella spp. Emerg Infect Dis 200; 9: 485-488.

(3.) Maratea J, Ewalt DR, Frasca S, et al. Evidence of Brucella sp. infection in marine mammals stranded along the coast of southern New England. J Zoo Wildlife Med 2003; 34: 256-261.

(4.) McDonald WL, Jamaludin R, Mackereft G, et al. Characterization of Brucella sp. stiain as a marine mammal type despite isolation from a patient with spinal osteomyelitis in New Zealand. J Clin Microbiol 2006; 44: 4363-4370.

(5.) United States Departinent of Commerce. National Oceanographic and Atmospheric Administration. NOAA finds bacterial infection as a cause of death for five northern Gulf dolphins; investigation continues. Available at www.noaanews.noaa.gov/ stories2011/20111027-dolphins.html

(6.) Petrillo VF, Severo V, Santos MM, Edelweiss EL. Recurrent infection with Chromobacterium violaceum: first case report from Soutir America. J Infect 1984; 9: 167-169.

(7.) Yang CH. Nonpigmented Chromobacterium violaceum bacteremic cellulitis after a fish bite. J Microbiol Immunol Infect 2011; 44: 401-405.

(8.) Midani S, Rathore M. Chromobacterium violaceum infection. South Med J 1998; 91: 464-466.

(9.) Macher AM, Casale BT, Fauci AS. Chronic granulomatous disease of childhood and Chromobacterium violaceum infections in the South Eastern United States. Ann Intern Med 1982; 97: 51-52.

(10.) Smith MD, Gradon JD. Bacteremia due to Comamonas species associated with exposure to tropical fish. South Med J 2003; 96: 815-817.

(11.) Wagner N, Otto L, Podda M, et al. Travel-related chronic hemorrhagic leg ulcer infection by Shewanella algae. J Travel Med 2013; 20: 262-264.

(12.) Vignier N, Barreau M, Olive C, et al. Human infection with Shewanella putrefaciens and S. algae: Report of 16 cases in Martinique and review of the literature. Am J Trop Med Hyg 2013; 89: 151-156.

(13.) Poovorawrn K, Chatsuwan T, Lakananurk N, et al. Shewanella haliotis associated with severe soft tissue infection, Thailand, 2012. Emerg Infect Dis 2013; 19: 1019-1021.

(14.) Pier GB, Madin SH. Stieptococcus iniae sp. nov., a beta-hemolytic streptococcus isolated from an Amazon freshwater dolphin, Inia geoffrensis. Int J Syst Bacteriol 1976; 26:545-553.

(15.) Weinstein MR, Litt M, Kertesz DA, et al. Invasive infections due to a fish pathogen, Stieptococcus iniae. N Engl J Med 1997; 337: 589-594.

James H. Diaz, MD, MPH & TM, DrPH, FCCM, FACMT

Dr. Diaz is Professor and Head of Environmental and Occupational Health Sciences in the School of Public Health and Professor of Anesthesiology in the School of Medicine at Louisiana State University Health Sciences Center in New Orleans.
Table 1: Representative marine pathogens and their antiobiotic
susceptibilities

Bacteria                         Antibiotic susceptibilities

Gram-positive bacteria

Erysipelothrix rksiopalie        Amoxicillin, piperacillin-
                                 taxobactam, erythromycin,
                                 doxycycline, aminoglycosides

Streptococcus iniae              Amoxicillin, piperacillin-
                                 tazobactam, cephalosporins

Gram-negative bacteria

Aeromonas hydrophila             Third-generation
                                 cephalosporins, second-
                                 generation quinolones,
                                 resistant to penicillins and
                                 first-generation
                                 cephalosporins

Gram-negative marine mammal
Brucella spp.

B. cetaceae (dolphin-            Tetracyclines (doxycycline) +
porpoise strain)                 rifampin or trimethoprim-
                                 sulfamethoxazole + rifampin
B. pennipediae (seal strain)

Chromobacterium niolaceiim       Aminoglycosides, carbapenems,
Comamonas spp.                   tetracyclines, trimethoprim-
                                 sulfamethoxazole, resistant to
                                 penicillins and cephalosporins

C.acidons                        Piperacillin-tazobactam,
                                 quinolones, aminoglycosides,
C.terrigena                      third-generation
                                 cephalosporins
C.testosteroni

Edwardsiella tarda               Aminoglycosides,
                                 cephalosporins, quinolones,
                                 teracyclines (doxycycline)

Morganella morganii              Carbapenems, cefepime,
                                 ciprofloxacin

Pseudomonas aeruginosa           Piperacillin-taxobactam,
                                 antipseudomonal
                                 cephalosporins, carbapenems,
                                 quinolones, aminoglycosides

Shewanellaspp,                   Aminoglycosides, quinolones,
  S. algae                       third generation
  S. putrefaciens                cephalosporins, resistant to
                                 penicillins and first-and
                                 second-generation
                                 cephalosporins

Gram-negative marine vibrios
  Vibrio vulnificus              Doxycycline + ceftazidime or
                                 quinolone; or cefotaxime +
                                 quinolone

  Vibrio carchariae              Antibiotics are not usually
                                 indicated for self-limited
  Vibrio parahemolyticus         Vibrio gastroenteritis

Marine acid-fast mycobacteria
  Mycobacterium marinum          Clarithromycin +
      (causes fish tank          ethambutol, rifampin
      granuloma)
    M. fortuitum                 Rifampin + streptomycin
    M. terrae
    M. ulcerans (causes
      Buruli ulcer following
      soil and/or stagnant
      water-contaminated
      wounds)
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Author:Diaz, James H.
Publication:The Journal of the Louisiana State Medical Society
Article Type:Report
Date:May 1, 2014
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