Chapter 79 Injuries From Nonvenomous Aquatic Animals
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The expanses of ocean and freshwater that cover the earth are the greatest wilderness. Seventy-one percent (or 362 million km2 [139,768,981 miles2]) of the earth’s surface is composed of ocean, the volume of which exceeds 523 km3 (325 million miles3). Underneath the surface lie huge mountain ranges, deep valleys, and many active volcanoes. Nearly one-half of the sea floor is composed of the abyssal plain, which lies at an average depth of 4 km (2.5 miles) and is largely devoid of life forms. Within the undersea realm exist four-fifths of all living organisms. We are aware of approximately 275,000 ocean species and thousands are as yet undiscovered.
The opportunity for direct encounters with aquatic organisms continues to increase because of enhanced recreational, industrial, scientific, and military oceanic and riverine activities related to ever-rising human populations. The most common cause of injuries is handling of animals that bite and sting in self-defense, followed by provoked, then unprovoked encounters.
Nearly 80% of the world’s population resides in coastal regions. In the United States, 50% of the population lives within 80 km (50 miles) of a coastline. It is estimated that 127 million U.S. citizens live along the coasts. A significant proportion of this population is directly involved as entrants into the aquatic world. Therefore, it is imperative that clinicians be familiar with hazards unique to the aquatic environment.
Although noxious marine organisms are concentrated predominantly in warm temperate and tropical seas, particularly in the Indo-Pacific region, hazardous animals may be found as far north as 50° latitude. Saltwater aquariums in private homes and public settings, intercontinental seafood shipping, and increasing accessibility of air travel to sport scuba and skin divers contribute to the risks.
Like the rainforest, the ocean depths have the potential to reveal virtually limitless active pharmaceutical agents, including antihelminthic, anticoagulant, antifungal, antimalarial, antiprotozoal, antituberculosis, antiinflammatory, and antiviral.120 Genetically engineered reproduction of the adhesive protein of the marine mussel Mytilus edulis has created a tissue adhesive agent that may one day prove superior to cyanoacrylic compounds. The sandcastle worm (Phragmatopoma califonica) manufactures a glue used to stick together sand and shell fragments. This is being investigated as a tissue adhesive for fragmented human bones. Toxins isolated from ascidians (tunicates, or sea squirts) include cyclic peptides, some of which (esteinascidin 743, aplidine) have undergone evaluation for cancer chemotherapy; others (e.g., thiocoraline and kahalalide F) may follow. Investigative techniques continue to improve. In pursuit of anatomic information that can elucidate the biology and ecology of fish, evolution, cellular physiology, and aquatic models of human disease, nuclear radiologists have performed in vivo nuclear magnetic resonance imaging (MRI) and spectroscopy of anesthetized (tricaine methsulfonate [MS222]) aquatic organisms.26 Most marine organisms rely on antimicrobial components of their innate immune defenses to combat pathogens. From this unique perspective, scientists seek to identify novel antimicrobials, among which the most promising are marine cationic antimicrobial peptides, defined as small (10 to 40 amino acids) peptides containing a prevalence of positively charged residues (lysine and arginine).137 As examples, these have been found in teleost fishes (pardaxin, pleurocidin, hepcidin), tunicates (styelin, clavanin), chelicerates (big defensin, tachyplesin), crustaceans (callinectin), gastropods (dolabellanin), and mollusks (mytilin). Their activities include synergy to induce cell lysis, modulating the host immune response, chemotaxis, macrophage development, production or inhibition of cytokines, and so forth. Sponges (phylum Porifera) and sharks (order Selachii) have become particular foci of biomedical screening over the past three decades.
Despite the wondrous nature of the deep, danger exists. The ubiquity of hazardous creatures and their propensity to appear at inopportune times make it imperative to be aware of them, to respect their territorial rights, and to avoid unpleasant contact with them.
Divisions and Definitions
Dangerous aquatic animals are divided into four groups: (1) those that bite, rip, puncture, or deliver an electric shock without envenomation; (2) those that sting (envenom),163 discussed in Chapters 80 and 81; (3) those that are poisonous on ingestion (see Chapter 72); and (4) those that induce allergies (see Chapter 73). Aquatic skin disorders are discussed in Chapter 82.
In Defense of the Fish
As in all nature (except for humans), indiscriminate aggression is rarely involved when injuries are inflicted by aquatic animals. Most injuries result from gestures of warning or self-defense; aquatic creatures rarely attack humans without provocation. Attacks are made in defense of young, in territorial dispute when mating activities are interrupted, or to procure food. Caution is the key word when dealing with potentially injurious aquatic creatures.
General Principles of First Aid
The physician must adhere to fundamental principles of medical rescue. Although many injuries and envenomations have unique clinical presentations, the cornerstone of therapy is immediate attention to the airway, breathing, and circulation. Along with specific interventions directed against a particular venom or poison, the rescuer must simultaneously be certain that the victim maintains a patent airway, breathes spontaneously or with assistance, and is supported by an adequate blood pressure. Because marine attacks and envenomations often affect swimmers and divers, the rescuer should anticipate drowning (see Chapter 75), immersion hypothermia (see Chapter 6), and decompression sickness or arterial air embolism (see Chapter 77). Any victim rescued from the ocean should be thoroughly examined for external and internal signs of a bite, puncture, or sting if such is a possibility.
Whether the injury is a bite, abrasion, or puncture, meticulous attention to basic wound management is necessary to facilitate healing and minimize post-traumatic infection.
All wounds acquired in the natural aquatic environment should be vigorously irrigated with sterile diluent, preferably normal saline (0.9% sodium chloride) solution. Seawater is not recommended as an irrigant because it carries a hypothetical infection risk. Sterile water or hypotonic saline is acceptable. Tap water (preferably disinfected) is a suitable irrigant and should be used when the alternative is delay to irrigation.5 Irrigation should be performed before and after debridement. A 19-gauge needle or 18-gauge plastic intravenous (IV) catheter attached to a syringe that delivers a pressure of 7031 to 14,061 kg/m2 (10 to 20 psi) will dislodge most bacteria without forcing irrigation fluid into tissue along the wound edges or deeper along dissecting tissue planes. Convenient ring-handle syringes with blunt irrigation tips and IV tubing that connects to standard IV bags are useful. At least 100 to 250 mL of irrigant should be flushed through each wound. If a laceration is from a stingray, proteinaceous (and possibly) heat-labile venom may be present in the wound. Therefore, if the wound is still painful at the time of irrigation, the irrigant may be warmed to a maximum temperature of 45° C (113° F).9
Antiseptic may be added to the irrigant if the wound appears to be highly contaminated. Povidone-iodine solution in a concentration of 1% to 5% may be used with a contact time of 1 to 5 minutes.131,189 When antiseptic irrigation is completed, the wound should be thoroughly irrigated with normal saline or tap water to minimize tissue toxicity from the antiseptic. Antiseptics that are particularly harmful to tissues include full-strength hydrogen peroxide, povidone-iodine scrub solution, hexachlorophene detergent, and silver nitrate.
Scrubbing should be used to remove debris that cannot be irrigated from the wound. Sharp surgical debridement is preferable to sponge scrubbing, which may increase infection rates, particularly when applied with harsh antiseptic solutions. Poloxamer 188 (Pluronic F-68), a nontoxic, nonionic surfactant skin wound cleanser (found in Shur-Clens 20%) that may be used to irrigate or scrub wounds, does not offer any significant advantage over traditional sterile saline irrigation.
Debridement is more effective than irrigation at removing bacteria and debris. Crushed or devitalized tissue should be removed with sharp dissection to provide clean wound edges and encourage brisk healing with minimal infection risk. The limitations are those imposed by anatomy, specifically skin tautness or the presence of vital structures. Anesthesia of wound edges may be attained by regional nerve block or local infiltration with lidocaine or bupivacaine, which do not damage local tissue defenses. A topical anesthetic mixture of tetracaine, epinephrine, and cocaine may be less desirable because of the vasoconstrictive effect of epinephrine and theoretical infection-potentiating effects. Definitive wound exploration, debridement, and repair should be undertaken in an appropriate sterile environment. It is often impractical to explore complex wounds in the emergency department. When necessary, operating loupes should be used to inspect the wound for residual foreign material, such as sand, seaweed, teeth, spine fragments, or integumentary sheath shards. Standard radiographs, static soft tissue techniques, computed tomography, ultrasound, MRI, or fluoroscopy may be used preoperatively or perioperatively to localize spines or teeth.
The decision to close a wound must weigh the risk of infection. The incidence of infection is high in wounds acquired in natural bodies of water because such wounds may be contaminated with venom, potentially virulent microorganisms, or both; because early adequate irrigation and debridement are often unavailable; and because definitive care is often delayed. Tight wound closure restricts drainage and promotes bacterial proliferation, particularly from anaerobes, which are common contaminants. Wounds at high risk in this regard include those on the hands, wrists, or feet; punctures and crush injuries; wounds into areas of fat with poor vascularity; and wounds to victims who are immunosuppressed. Whenever possible, the use of sutures to close dead space in contaminated wounds should be minimized because the absorbable sutures act as foreign bodies.
Prophylaxis against Tetanus
Any wound that disrupts the skin can become contaminated with Clostridium tetani. Anaerobic bacteria, predominantly of the genus Clostridium, have been isolated in shark tissue and as part of the oral flora of alligators and crocodiles. Proper immunization with tetanus toxoid virtually eliminates the risk of disease. However, although it was previously accepted that the protective level of toxin-neutralizing antibody is 0.01 antitoxin unit/mL, it appears that clinical tetanus can develop despite an antibody level many times that amount. Therefore, it is imperative to provide an early and adequate booster injection. If the victim is older than age 50 years, is from an underdeveloped country, or cannot provide a definite history of tetanus immunization, it is likely that circulating toxin-neutralizing antibody will be suboptimal. Prophylaxis should be provided according to the scheme shown in Chapter 22 in Table 22-5. Tdap (tetanus, reduced diphtheria, and acellular pertussis vaccine) should be used instead of Td for routine tetanus boosters and wound management in adolescents and adults.
Bacteriology of the Aquatic Environment
Wounds acquired in the aquatic environment are soaked in natural source water and sometimes contaminated with sediment. Penetration of the skin by the spines or teeth of animals, the razor edges of coral or shellfish, or mechanical objects such as the blades of a boat propeller may inoculate pathogenic organisms into a wound. Sports activities, such as surfing, snorkeling, and diving, lead to ubiquitous abrasions and minor lacerations that heal slowly and with marked soft tissue inflammation. Wounds acquired in the aquatic environment tend to become infected and may be refractory to standard antimicrobial therapy. Not infrequently, indolent or extensive soft tissue infections develop in the normal or immunocompromised host.15,141 A clinician faced with a serious infection caused by an aquatic injury frequently needs to administer broad-spectrum antibiotics to a patient before definitive laboratory identification of pathogenic organisms has been obtained.
Ocean water provides a saline milieu for microbes. The salt dissolved in ocean water (3.2% to 3.5%) is 78% sodium chloride (sodium 10.752 g/kg; chlorine 19.345 g/kg). Other constituents include sulfate (2.791 g/kg), magnesium (1.295 g/kg), potassium (0.39 g/kg), bicarbonate (0.145 g/kg), bromine (0.066 g/kg), boric acid (0.027 g/kg), strontium (0.013 g/kg), and fluorine (0.0013 g/kg). The temperature of the surface waters varies with latitude, currents, and season. Tropical waters are warmer and maintain a more constant temperature than do temperate and subtropical waters, which are subject to substantial meteorologic variation. Shallow and turbulent coastal waters are generally richer in nutrients than is the open ocean, which is reflected in the diversity of life that can be identified in the intertidal zone. Although the greatest number and diversity of bacteria are found near the ocean surface, diverse bacteria and fungi are found in marine silts, sediments, and sand and within the oral cavities of marine organisms. In ocean waters having marked differences in density, the greatest concentration of bacteria is noted at the thermocline, where changes in both temperature and salinity are usually found.149 This effect is less active in many coastal waters, where tide and wind-driven perturbations may create a more even distribution of sediments, microbes, salinity, and temperature. Microbes are most abundant in areas that have the greatest numbers of higher life forms. Marine bacteria are generally halophilic, heterotrophic, motile, and gram-negative rod forms. Growth requirements vary from species to species with respect to use of organic carbon and nitrogen sources, requirements for various amino acids, vitamins and cofactors, sodium, potassium, magnesium, phosphate, sulphate, chloride, and calcium. Most marine bacteria are facultative anaerobes, which can thrive in oxygen-rich environments. Few are obligatory aerobes or anaerobes. Some marine bacteria are highly proteolytic, and the proportion of proteolytic bacteria seems to be greater in the oceans than on land or in freshwater habitats.149 It has been observed that sharks may harbor multidrug-resistant bacteria, which indicates that these animals may have encountered synthetic drugs that found their way into rivers and other waterways.
Diversity of Organisms
Unique conditions of nutrient and inorganic mineral supply, temperature, and pressure have allowed evolution of unique, highly adapted marine microbes.205,206 In addition, numerous other bacteria, microalgae, protozoa, fungi, yeasts, and viruses have been identified in or cultured from seawater, marine sediments, marine life, and marine-acquired or marine-contaminated infected wounds or body fluids of septic victims. In their natural environment, the bacteria serve to scavenge and transform organic matter in the intricate cycles of the food and growth chains. Some of these bacteria are listed in Box 79-1.147 Enteric pathogenic bacteria have been isolated from sharks.70 A shark attack victim in South Africa who sustained serious injuries to his lower extremities was reported to have developed a fulminant infection attributed to Bacillus cereus shown to be sensitive to fluoroquinolones, amikacin, clindamycin, vancomycin, and tetracyclines and resistant to penicillin and cephalosporins (including third-generation). In another report, one shark (presumed bronze whaler) attack victim in Australia grew both Vibrio parahaemolyticus and Aeromonas caviae from his wounds, whereas another grew Vibrio alginolyticus and Aeromonas hydrophila from his wounds.152 It is now fairly well known that Vibrio species and Aeromonas species are potential pathogens residing in ocean water and fresh water.
BOX 79-1 Bacteria and Fungus Isolated from Marine Water, Sediments, Marine Animals, and Marine-Acquired Wounds
For practical purposes, most marine isolates are heterotrophic (require exogenous carbon and nitrogen-containing organic supplements) and motile gram-negative rods. Halomonas venusta, a halophilic, nonfermentative, gram-negative rod, was reported as a human pathogen in a wound that originated from a fish bite.190 Previous opinions that enteric pathogens (associated with the intestines of warm-blooded animals) deposited into marine environments ultimately succumb to sedimentation, predation, parasitism, sunlight, temperature, osmotic stress, toxic chemicals, or high salt concentration may be untrue.69 Pathogens may accumulate in surface water in association with lipoidal particulates, from which they are rapidly dispersed toward the shore by wave and wind activity. In addition, dredging, storms, upwellings, and other benthic disturbances may churn enteric organisms into the path of wastewater nutrients. In the United States, coastal and Great Lakes beaches regularly have bacteria counts above the Environmental Protection Agency’s threshold values for safety. Sewage spills and intentional industrial effluent release contribute to harmful contamination, notably including enteric bacteria.
Wound Infections Caused by Vibrio Species
Vibrio organisms can cause gastroenteric disease (gastroenteric Vibrio infections are discussed in Chapter 68) and soft tissue infections, particularly in immunocompromised hosts. Extraintestinal infections may be associated with bacteremia and death. Vibrio species are the most potentially virulent halophilic organisms that flourish in the marine environment. The teeth of a great white shark were swabbed and yielded V. alginolyticus, V. fluvialis, and V. parahaemolyticus.30 Mako shark tooth culture has yielded V. damsela, V. furnissii, and V. splendidus I.6 V. parahaemolyticus has also been identified in freshwater habitats.10 Water that is brackish (salinity of 15-25 parts per thousand [ppt]) allows the growth of Vibrio species if appropriate nutrients are present; V. vulnificus infection has been documented after exposure to waters with salinities of 2 and 4 ppt. The optimal season for exposure appears to be summer, when water temperatures encourage bacterial proliferation. In most studies reported, infections seem to cluster during the summer months; this may be related to increased numbers of people at the seashore. This has been corroborated to some degree by the observation that V. parahaemolyticus cultured from marine mammals was recovered only in the warmer months of the year in the northeastern United States or in animals from subtropical regions. Sharks appear to develop some immunity to autochthonous Vibrio species, as suggested by the detection of a binding protein similar to the immunoglobulin M (IgM) subclass of immunoglobulin. Allochthonous (for the shark) Vibrio species, such as V. carchariae, may be the agents of elasmobranch disease when the animal is under stress. Other species, such as V. anguillarum and V. tapetis, are pathogens of aquatic vertebrates or invertebrates.12
Vibrio species are halophilic, gram-negative rods that are facultative anaerobes capable of using D-glucose as their sole or principal source of carbon and energy.48 They are part of the normal flora of coastal waters not only in the United States but also in many exotic locations frequented by recreational and industrial divers and seafarers. Vibrios are mesophilic organisms and grow best at temperatures of 24° to 40° C (75.2° to 104° F), with essentially no growth below 8° to 10° C (46.4° to 50° F). Certain other “marine bacteria” are facultative psychrophiles, barophiles, or both. Vibrio species seem to require less sodium for maximal growth than do other more fastidious marine organisms, a factor that allows explosive reproduction in the 0.9% saline environment of the human body. At least 11 of the 34 recognized Vibrio species have been associated with human disease.48 Wound infections have been documented to yield V. cholerae O group 1 and non-O1, V. parahaemolyticus, V. vulnificus, V. alginolyticus, and V. damsela. Septicemia, with or without an obvious source, has been attributed to infections with V. cholerae non-01, V. parahaemolyticus, V. alginolyticus, V. vulnificus, and V. metschnikovii. Vibrio may infect fish, causing significant mortality in fish culture facilities. The affliction manifests with lethargy, loss of appetite, skin sores, exophthalmia, and gastrointestinal hemorrhage.
Vibrio parahaemolyticus is a halophilic gram-negative rod. The organisms are found in waters along the entire coastline of the United States. Generally, the incidence of clinical disease is greatest in the warm summer months when the organism is commonly found in zooplankton. V. parahaemolyticus absorbs onto chitin and to minute crustacean copepods that feed on sediment. It has been postulated that unusual warm coastal currents (such as El Niño) may contribute to increased proliferation of Vibrio species. The optimal growth temperature of V. parahaemolyticus is 35° to 37° C (95° to 98.6° F); under ideal conditions, the generation time has been estimated at less than 10 minutes, with explosive population growth from 10 to 106 organisms in 3 to 4 hours.
Extraintestinal wound infections are most common in persons who suffer chronic liver disease or immunosuppression. Although more than 95% of V. parahaemolyticus strains associated with human illness are positive, the relationship to pathogenicity of the Kanagawa reaction (production of a cell-free hemolysin on high salt-mannitol [Wagatsuma] agar), caused by a heat-stable direct hemolysin, is not yet clear. Furthermore, most marine strains are not Kanagawa positive. Virulence factors include proteases, beta-hemolysins (thermostable direct hemolysin [tdh] and tdh-related hemolysin [trh]), adhesins, and the expression of virulence genes, including the toxR operons.12,164 Some primary soft tissue infections previously attributed to V. parahaemolyticus may theoretically be attributed to misidentified V. vulnificus. Panophthalmitis requiring enucleation occurred in a man who suffered a corneal laceration.173
Vibrio vulnificus (formerly known as a “lactose [fermenting]-positive” vibrio) is a halophilic gram-negative bacillus. V. vulnificus (Latin for “wounding”) is found in virtually all U.S. coastal waters and has been reported to cause infection worldwide.11 It prefers salinity of 0.7% to 1.6%; although it prefers a habitat of warm (at least 20° C [68° F]) seawater, it can be found in much colder water. It does not appear to be associated with fecal contamination of seawater. It has been shown to exist in Chesapeake Bay with bacterial counts comparable with those reported from the Gulf of Mexico.203 A series of nine cases of Vibrio infection, in most cases of the species vulnificus, was reported associated with finning injury of the hands.47
V. vulnificus may or may not have an acidic polysaccharide capsule (opaque colony), which confers protection against bactericidal activity of human serum and phagocytosis and thus renders the organism more virulent in animals. At extremely low frequency, some strains can shift between unencapsulated (avirulent; translucent colony) and capsulated (virulent) serotypes. The encapsulated isolates show exquisite (positive) sensitivity to iron. Virulent isolates can use 100% but not 30% saturated (normal for humans) transferrin as an iron source, as well as iron in hemoglobin and hemoglobin–haptoglobin complexes. V. vulnificus exhibits enhanced growth and virulence in the presence of increased serum iron concentration or saturated transferrin-binding sites.2 V. vulnificus is classified into three biotypes: biotype 1 is pathogenic for humans and biotype 2 is pathogenic for fish.48,49 Biotype 3 causes soft-tissue infections and septicemia following contact with fish from freshwater ponds; it was first noted in Israel. Within biotype 1, various genetically distinct subgroups identified by randomly amplified polymorphic deoxyribonucleic acid (DNA) polymerase chain reaction (PCR) appear to be especially virulent.8 Furthermore, complete genomic sequencing of V. vulnificus YJ016, a biotype 1 strain, reveals gene clusters related to pathogenicity (cell adhesion, colonization, cytotoxicity, and tissue destruction), including capsular polysaccharide, siderophore biosynthesis and transport, and heme receptor and transport.49 In vivo antigen technology can identify virulence genes produced and expressed in humans.93 The ability of biotype 1 to multiply and produce a toxic metalloprotease in human serum may be a prominent virulence factor.196
Infection worsens rapidly after the initiation of symptoms and has been noted most frequently in men older than age 40 years with preexisting hepatic dysfunction (particularly cirrhosis), end-stage renal impairment, leukopenia, or impaired immunity (malignancy, leukemia, hypogammaglobulinemia, human immunodeficiency virus [HIV] infection, diabetes, bone marrow suppression, long-term corticosteroids), although it has been reported in young, previously healthy individuals.* One case followed application of fish blood by a healer as a traditional remedy to a chronic leg ulcer in an obese patient suffering from recurrent erysipelas.174 Preexisting liver disease is a predictor of death, with 50% of such individuals in one series succumbing to the illness.80 Persons with high serum iron levels (from chronic cirrhosis, hepatitis, thalassemia major, hemochromatosis, multiple transfusions [such as are given for aplastic anemia]) or achlorhydria (low gastric acid; may be iatrogenically induced with H2 blockers) may be at greater risk for fulminant bacteremia.2,168,183 This has been attributed in part to the protective effect of gastric acid, the iron requirement of the organism, and the effects of liver disease (decreased polymorphonuclear leukocyte and macrophage activity, flawed opsonization, and shunting of portal blood around the liver). It has been proposed that an effective host response against V. vulnificus and similar iron-sensitive pathogens (e.g., Listeria monocytogenes, Klebsiella spp., and Yersinia spp.) is in part augmented by hepcidin, a cysteine-rich cationic antimicrobial peptide central to iron metabolism.8,195 V. vulnificus produces a siderophore (vulnibactin) and a protease that may enhance pathogenicity.2 Other pathogenicity factors may be the polysaccharide capsule, hemolysin, type IV pili and other proteases, including a serine protease and a 45-kDa metalloprotease regulated through quorum sensing at a lower temperature than core body temperature.124,194
The syndrome consists of flu-like malaise, fever, vomiting, diarrhea, chills, hypotension, and early skin vesiculation that evolve into necrotizing dermatitis and fasciitis, with vasculitis and myositis (Figures 79-1 and 79-2).204 Hematogenous seeding of vibrios to secondary cutaneous lesions is probable. Primary wound infections (approximately 30% of cases) rapidly show marked edema, with erythema, vesicles, and hemorrhagic or contused-appearing bullae, progressing to necrosis. This may require radical surgical debridement or amputation. Up to 25% of these victims may have sepsis. When V. vulnificus is recovered from the blood of a victim with sepsis attributable to a wound infection, the case fatality rate may exceed 30%.80 Extracellular elastin-lysing proteases elaborated by the organism, as well as a potent collagenase, probably contribute to the rapid invasion of healthy tissue. V. vulnificus also produces a cytotoxin-hemolysin and phospholipases. Cytolysin produced by most pathogenic strains of V. vulnificus is extremely toxic to mice when injected IV and results in severe perivascular edema and neutrophil infiltration in lung tissues.89,135 The precise roles of these and other factors (pili, mucinase, chondroitinase, hyaluronidase) in the in vivo pathogenicity of the organism have yet to be determined. Bleeding complications (which may include gastrointestinal hemorrhage and disseminated intravascular coagulation) are common and may be attributed in part to thrombocytopenia. Gastroenteritis is more common (15% to 20%) with the septicemic presentation than with primary wound infection and may exist as an isolated entity (approximately 10% of cases), although it is debated that illness has been erroneously attributed to the asymptomatically carried organism. Vibrio vulnificus endometritis has been reported after an episode of intercourse in the waters of Galveston Bay, Texas.178 Other presentations of V. vulnificus infections have included meningitis, necrotizing fasciitis following lightning strike in a windsurfer, spontaneous bacterial peritonitis, corneal ulcers, epiglottitis, and infections of the testes, spleen, and heart valves.185
FIGURE 79-1 Ecthyma gangrenosum associated with Vibrio vulnificus sepsis.
(Courtesy Edward J. Bottone, MD, Department of Microbiology, Mt Sinai Hospital, NY.)
The explosive nature of the syndrome can lead to gram-negative sepsis and death, reportedly in up to 50% of cases. The mortality rate may be as high as 90% in victims who become hypotensive within 12 hours of initial examination by a physician. For wound infections from all Vibrio species, the organism may only be recovered from blood specimens in less than 20% of victims.80 Appropriate antibiotics should be administered as soon as the infection is suspected (see later). In one report, V. vulnificus sepsis was treated with antibiotic therapy, debridement of necrotic tissues, and direct hemoperfusion using polymyxin B immobilized fiber, which served as an artificial reticuloendothelial system and removed endotoxin from the circulating blood.153 In an immunocompetent victim who acquired a V. vulnificus hand infection from peeling shrimp, treatment with oral ciprofloxacin was successful. In a series of seven patients treated for primary skin and soft tissue infections secondary to V. vulnificus, prompt operative exploration and debridement were correlated with a decrease in the intensive care unit and hospital length of stay, particularly if the surgery occurred within 72 hours from the time of infection.77 The authors noted that all patients had necrosis of underlying subcutaneous tissue, whereas some did not demonstrate skin necrosis.
Vibrio mimicus is a motile, nonhalophilic, gram-negative, oxidase-positive rod with a single flagellum. It can be distinguished from V. cholerae by its inability to ferment sucrose, inability to metabolize acetylmethyl carbonyl, sensitivity to polymyxin, and negative lipase test. An ear infection may follow exposure to ocean water. Isolates are sensitive to tetracycline. Physicians who collect stool samples for culture to identify suspected V. mimicus must alert the laboratory to use appropriate culture media (thiosulfate–citrate–bile salts–sucrose [TCBS] agar).
Vibrio alginolyticus, found in seawater, has been implicated in soft tissue infections (e.g., those caused by coral cuts or surfing scrapes), sinusitis, and otitis, particularly after previous ear infections or a tympanic membrane perforation. Although bacteremia has been reported in immunosuppressed patients and patients with burns, V. alginolyticus does not generally carry the virulent potential of V. vulnificus.119 Typical symptoms include cellulitis, with seropurulent exudate. Its distinguishing microbiologic features are stated to be sucrose and lactose fermentation, growth in 1% tryptone broth plus 10% NaCL, positive Voges–Proskauer reaction, negative urease reaction, and susceptibility to vibriostatic compound O/129. However, because these indices may vary, identification may be difficult. Antibiotic resistance may be a feature of V. alginolyticus infection.
Photobacterium (formerly Vibrio or Listonella) damsela, formerly enteric group EF-5 and so-named because it is pathogenic for the damselfish, causes wound infections similar to those attributed to vibrios. Rapidly progressive infection leading to muscle necrosis and fasciitis or to sepsis and death may transpire in an immunosuppressed victim or person with normal immunity.66,68,175 This may be related to an extracellular cytolysin (damselysin) or other unidentified enzymes or virulence factors.
Vibrio cholerae is associated with severe gastroenteritis (see Chapter 68). With regard to tissue infection, a case of necrotizing fasciitis and septic shock caused by V. cholerae non-O1 (not agglutinated in cholera polyvalent O1 antiserum) acquired in San Diego, California, has been described.192 The victim suffered from preexisting diabetes mellitus complicated by chronic plantar ulceration of the affected limb. V. cholerae may cause severe disease signs in Japanese sweetfish (ko-ayu or Plecoglossus altivelis), certain shrimp (e.g., Penaeus monodon), and ornamental fish in India.13,76,171
Growth in Culture
Although plating on standard clinical laboratory media may detect only 0.1% to 1% of the total number of microorganisms found in seawater or marine sediment, most marine bacteria that are pathogenic to humans can be readily recovered on standard media. Although pathogenic Vibrio species can grow on conventional blood agar media, other marine bacteria may require saline-supplemented media and incubation at 25° C (77° F) instead of the standard 35° to 37° C (95° to 98.6° F). In culture, marine bacteria may grow at a slower rate than terrestrial bacteria, which delays identification. Pleomorphism in culture may be attributed to adaptation to small concentrations of nutrients in seawater. Most organisms require sodium, potassium, magnesium, phosphate, and sulfate for growth; a few require calcium or chloride.
All Vibrio species grow in routine blood culture mediums and on nonselective mediums, such as blood agar. TCBS agar is selective and recommended for the detection of marine Vibrio organisms, although cellobiose–polymyxin B–colistin (CPC) agar may be as good or better.20,111 An alternative is Monsur taurocholate–tellurite–gelatin agar. A large clinical laboratory near the ocean might consider the use of TCBS or CPC agar routinely. Pathogenic vibrios generally grow on MacConkey agar. All species except V. cholerae and V. mimicus require sodium chloride for growth. Enrichment broth (alkaline peptone water with 1% NaCl) is recommended for isolation of vibrios from convalescent and treated patients. Another enrichment broth that may be more effective is 5% peptone, 1% NaCl, and 0.08% cellobiose (PNC) at pH 8.0.84 A comparison of strategies for the detection and recovery of V. vulnificus from marine samples of the western Mediterranean coast determined that the best strategy consisted of the combination of culture-based methods (3-hour enrichment in alkaline-saline peptone water at 40° C [104° F], followed by culture on CPC agar) and DNA-based procedures (specific PCR amplification of the presumptive colonies with primers Dvu 9V and Dvu 45R).6
Key characteristics that aid in the separation of Vibrio species from other medically significant bacteria (Enterobacteriaceae, Pseudomonas, Aeromonas, Plesiomonas) are motility by polar flagella, the production of oxidase, fermentative metabolism, requirement of sodium chloride for growth, and susceptibility to the O/129 vibriostatic compound. V. vulnificus can be cultured from the blood, wounds (bullae), and stool. The laboratory must be cautioned to use selective culture media with a high salt content (3% NaCl) for prompt identification. Suggestive features include positive fermentation of glucose, positive catalase and oxidase tests, positive indole test, positive reaction for both lysine and ornithine decarboxylase, positive o-nitrophenyl-β-D-galactopyranoside, and inability to ferment sucrose. A useful identification scheme for pathogenic Vibrio species is found in the chapter on Vibrio in the most recent edition of the American Society for Microbiology’s Manual of Clinical Microbiology.
Because growth of V. vulnificus in culture generally requires 48 hours, current research is directed at a more rapid diagnostic test. Direct identification of V. vulnificus in clinical specimens by nested PCR has been accomplished using serum specimens and bulla aspirates from septicemic patients.107 A nested PCR method for rapid and sensitive detection of V. vulnificus in fish, sediments, and water has been developed.7 Simultaneous detection of five marine fish pathogens (V. vulnificus, Listonella anguillarum, Photobacterium damsela, Aeromonas salmonicida, and V. parahaemolyticus) has been accomplished by using multiplex PCR and a DNA microarray.67 This technique has not yet been applied to diagnosis of pathogens afflicting humans.
Mycobacteria must be cultured in media such as Middlebrook 7H10 or 7H11 agar or Lowenstein–Jensen medium; fungi require a medium such as Sabouraud dextrose or brain–heart infusion/Sabhi agar. Antibiotic susceptibility testing can be performed using established procedures, except for the addition of NaCl 2.3% to the Mueller–Hinton broth or agar used for disk diffusion. Certain commercial test kits may not accurately identify marine organisms. In the setting of wound infection or sepsis, the clinician should alert the laboratory that a marine-acquired organism may be present. If a laboratory does not have the time or resources to perform a complete identification, the bacteria may be sent to a reference laboratory. Marine bacteria are kept in the American Type Culture Collection. Because of the diversity of species, complete agreement has not yet been reached on comprehensive taxonomic criteria for identification.
The objectives for the management of infections from marine microorganisms are to recognize the clinical condition, culture the organism, and provide antimicrobial therapy. Management of marine-acquired infections should include therapy against Vibrio species. Antibiotic selection should be guided by the most current recommendations. Historically, third-generation cephalosporins (cefoperazone, cefotaxime, or ceftazidime) provide variable coverage in vitro; first- and second-generation products (cefazolin, cephalothin, cephapirin, cefamandole, cefonicid, ceforanide, or cefoxitin) appear to be less effective in vitro. The organism has been reported in some cases to be resistant in vitro to third-generation cephalosporins, mezlocillin, aztreonam, and piperacillin.139 A combination of cefotaxime and minocycline seems to be synergistic and extremely effective against V. vulnificus in vitro.53 Oral cultures taken from two captive moray eels at the John G. Shedd Aquarium in Chicago, Illinois, demonstrated V. fluvialis, Photobacterium damsela, V. vulnificus, and Pseudomonas putrefaciens sensitive to cefuroxime, ciprofloxacin, tetracycline, and trimethoprim–sulfamethoxazole.63 Imipenem–cilastatin is generally efficacious against gram-negative marine bacteria, as are trimethoprim–sulfamethoxazole and tetracycline. Gentamicin, tobramycin, and chloramphenicol have tested favorably against P. putrefaciens and Vibrio strains. Nonfermentative bacteria (such as Alteromonas, Pseudomonas, and Deleya species) appear to be sensitive to most antibiotics. In a mouse model, combination therapy with minocycline and cefotaxime was more effective than either drug alone.52
Quantitative wound culture has no advantage before the appearance of a wound infection. Pending a prospective evaluation of prophylactic antibiotics in the management of marine wounds, the following recommendations are based on the indolent nature and malignant potential of soft tissue infections caused by Vibrio species:
If the victim is managed as an outpatient, the drugs of choice to cover Vibrio are ciprofloxacin, trimethoprim–sulfamethoxazole, or tetracycline. Cefuroxime is an alternative. It is a clinical decision whether oral therapy should be preceded by a single IV or intramuscular (IM) loading dose of a similar or different antibiotic, commonly an aminoglycoside.
If sepsis is severe, additional aggressive measures beyond surgery and antibiotics, such as administration of recombinant human activated protein C, may be required.4 Hyperbaric oxygen therapy has been used as adjunctive therapy in V. vulnificus septicemia and cellulitis, but there is no standard recommendation for this modality for this indication.193
Diversity of Organisms
The natural freshwater environment of ponds, lakes, streams, rivers, lagoons, harbors, estuaries, and artificial bodies of water is probably as hazardous as the ocean from a microbiologic standpoint. Waterskiing accidents, propeller wounds, fishhook punctures, lacerations from broken glass and sharp rocks, fish fin or catfish stings, and crush injuries during white-water expeditions are commonplace. A large number of bacteria have been identified in water, sediments, animals, and wounds. In fringe areas of the ocean that carry brackish water (NaCl content <3%), marine bacteria, salt-tolerant freshwater bacteria, and brackish-specific bacteria, such as Agrobacterium sanguineum, are noted. The combined effects of human and animal traffic and waste disposal increase the risk for coliform contamination. In Great Britain, antibiotic-resistant Escherichia coli have been documented in rivers and coastal waters.161 Coxsackievirus A16 has been isolated from children stricken ill after bathing in contaminated lake water.58 Of particular note is the presence of virulent species, such as Chromobacterium violaceum, V. parahaemolyticus, and A. hydrophila, associated with serious and indolent wound infections.191 The last can be cultured from natural bodies of water, as well as from the mouths of domesticated aquarium fish, such as the piranha.148 Biologic control agents, such as guppy fish bred in wells to control mosquito proliferation, can carry bacterial pathogens such as Pseudomonas.46
One investigation sampled water, inanimate objects, and animals from freshwater environments in California, Tennessee, and Florida.10 Bacteria isolated were predominantly gram-negative and included A. hydrophila, Flavobacterium breve, Pseudomonas species, V. parahaemolyticus, Serratia species, Enterobacter species, Plesiomonas shigelloides, Bacillus species, Acinetobacter calcoaceticus, and Alcaligenes denitrificans.
Primary amebic meningoencephalitis is caused by infection with Naegleria fowleri, a thermophilic, free-living ameba found in freshwater environments. The infection is associated with human activities that allow entry of water into the nose, from where the ameba migrate to the brain via the olfactory nerve.
Wound Infections Caused by Aeromonas Species
Aeromonas hydrophila (Latin for “gas producing” and “water loving”) is a gram-negative, facultatively anaerobic, polarly flagellated, non–spore-forming, and motile rod member of the family Vibrionaceae that commonly inhabits soil, freshwater streams, and lakes.3,14,103,188 Aeromonas species are widely distributed and found at wide ranges of temperature and pH. Five species (A. hydrophila, A. sobria, A. schubertii, A. veronii, and A. caviae) of the 9 that have been recovered from clinical material have been linked with human disease; there are 13 or more distinct genotypes.1 A. hydrophila is pathogenic to amphibians, reptiles, and fish. Soft tissue and gastroenteric infections predominate in humans. Virulence factors elaborated by Aeromonas species include hemolysin, cytotoxin, enterotoxin, cholera toxin–like factor, and hemagglutinins.27,187 Aeromonas species are sometimes misidentified as members of the genus Vibrio by commonly used screening tests.1
A wound, particularly of the puncture variety, immersed in contaminated water may become cellulitic within 24 hours, with erythema, edema, and a purulent discharge.156,201 The lower extremity is most frequently involved. This usually occurs from stepping on a foreign object or being punctured underwater. The appearance may be indistinguishable from a typical streptococcal cellulitis, with localized pain, lymphangitis, fever, and chills. Untreated or managed with antibiotics to which the organism is not susceptible, this may rarely progress to a severe gas-forming soft tissue reaction, bulla formation, necrotizing myositis, or osteomyelitis. Appearance similar to ecthyma gangrenosum caused by Pseudomonas aeruginosa has been reported in Aeromonas septicemia.
Fever, hypotension, jaundice, and chills are common manifestations of septicemia.96 Additional clinical manifestations include abdominal pain or tenderness, altered consciousness, acute renal failure, bacteremic pneumonia, and coagulopathy.90 In a manner analogous to the pathogenicity of virulent Vibrio species, the chronically ill or immunocompromised host (e.g., chronic liver disease, neoplasm, diabetes, uremia, corticosteroid therapy, extensive burns) is probably at greater risk of a severe infection or complication, such as meningitis, endocarditis, or septicemia. Freshwater aspiration may result in A. hydrophila pneumonitis and bacteremia. Infection has followed the bite of an alligator. A 15-year-old boy suffered an A. hydrophila wound infection after a bite from his pet piranha. For unknown reasons, there is a marked preponderance of male victims. This may represent the phenotypic variation of critical bacterial adhesins or may simply reflect activity patterns of male humans. Corneal ulcer caused by A. sobria was reported after abrasion by a freshwater reed.44
Because of the microbiologic similarity of Aeromonas on biochemical testing to members of the Enterobacteriaceae family, such as E. coli or Serratia species, it is important to alert the laboratory to the clinical setting. In the microbiology laboratory, Aeromonas species may be identified on the basis of positive oxidase reaction, no growth on TCBS agar, growth on MacConkey agar, and resistance to the vibriostatic compound O/129.96
Gram’s stain of the purulent discharge may demonstrate gram-negative bacilli, singly, paired, or in short chains. Given the appropriate clinical setting (after a wound acquired in the freshwater environment), this should not be casually attributed to contamination.89 A. hydrophila is generally sensitive to chloramphenicol, aztreonam, gentamicin, amikacin, tobramycin, trimethoprim–sulfamethoxazole, cefotaxime, cefuroxime, moxalactam, imipenem, ceftazidime, ciprofloxacin, and norfloxacin. In one case, culture of a severe wound infection demonstrated the presence of two species, A. hydrophila and A. sobria. Notably, the latter was resistant to tetracycline in vitro. For a severe infection, initial therapy that includes an aminoglycoside provides coverage against concomitant Pseudomonas or Serratia infection. As has been demonstrated with Vibrio species, the first-generation cephalosporins, penicillin, ampicillin, and ampicillin-sulbactam are not efficacious, perhaps because of the production of a β-lactamase by the organism. Aeromonas species are capable of producing chromosomally encoded β-lactamases induced by β-lactam antibiotics. This leads to resistance to penicillins, cephalosporins, and monobactams. The β-lactamase inhibitors, such as clavulanate, are not effective against these β-lactamases, so that amoxicillin-clavulanate may not kill Aeromonas.136 The optimal therapy for invasive infections caused by cefotaxime-resistant A. hydrophila is not known, but a recent study of in vitro and in vivo (mice) activities of fluoroquinolones suggest that ciprofloxacin may be as effective as cefotaxime–minocycline.95 In this study, ciprofloxacin and levofloxacin showed greater activity than did gatifloxacin, moxifloxacin, and lomefloxacin.
Initial therapy of a severe soft tissue infection related to Aeromonas should include aggressive wound debridement to mitigate the potentially invasive nature of the organism. In one case of severe cellulitis unresponsive to debridement, fasciotomy, and antibiotic therapy, treatment with hyperbaric oxygen was felt to contribute to successful infection control.118
Curiously, medicinal leeches can harbor Aeromonas in their gut flora; soft tissue infections related to this phenomenon have been reported.165 The genus Plesiomonas also belongs to the family Vibrionaceae; it has been definitively linked with aquarium-associated infection complicated by watery diarrhea and fever.
Infections Caused by a Fish Pathogen, Streptococcus iniae
Streptococcus iniae is a pathogen of fish, noted to cause subcutaneous abscesses in Amazon freshwater dolphins (Mammalia: Inia geoffrensis) kept in captivity.197 Epizootic fatal meningoencephalitis in fish species caused by streptococci has been observed in outbreaks affecting tilapia, yellowtail, rainbow trout, and coho salmon. S. iniae has emerged as a serious pathogen of farmed barramundi in Australia.29 Persons who handle these fish are at risk for bacteremic illness, which can manifest as cellulitis or sepsis. Endocarditis, meningitis, and arthritis have been noted to accompany S. iniae infection.
The tilapia (Oreochromis and Tilapia species) are also known as St. Peter’s fish or Hawaiian sunfish. The surfaces of these commonly aquacultured fishes may be colonized with S. iniae. Persons of Asian descent have been identified as prone to infection, probably because they often prepare this fish with the intent to dine. Typically, the victim recalls puncturing the skin of the hand with a fin, bone, or implement of preparation. Cellulitis with lymphangitis and fever is common, without skin necrosis or bulla formation.197
In culture, S. iniae shows β-hemolysis. However, it may appear to be α-hemolytic because the narrow zone of β-hemolysis is ringed by more prominent zone of α-hemolysis. Therefore, it may be misidentified as a viridans streptococcus and thus considered a contaminant. A reasonable approach to antibiotic therapy includes penicillin, cefazolin, ceftriaxone, erythromycin, clindamycin, or trimethoprim–sulfamethoxazole. In one series, ciprofloxacin showed slightly less efficacy in vitro.
A General Approach to Antibiotic Therapy
Management of freshwater-acquired infections should include therapy against Aeromonas species. First-generation cephalosporins provide inadequate coverage against growth of freshwater bacteria. Third-generation cephalosporins provide excellent coverage, whereas second-generation products are less effective. Ceftriaxone may not be efficacious against Aeromonas species. Ciprofloxacin, imipenem, ceftazidime, gentamicin, and trimethoprim–sulfamethoxazole are reasonable antibiotics against gram-negative microorganisms. Trimethoprim or ampicillin alone may be inefficacious.
Whether to begin antimicrobial therapy before establishment of a wound infection is controversial. Pending a prospective evaluation of prophylactic antibiotics in freshwater-acquired wounds, the following recommendations are based on the potentially serious nature of soft tissue infections caused by Aeromonas species:
Myth and folklore surround sharks, the most feared of sea creatures. Although dreaded, sharks are among the most graceful and magnificent denizens of the deep. Sharks may be found in all seas but the Southern Ocean and occur in some tropical rivers and riverine lakes. Sharks range in size from the small spined pygmy shark Squaliolus laticaudus (10 to 15 cm [3.9 to 5.9 inches]) and dwarf dogshark Etmopterus perryi (15.4 cm [6 inches]) to the whale shark Rhincodon typus (more than 18 m [59 feet] and 22,700 kg [50,000 lb]), a plankton feeder (Figure 79-3, online).
Attacks by these occasionally savage animals have always held enormous fascination for scientists, adventurers, and clinicians. The problem was highlighted for the U.S. military in 1945 during World War II when crew members from the USS Indianapolis perished in shark-infested waters. On July 30, the heavy cruiser was sunk by a Japanese torpedo, resulting in hundreds of deaths plus reports of an estimated additional 60 to 80 shark attack fatalities of survivors left adrift for 5 days. This estimate is certainly a high figure inflated by historic misinterpretation of scavenge bites on already dead servicemen and some exaggeration, but nevertheless, the approximately two dozen bites on live survivors involved in this tragedy represents the largest reported incidence of mass shark attacks (GHB interviews with survivors).
The bull shark Carcharhinus leucas (Figure 79-4) is a frequent visitor and occasional resident of tropical and warm-temperate rivers. It commonly penetrates 161 km (100 miles) or more up freshwater rivers, such as the Ganges, Nile, and Zambezi and has been recorded from the Amazon River at Iquitos, Peru, 4000 km from the Atlantic Ocean, and as far inland as Illinois in the Mississippi River.130,177 These sharks also live in Lake Nicaragua and have had their aggressive behavior attributed in part to high levels of testosterone. During the summer of 2001, the “summer of the shark” in the U.S. media, a bull shark was believed to have attacked an 8-year-old child off the Gulf Coast of Florida.
The International Shark Attack File (ISAF) has its origin from the Shark Research Panel created by the Office of Naval Research (ONR) in 1958. The File was initiated by Perry W. Gilbert and Leonard P. Schultz in 1958 for the Smithsonian Institution, American Institute of Biological Sciences, Cornell University, and the ONR. In 1967, the data were sent to Mote Marine Laboratory in Sarasota, Florida, where H. David Baldridge analyzed 1165 reported attacks and case histories and prepared a special technical report, Shark Attack Against Man, for the U.S. Navy Bureau of Medicine and Surgery in 1973. After a period of maintenance at the National Underwater Accident Data Center at the University of Rhode Island, in 1988 the Shark Attack File moved to the University of Florida at Gainesville, where it is maintained by the International Elasmobranch Society and the Florida Museum of Natural History under the direction of George H. Burgess.35 It remains an authoritative collection of analyzed data, containing a series of more than 4000 individual investigations from the mid-1500s to the present. Other regional scientific records of shark attacks are maintained by the California Department of Fish and Game, the Natal Sharks Board (South Africa), Taronga Zoo (Australia), University of Sao Pãulo (Brazil), and Department of Land and Natural Resources (Hawaii). All of these organizations serve as cooperators with ISAF, feeding results of regional investigations into the ISAF database. Hundreds of cooperating scientific observers located throughout the world act in a similar capacity, ensuring broad international coverage.
The world’s shark populations are in danger from overfishing, particularly in light of their slow growth rate, late sexual maturation, relatively lengthy gestation periods, and low number of offspring. Each year, more than 100 million elasmobranchs (sharks, skates, and rays), including 1.6 million metric tons, or approximately 3.5 billion lb of shark, or 10 million elasmobranchs for each human shark-related fatality, are killed in fisheries. One-half of this total represents incidental by-catch (nontargeted captures in fishing nets or on longlines fishing for other species).23 The National Marine Fisheries Service estimates that 20 million metric tons of marine wildlife are killed and thrown back into the sea as by-catch. (Figure 79-5, online) This activity may double the estimated shark mortality figures. Commercial fishing mortality of sharks in U.S. waters averages 20,000 metric tons (44,092,000 lb) per year. Great declines in shark populations along the eastern coast of the United States have occurred over the past two decades, a trend that is worldwide. Some commercially targeted species have declined by as much as 80%. The most dramatic declines were seen in dusky sharks. Innumerable animals are ground into fertilizer. More than 90% of captured sharks are discarded.
The fishery interest in sharks centers on the fins, including those of the blue, hammerhead (Figures 79-6 and 79-7, online), silky (Figure 79-8), mako, and thresher sharks. These are of great value in the Orient, where they are made into shark fin soup, a traditional dish that signifies high economic status and is reputed to be an aphrodisiac. Interest in fins has also spawned the heinous and wasteful practice of finning, in which a shark is captured, its fins are sliced off (Figure 79-9), and then it is returned to the water (Figure 79-10).115 Shark-fin soup, which dates back from the Chinese Sung Dynasty in 960 AD, is sold for upward of $150 per bowl. The prepared fins themselves may sell for more than $800 per pound. It has been estimated that 350 tons of shark fins may be consumed each year. The International Commission for the Conservation of Atlantic Tunas created a ban on shark finning in November 2004, to join the United States, which banned shark finning in the Atlantic Ocean in 1993 and in the Pacific Ocean in 2002, in such a prohibition. Shark flesh is a major food source in both developed (commonly the fish in European “fish and chips”) and undeveloped (artisinal fisheries) countries. Mako shark flesh is similar to that of swordfish and often serves as a more than adequate culinary substitute. To date, sharks do not routinely appear to carry ciguatera toxin, except in the liver; however, serious poisoning from shark ingestion has been reported28 (see Chapter 72).
In Tahiti and some other Polynesian locations, sharks are occasionally mercilessly killed simply to acquire their teeth for jewelry manufacture. The great white shark has been declared a protected species in South Africa, Australia, the Maldives, California, and the Atlantic waters of the United States. In 1991, the South African government declared the great white shark (Figures 79-11 to 79-13, online) a protected species within 322 km (200 miles) of its coast. The U.S. government has lowered allowable fishing quotas in Atlantic waters, and Australia closely monitors its shark fisheries. In October 2004, a global wildlife treaty by the Convention on International Trade in Endangered Species (CITES) offered new protection to great white sharks. In other areas, however, sharks and their relatives are largely unregulated and populations are in serious decline. Some species, especially those that enter rivers, are potentially at risk of extinction.
Of note is the failure of designation of “no-take” areas within marine coral reef ecosystems to demonstrably diminish the depletion of reef shark species, such as the whitetip reef shark and gray reef shark (Figure 79-14, online) in Australia, as opposed to no-entry zones. The latter are aerially surveyed and strictly enforced exclusion areas. Anything less appears to allow widespread predation by humans upon sharks.151 Poaching and underreporting of catches are rampant.
Life and Habits
Sharks (from xoc, pronounced “shock,” a Yucatee word from the Mayan language and a glyph for “fish”) have inhabited the oceans for at least 400 million years.24 They appeared on the planet during the Devonian period, approximately 200 million years before the dinosaurs. Indeed, many living species of sharks belong to the same genera as species from the Cretaceous period, one hundred million years ago.167 Ancestral sharks may have been enormous; Carcharocles megalodon, which roamed the seas between 20 million and 1.5 million years ago, probably grew to a length of more than 15 m (49 feet), with teeth longer than 15.2 cm (6 inches). This was a predator of astronomic proportions that apparently largely fed on whales.
Shark attack is perhaps first depicted on a vase dated circa 725 BC from the Island of Ischia west of modern day Naples, and it is recorded in early Greek literature. Some 35 of about 375 species of sharks have been implicated in the 75 to 100 shark attacks on humans that are estimated to occur annually worldwide (on-average, 65 attacks per year were recorded by the ISAF in the first decade of the 21st century), and another 35 to 40 species are considered potentially dangerous. It is often commented that shark attacks may be underestimated, largely because of failure to report.179 Even if this is the case, it is unlikely that a completely accurate estimation would change the epidemiologic significance, compared with other causes of water-related deaths.
U.S. coastal waters typically are the setting for one-third or more of the annual number of shark attacks. The great American colonial painter John Singleton Copley’s 1778 painting Watson and the Shark (Figure 79-15), which depicts an encounter between the Englishman Brook Watson (1735 to 1807) and a shark that bit off his right foot in Havana Harbor in 1749, is one of the earliest authenticated records of a shark attack.24 ISAF has records of attacks going back into the mid-1500s. Less than 10 deaths from shark attacks are reported worldwide each year; ISAF data document an average of five deaths per year during the past decade. In 2003, it was noted that reported unprovoked shark attacks worldwide had declined for 3 straight years, dropping from 79 in 2000 to 63 in 2002 to 55 in 2003, with a similar decline in overall mortality from 13% in the 1990s to 7% in 2003.165
FIGURE 79-15 Watson and the Shark, by John Singleton Copley, 1778.
(Copyright 2005 Museum of Fine Arts, Boston.)
The most frequently documented offenders are three larger animals: the great white (Figure 79-16), bull, and tiger (Galeocerdo cuvieri) (Figure 79-17, online) sharks. All three reach large sizes, routinely seek larger prey items, and have broadly serrated teeth that facilitate shearing. Bull sharks are perhaps the species of greatest concern owing to their habitat preference (inshore waters, including estuaries and rivers, which places them close to human activity) and tenacious mode of attack. The species is certainly underrepresented in attribution statistics because its distributional range overlaps those of many species similar in appearance. An outbreak of shark attacks off Pernambuco, Brazil, largely involved this species.79 However, blacktip (Carcharhinus limbatus) and possibly spinner (Carcharhinus brevipinna) sharks, which are thought to be involved in most of Florida’s numerous (15 to 20 per year) minor bites, may be involved in even more incidents.35 Identification of attacking species is a difficult task because victims seldom see the attacker well enough to make an accurate identification and because identification of most shark species, especially requiem sharks of the family Carcharhinidae, is notoriously difficult, even for trained scientists. Definitive identification can be made by examining tooth fragments left behind in a wound, but this is an infrequent occurrence. Thus, easily identified species such as white, tiger, bull, and nurse sharks sit high on documented attacker lists, whereas most requiem shark incidents are grossly underreported. Less commonly reported attackers include the sand tiger (ragged tooth or grey nurse) (Figure 79-18), blue (Figure 79-19), blacktip reef (Figure 79-20), bronze whaler, lemon (Figures 79-21 to 79-23; Figures 79-22 and 79-23, online), shortfin mako (Figures 79-24 and 79-25; Figure 79-25, online), grey reef (Figure 79-26), oceanic whitetip (Figures 79-27 and 79-28; Figure 79-28, online), sandbar, sevengill, Caribbean reef, and dusky sharks (ISAF data). Hammerhead (Figure 79-29), Galápagos, and nurse (Figures 79-30 to 79-32; Figures 79-31 and 79-32, online) shark attacks are rarely reported. The famous series of attacks along the New Jersey shore in the summer of 1916 are thought to be attributable to a single great white shark. Tiger sharks are the most commonly identified attackers in the Hawaiian Islands and other tropical regions. Most attacks are reported from North America, with Florida (and its central east coast) leading the list. A “leveling off” of annual shark attack numbers during the past decade suggests that it is possible that people are becoming a bit more intelligent about when and where they enter the water.
FIGURE 79-16 Great white shark (Carcharodon carcharias). The most dangerous of sharks, this animal has been implicated in many attacks on humans.
(Courtesy Howard Hall.)