Envenomation by Aquatic Vertebrates

Chapter 81 Envenomation by Aquatic Vertebrates



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See Chapter 79 for a discussion of infections associated with aquatic wounds and the relevant antimicrobial therapy. An analysis that compared DNA sequences from 233 fish species was used to create a family tree for spiny-rayed fishes. This indicates that previous estimates of approximately 200 venomous fishes should be revised to suspect at least 1200 fishes in 12 clades (a group of biologic taxa or species that share features inherited from a common ancestor) as perhaps venomous.93


A common clinical question is how best to image embedded spines, such as those from stingrays, scorpionfishes, sea urchins, etc. Some prove to be radiopaque and some are not. One limited study evaluated intraarticular foreign bodies using sea urchin spines and chicken thigh-leg combinations.59 Pending further evidence, computed tomography (CT) and magnetic resonance imaging (MRI) appear to be more reliable modalities than plain radiography, ultrasonography, or fluoroscopy. However, for reasons of limiting radiation exposure or expense, one of the latter three may be chosen as the initial imaging technique.



Stingrays


Stingrays are the most commonly incriminated group of fish involved in human envenomations. They have been recognized as venomous since ancient times, known as “demons of the deep” and “devil fish.” Aristotle (384 to 322 BC) made reference to their stinging ability. Stingray spines were used in certain Maya bloodletting procedures and rituals.54


Stingrays are members of the class Chondrichthyes (cartilaginous fish), subclass Elasmobranchii (plates and gills; with sharks and chimaeras), order Rajiformes (which contains stingrays [Dasyatidae], guitarfish [Rhinobatidae], skates [Rajidae], electric rays [Torpedinidae], eagle rays [Myliobatidae], mantas [Mobulidae], and freshwater rays [Potamotrygonidae]). Twenty-two species of stingrays are found in U.S. coastal waters, 14 in the Atlantic and 8 in the Pacific. The family Dasyatidae includes most of the species that cause human envenomation. Skates are harmless. It is likely that at least 2000 stingray injuries take place each year in the United States. On the west coast of the United States, the round stingray (Urolophus [or Urobatis] halleri) is a frequent stinger; along the southeastern coast, it is the southern stingray (Dasyatis americana). Most attacks occur during the summer and autumn months, as vacationers venture into the surf that may be laden with congregating (for spawning purposes) rays. Freshwater species do not inhabit U.S. waters. They are found in South America, Africa, and Southeast Asia. Skates are related to rays and look similar, but do not carry a sting, so are harmless to humans.



Life and Habits


Stingrays are cartilagenous fish that are usually found in tropical, subtropical, and warm temperate oceans, generally in shallow (intertidal) water areas, such as sheltered bays (Figure 81-1, online), shoal lagoons, river mouths, and sandy areas between patch reefs (Figure 81-2, online).72 Although rays are generally found above moderate depths, at least one deep-sea species has been discovered. Rays can enter brackish and fresh waters as well. For instance, freshwater stingrays are common in rivers and tributaries in South America (Figure 81-3, online).51





Rays are small (several inches) to large (up to 4 m × 2 m [12 feet × 6 feet]) creatures observed lying on top of the sand and mud or partially submerged, with only the dorsally placed eyes and spiracles and part of the tail exposed (Figure 81-4). Their dorsoventrally flattened bodies are round-, diamond-, or kite-shaped, with wide pectoral fins that look like wings (Figure 81-5). The large fleshy cephalic lobes that appear to extend from the front of the head in manta rays are continuations of modified and enlarged pectoral fins. Rays are nonaggressive scavengers and bottom feeders that burrow into the sand or mud to feed on worms, mollusks, and crustaceans. The mouth and gill plates are located on the ventral surface of the animal (Figure 81-6). The flattened shape is largely configured by the modified pectoral fins, or “wings,” of the animal. These wings ripple or flap to propel the animal through the water (Figure 81-7, online).







Venom and Venom Apparatus


The venom organ of stingrays consists of one to four venomous stings on the dorsum of an elongate, whiplike caudal appendage. Anatomic types of stingray venom organs, and thus stinging ability, are differentiated into four groups based on their adaptability as a defense organ (Figure 81-8): (1) the gymnurid type (butterfly rays, or Gymnuridae), with a poorly developed sting of up to 2.5 cm (1 inch) placed at the base of a short tail; (2) the myliobatid type (eagle and bat rays, or Myliobatidae), with a sting of up to 12 cm (4.7 inches) placed at the base of a cylindric caudal appendage that terminates in a long whiplike tail; (3) the dasyatid type (stingrays and whip rays, or Dasyatidae), with a sting of up to 37 cm (14.5 inches) placed at the base or further out on the caudal appendage that terminates in a long whiplike tail; and (4) the urolophid type (round stingrays, or Urolophidae), with a sting of up to 4 cm (1.5 inches) located at the base of a short, muscular, well-developed caudal appendage. The efficiency of the apparatus is related to the length and musculature of the tail and to the location and length of the sting. Eagle rays and some mantas (Atlantic Mobula mobular and Pacific Mobula japanica) have a stinging apparatus, but it is less of a threat because the spine is located at the base of the tail and is not well adapted as a striking organ. Although the Pacific manta (Manta birostris) may grow to a width (“wingspan”) of 6 m (20 feet) and weight of 1800 kg (4000 lb), it dines on small fish, crustaceans, and microorganisms (Figures 81-9 to 81-11; Figures 81-10 and 81-11, online). There is some DNA evidence and a prevailing opinion that all mantas may be of the same species (Manta birostrisi), which will in time render other Latin names and some common names obsolete. Many divers have “hitched” a ride on the wings of a manta; there are no reports of envenomation. However, manta skin is rough and can abrade unprotected human skin. A stingray “hickey” is a mouth-bite created by powerful grinding plates that produces superficial erosions and ecchymosis in an oral pattern. People who hand-feed stingrays may incur this type of injury.36 The suction force generated by a stingray is sufficient to pull in a large amount of soft tissue, for example, from an obese thigh. This may result in a large and painful contusion or hematoma.






In all cases, the venom apparatus of stingrays consists of a bilaterally retroserrate spine or spines and the enveloping integumentary sheath or sheaths. The elongate and tapered vasodentine (modified dentin permeated by blood and capillaries) spine is firmly attached to the dorsum of the tail (whip) by dense collagenous tissue and is edged on either side by a series of sharp retrorse teeth. Along either edge on the underside of the spine are the two ventrolateral grooves, which house the soft venom glands. The entire spine is encased by the integumentary sheath, which also contains some glandular cells. The sting is often covered with a film of venom and mucus. The spine is replaced if detached.


The venom contains various toxic fractions, including serotonin, 5′-nucleotidase, and phosphodiesterase. Russell and others have investigated the pharmacologic properties of stingray venoms.32,86 In animal studies, they have demonstrated significant venom-induced peripheral vasoconstriction, bradycardia, tachycardia, atrioventricular block, ischemic Q and ST-T wave abnormalities, asystole, central respiratory depression, seizure activity, ataxia, coma, and death. The venom did not appear to be a paralytic neuromuscular agent. Research on stingray venom from the 1950s observed that heating the venom to a temperature above 50° C (122° F) diminished some biologic effects. Haddad analyzed proteins from freshwater stingray (Potamotrygon falkneri) venom using SDS-polyacrylamide gel electrophoresis and identified components with gelatinolytic, caseinolytic, and hyaluronidase activities.51 Others have identified hyaluronidase from the freshwater stingray Potamotrygon motoro.73 A novel bioactive peptide, Porflan, from the stingray Pomatotrygon gr. orbignyi induces leukocyte rolling and adherent cells and is proinflammatory in mice.28


Electric rays are discussed in Chapter 79.



Clinical Aspects


Stingray “attacks” are purely defensive gestures that occur when an unwary human wading in shallow waters handles, corners, or steps on a camouflaged creature (Figure 81-12). A frequently cited estimate of annual stingray injuries incurred in U.S. coastal waters is 750 to 1500, although there is no reliable reporting system for these injuries. Estimates are higher in tropical regions. The tail of the ray reflexively whips upward and accurately thrusts the caudal spine or spines into the victim, producing a puncture wound or jagged laceration (Figure 81-13). The integumentary sheath covering the spine is ruptured and venom is released into the wound, along with mucus, pieces of the sheath, and fragments of the spine. On occasion, the entire spine tip is broken off and remains in the wound (Figure 81-14).87 “Domesticated” stingrays, such as those that congregate at “Stingray City” in the waters of Grand Cayman Island (Figures 81-15 to 81-17; Figures 81-16 and 81-17, online), are habituated to the presence of humans and apparently pose less hazard for a spine puncture, but may still be induced to bite. It has been observed that there are hematologic differences between stingrays at tourist and nonvisited sites that reflect suboptimal stingray health in response to stress.90








A stingray wound from a spine puncture is both a traumatic injury and an envenomation. The former involves the physical damage caused by the sting itself. Because of the retrorse serrated teeth and powerful strikes, significant lacerations can result. Secondary bacterial infection is common. Osteomyelitis may occur if the bone is penetrated. Most injuries occur when the victim steps on a ray; another common cause is handling a ray during its extraction from a fishing net or hook.34 The lower extremities, particularly the ankle and foot, are involved most often, followed by the upper extremities, abdomen, and thorax. In a rare case, the heart may be directly injured.84 The tragic death in September 2006 of 44-year-old naturalist Stephen Irwin occurred at Batt Reef off the remote coast of northeastern Queensland, Australia, when he swam directly over a stingray that put a stingray spine into his chest. Death was attributed to a direct heart puncture. He was filming a documentary titled Ocean’s Deadliest. Fatalities have occurred after abdominal penetration and from exsanguination from the femoral artery. There have been reported cases of survival following cardiac injury, including one from the sting of a blue-spotted stingray (Dasyatis kuhlii) that leaped into the boat of a 75-year-old man.80 Pseudoaneurysm of the superficial femoral artery caused by stingray envenomation has been reported.18 One death has been attributed to tetanus complicating a leg wound. A spine partially or totally denuded of its sheath and venom glands may not cause an envenomation.37 A detached stingray spine may be used as a weapon. A man stabbed between the shoulder blades with stingray spine suffered a direct spinal cord injury at the level of T7-T8. He was extremely fortunate to make nearly a complete recovery after delayed operative removal.48


The envenomation classically causes immediate local intense pain, edema, and variable bleeding. The pain may radiate centrally, peaks at 30 to 60 minutes, and may last for up to 48 hours. The wound is initially dusky or cyanotic and rapidly progresses to erythema and hemorrhagic discoloration, with rapid fat and muscle hemorrhage and necrosis.11,60 Although the mechanisms causing pain, edema, and necrosis are not definitively determined, it is possible that the mucus covering the animal might contribute to the injury.70 If discoloration around the wound edge is not immediately apparent, within 2 hours it often extends several centimeters from the wound. Hemorrhagic blisters resembling a severe thermal burn or frostbite may occur and may be worsened by overzealous therapeutic hot water immersion.89,99 Minor stings may simulate bacterial cellulitis. Delayed healing seen following stingray injuries is usually attributed to direct venom toxicity and infections. One analysis of the tissue surrounding a necrotic center 96 hours after envenomation revealed a perivascular and interstitial mononuclear cell infiltrate with numerous eosinophils and rare neutrophils. The phenotype of the lymphoid population was predominately CD3+ T cells that coexpressed CD4+ and contained T cell–restricted intracellular antigen (TIA+) granules corresponding to the NK1.1 subpopulation of CD4+ T cells. Abundant eosinophils in the vicinity of a stingray soft tissue wound have been noted.83 All of this is indicative of an immunologic reaction, which, if present, might contribute to the delayed healing of stingray injuries.44


Systemic manifestations include weakness, nausea, vomiting, diarrhea, diaphoresis, vertigo, tachycardia, headache, syncope, seizures, inguinal or axillary pain, muscle cramps, fasciculations, generalized edema (with truncal wounds), paralysis, hypotension, arrhythmias, and death.47,58 The paralysis may represent spastic muscle contractures induced by pain, which are a tremendous hazard for a diver or swimmer.


When handled, a stingray may place its underside adjacent to a human limb or even wrap itself around a leg. The stingray may then bite the victim with a powerful crushing force sufficient to sever a digit or to create a substantial hematoma (Figure 81-18). A lesser wound may amount to a “stingray hickey.”35,36 (Rays will sometimes soar (“fly”) out of the water, particularly in the vicinity of a motorized boat. This behavior is attributed to a defensive maneuver, although rays will also jump in the act of birth and to dislodge parasites. In 2008, a woman in a boat was killed from head injuries from the blunt impact of a spotted eagle ray that landed in the boat. The clinical syndrome associated with freshwater stingray envenomation may in general be more severe than that associated with marine stingray envenomation.9




Treatment


The success of therapy is largely related to the rapidity with which it is undertaken. Treatment is directed at combating the effects of the venom, alleviating pain, and preventing infection. As soon as possible, the wound should be soaked in nonscalding hot water to tolerance (upper limit 45° C [113° F]) for 30 to 90 minutes. This might attenuate some of the thermolabile components of the protein venom (although this has never been proved in vivo) or interrupt nerve impulse transmission, and, in some envenomations, relieves pain.30 Hot water immersion likely has minimal or no effect on the ultimate degree of soft tissue necrosis. If hot water for immersion and irrigation (see below) is not immediately available, the wound should be irrigated immediately with nonheated water or saline. If sterile saline or water is not available, tap water may be used. This removes some venom and mucus and may provide minimal pain relief.


There is no indication for the addition of ammonia, magnesium sulfate, potassium permanganate, or formalin to the soaking solution. Under these circumstances they are toxic to tissue and may obscure visualization of the wound. During the hot water soak (or at any time, if soaking is not an option), the wound should be explored and debrided of any readily visible pieces of the sting or its integumentary sheath, which would continue to envenom the victim. Although the standard recommendation is to remove the spine and fragments as soon as possible (to limit the extent of envenomation and pain), if a spine is seen to be lodged in the victim and has acted as a dagger deeply into the chest, abdomen, or neck (this is extremely rare) and may have penetrated a critical blood vessel or the heart, it should be managed as would be a weapon of impalement (e.g., a knife). In this case, the spine should be left in place (if possible) and secured from motion until the victim is brought to a controlled operating room environment where emergency surgery can be performed to guide its extraction and control bleeding that may occur upon its removal.80


Cryotherapy may be disastrous, and no data yet support the use of antihistamines or steroids. One local remedy, application of the cut surface of one-half a bulb of onion directly to the wound, has been reported to decrease the pain and perhaps inhibit infection after a sting from the blue-spotted stingray D. kuhlii (Figure 81-19).100 The author noted that this approach is used in the Northern Territory of Australia for other fish spine stings, and that the medicinal use of the Liliaceae plant family has been recorded in many cultures. No other folk remedy, including the application of macerated cockroaches, cactus juice, “mile-a-minute” leaves, fresh human urine, or tobacco juice, has been proved effective.76



Local suction, if applied in the first 15 to 30 minutes, has been suggested by some clinicians to be of potential value (this is controversial), as may a proximal constriction band (also controversial) that occludes only superficial venous and lymphatic return. If a constriction band is deployed, it should be released for 90 seconds every 10 minutes to prevent ischemia.


Pain control should be initiated during the first debridement or soaking period. Narcotics may be necessary. Local infiltration of the wound with 1% to 2% lidocaine (Xylocaine) or bupivacaine 0.25% (not to exceed 3 to 4 mg/kg total dose in adults; not approved for children under the age of 12 years) without epinephrine may be useful. A regional nerve block may be necessary.


After the soaking procedure, the wound should be x-rayed (Figure 81-20) or otherwise imaged, then prepared in a sterile fashion, reexplored, and thoroughly debrided, particularly of hemorrhagic fat and obviously necrotic tissue. Wounds may be packed open for delayed primary closure or sutured loosely around adequate drainage in preference to tight closure, which might increase the likelihood of wound infection. Another approach that has been mentioned is wound excision followed by packing with an alginate-based wick dressing.38,76 Prophylactic antibiotics are recommended because of the high incidence of ulceration, necrosis, and secondary infection. Necrotizing fasciitis caused by Vibrio alginolyticus has followed stingray injury in a victim with preexisting hepatic cirrhosis.57 It has also been attributed to Photobacterium damsela (formerly Vibrio damsela) in a person with normal immunity punctured by a stingray in the tibialis anterior muscle.10 If the abdominal cavity is penetrated, the victim should receive cefoxitin, clindamycin–gentamicin, or another intravenous regimen intended to cover bowel flora in addition to any antibiotic(s) chosen to cover marine microbes.



If the treatment plan is to treat and release, the victim should be observed for at least 3 to 4 hours for systemic side effects. Properly treated wounds may require a few months to fully heal with complete resolution of local tissue swelling (Figure 81-21). Wounds that are not properly debrided or explored and cleansed of foreign material may fester for weeks or months.40 Such wounds may appear infected, but what really exists is a chronic draining ulcer initiated by persistent retained organic matter. Within the first few weeks after an envenomation, a foreign body can sometimes be observed by soft tissue radiograph, ultrasound, CT, or MRI. After a few weeks, exploration may reveal erosion or necrosis of adjacent soft tissue structures, synovitis, and/or the formation of an epidermal inclusion cyst or other related foreign body reaction.12,97 As with other marine-acquired wounds, indolent infection should prompt a search for unusual microorganisms. A case of invasive fusariosis (Fusarium solani) after stingray envenomation responsive to sequential debridement and ketoconazole (the latter of indeterminate effect) has been reported.56 Necrotizing fasciitis due to Photobacterium (Vibrio) damsela followed a leg laceration caused by a stingray. Notably, the patient had the wound sutured primarily and was not prescribed an antibiotic at the time of the repair.10 Hyperbaric oxygen therapy has been cited to contribute to wound healing in a refractory case of stingray-induced soft tissue necrosis and postulated infection.83 Another treatment to accelerate wound healing in a refractory case is topical recombinant human platelet-derived growth factor-BB (becaplermin gel 0.01%) every 12 hours underneath a moist dressing.7





Scorpionfish and Similar Venomous Fish


Scorpionfish are members of the family Scorpaenidae and follow stingrays as perpetrators of piscine vertebrate stings. Distributed in tropical and less commonly in temperate oceans, several hundred species are divided into three groups typified by different genera on the basis of venom organ structure: (1) Pterois (zebrafish, lionfish, and butterfly cod), (2) Scorpaena (scorpionfish, bullrout, and sculpin), and (3) Synanceja (stonefish). All have a bony plate (stay), which extends across the cheek from the eye to the gill cover. Each group contains a number of different genera and species; at least 80 species of the family Scorpaenidae have been implicated in human injuries or studied anatomically, biochemically, or physiopharmacologically.


Other venomous fish that sting in a manner similar to scorpionfish include the Atlantic toadfish (family Batrachoididae, genus Thalassophyrne) (Figure 81-22), with two venomous dorsal fin spines and venomous spines on the gill covers, and the Pacific ratfish (Hydrolagus colliei) (Figure 81-23) and European ratfish (Chimaera monstrosa), both with a single dorsal venomous spine.50 Toadfish hide in crevices and burrows, under rocks and debris, or in seaweed, sand, or mud. They may change coloration rapidly and remain superbly camouflaged. Rabbitfish (family Siganidae) (Figure 81-24, online) and leather jacks (leather backs or leather jackets, family Carangidae) carry venomous spines or fins and pose additional risks. Stargazers (family Uranoscopidae) have spines but do not appear to be venomous (Figures 81-25 and 81-26; Figure 81-26, online).








Life and Habits


Zebrafish (lionfish, firefish, or turkeyfish) are beautiful, graceful, and ornate coral reef fish generally found as single or paired free swimmers or hovering in shallow water (Figures 81-27 to 81-29; Figures 81-28 and 81-29, online). They are increasingly popular as aquarium pets and are imported illegally as part of the “underground zoo.” They have recently been introduced to the Atlantic Ocean, perhaps released from aquaria, and have been spotted from North Carolina to South Florida.4 They are proliferating in areas such as the Bahamas. To date, the introduction of “exotic” (sometimes referred to as alien, nonnative, nonindigenous, or introduced) species of fishes has not resulted in the extinction of native species in marine habitats, but this has been mentioned as a concern because of the feeding behavior of zebrafish. The western red lionfish Pterois volitans is a recently introduced species.85





Scorpionfish proper (Scorpaena) dwell on the bottom in shallow water, bays, coral reefs, and along rocky coastlines, to a depth of 50 fathoms. Their shape and coloration provide excellent camouflage, allowing them to blend in with the ambient debris, rocks, and seaweed (Figures 81-30 to 81-35; Figures 81-31 to 81-35, online). They can be captured by hook and line and serve as important food fish in many areas. The protective coloration and concealment in bottom structures make scorpionfish difficult to visualize. Some species bury themselves in the sand, and most dangerous types lie motionless on the bottom. In the United States, they are found in greatest concentration around the Florida Keys and in the Gulf of Mexico, off the coast of southern California, and in Hawaii.








Stonefish live in shallow waters, often in tide pools and among reefs (Figures 81-36 to 81-38; Figures 81-37 and 81-38, online). They frequently pose motionless and absolutely fearless under rocks, in coral crevices or holes, or buried in the sand or mud. The fish use their pectoral fins to dredge sand or mud from beneath themselves, so that they can settle deeply with only the mouth and eyes exposed.61 They are so sedentary that algae frequently take root on their skin (Figures 81-39 and 81-40; Figure 81-40, online). They are usually 15 to 20 cm (6 to 8 inches) in length, but can grow to 30 cm (12 inches). Stonefish are not indigenous to North American coastal waters.








Venom and Venom Apparatus


The venom organs are the 12 or 13 (of 18) dorsal (Figure 81-41), 2 pelvic, and 3 anal spines, with associated venom glands. Although they are frequently large, plumelike, and ornate, the pectoral spines are not associated with venom glands. Each spine is covered with an integumentary sheath, under which venom filters along grooves in the anterolateral region of the spine from the paired glands situated at the base or in the midportion of the spine. It is estimated that the two venom glands of each dorsal stonefish spine carry 5 to 10 mg of venom, closely associated with antigenic proteins of high molecular weight (between 50,000 and 800,000).21 Scorpionfish venom contains multiple toxic fractions and, in the case of stonefish venom, has been likened in potency to cobra venom. It contains a mixture of proteins containing several enzymes, including hyaluronidase.61 Hyaluronidase is a spreading factor in venoms because it degrades hyaluronate, which helps structure connective tissue. The major toxic component of Synanceja venom (stonustoxin) is a protein of molecular weight 148,000 (comprising alpha and beta subunits of molecular weights 71,000 and 79,000, respectively) that is both antigenic and heat labile. Similar purified toxins from other species are trachynilysin from S. trachynis (Australian estuarine stonefish) and verrucotoxin (a glycoprotein) from S. verrucosa (reef stonefish).88 The principal action of stonefish venom appears to be direct muscle toxicity, resulting in paralysis of cardiac, involuntary, and skeletal muscles.45 In an analysis of biologic activity, stonefish (Synanceja horrida, the Indian stonefish) venom exhibited edema-inducing, hemolytic, hyaluronidase, thrombin-like, alkaline phosphomonoesterase, 5′-nucleotidase, acetylcholinesterase, phosphodiesterase, arginine esterase, and arginine amidase activities.63 In a recent evaluation, chromatographic analysis with electrochemical detection showed the presence of substances comigrating with norepinephrine, dopamine, and tryptophan. Serotonin (5-hydroxytryptamine) was not detected.43 Crude venom of the stonefish Synanceja verrucosa possesses numerous enzymatic properties, including hyaluronidase, 8 esterases, and 10 aminopeptidases.42 Intracellular Ca2+ levels are increased by venoms of the soldierfish (Gymnapistes marmoratus), lionfish (Pterois volitans), and stonefish (Synanceia trachynis), possibly via the formation of pores in the cellular membrane, which, under certain conditions in experimental animals, may lead to necrosis.26 In addition, trachynilysin activity on the heart, often noted as negative inotropy, may also be a function of Ca2+ influx.88 The hemolytic activity of stonustoxin may in some part depend on surface tryptophan residues.102 The cardiovascular effects of stonefish venom have been attributed in part to its activity at muscarinic receptors and adrenoceptors, and pain effects perhaps to its activity at bradykinin receptors.22 Similar receptor activity, neutralized by stonefish antivenom, has been noted with lionfish venom.24 The pain-causing protein in bullrout (Notesthes robusta) venom is an algesic protein (169.8 to 174.5 kDa) called nocitoxin.53


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