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Invasive lionfish (Pterosis volitans) pose public health threats.

LIONFISH ENVENOMATION: REPORT OF A CASE

(Adapted from Patel MR, Wells S. J Hand Surg 1993 (3))

A 22-year-old tropical fish collector was cleaning his home saltwater aquarium when he was impaled on the tip of his right middle finger by 3 of the 12 venomous dorsal spines on his pet lionfish, Pterosis volitans (Figure 1). He experienced immediate, excruciating pain in his finger and right hand, and the injury site demonstrated an intense erythematous reaction surrounding the puncture marks. As an amateur aquarist, he was aware of the venomous nature of lionfish and sought immediate emergency department care, where warm (45[degrees]C) water soaks to inactivate the heat-labile venom began. A radiograph of his right hand demonstrated no retained foreign bodies. Within one hour of the injury, a fluid-filled blister developed surrounding the puncture sites and then extended over the next 12 hours from the tip of the right middle finger to the proximal interphalangeal (IP) joint. With the blistered epidermis stretched, translucent, and tense, the three puncture sites could be seen in the dermis. The patient received tetanus prophylaxis and intravenous antibiotics; and, although his pain had subsided, local pain and edema prevented any motion at the proximal IP joint. Nineteen hours following envenomation, the blister was excised and the underlying dermis was described as erythematous and oozing serous fluid. An absorbent pressure dressing was applied to the wound; and active range-of-motion physiotherapy (PT) and oral antibiotics begun. Copious oozing from the wound continued, and an area of numbness developed on the dorsum of the distal IP joint. Within a week, dermal necrosis developed on the dorsum of the distal IP joint without exposing the underlying extensor tendon. A flexion contracture developed at the proximal IP joint. It took four weeks for the necrotic ulcer on the dorsum of the right middle finger to heal. Active PT gradually restored full range of motion of the IP joints over six weeks.

METHODS

In order to describe the epidemiology of lionfish exposures, mechanisms of envenoming and poisoning, presenting manifestations, management, and prevention of injuries and foodborne poisonings, internet search engines, including PubMed, Medline, Ovid, Google[R], and Google Scholar[R], were queried with the key medical subject heading (MESH) words, "lionfish, envenomation; scorpionfish (Scorpaenidae), injuries; poisoning, ciguatera, ciguatoxin." Case reports, case series, epidemiological investigations, and toxicological studies were reviewed; high risk behaviors and occupations for lionfish injuries were identified; and human lionfish-inflicted injuries were stratified by their stages of progression from initial puncture to necrotic ulceration.

RESULTS

The Biology, Behavior, and Taxonomy of Scorpionfish

Lionfish are members of the venomous family Scorpaenidae which is among the largest in the vertebrate fish phylum (Chordata) with 45 genera and 380 species. Of these species, nearly 100 have inflicted venomous spine injuries in humans. (4-6) The scorpaenids are usually classified according to the morphology of their spines and associated venom glands as lionfish, scorpionfish, and stonefish (Table 1).

Lionfish (Pterosis spp.) have long, slender, grooved spines covered by a thin integument with paired venom glands at the spine base (Figure 2). (4-6) Scorpionfish (Scorpaena spp.) have long, thick, grooved spines covered by a thick integument with moderate-sized, paired venom glands at the spine base. (4-6) Stonefish (Synanceja spp.) have short, thick spines covered by a thick integument with large, paired venom glands at the spine base that empty quickly when compressed by torn integumentary sheaths. (4-6) The scorpaenids are all bottom-dwelling fish that prefer to feed on smaller fish on relatively shallow reefs and in rocky lagoons. (4-6) Lionfish are the most aggressive of the scorpaenids and will prey on their own young and other smaller fish, even in an aquarium. Stonefish simply lie camouflaged and motionless on the sea floor awaiting a meal displaying their strong dorsal spines only for defense if threatened. (4-6) Scorpionfish, such as the California scorpionfish or sculpin, are also docile and well-camouflaged, and cause envenomation injuries when caught in nets, hooked by commercial and recreational fishermen, or speared by divers. (4) The scorpaenids range in length from 2-3 inches as juveniles to 15-17 inches as adults and can weigh up to a pound. (4) Lionfish are the most prolific breeders and can release two egg clusters monthly, containing up to 15,000 eggs. (4,5) There are nine species of lionfish, two of which have invaded US waters: (1) Pterosis volitans, the red lionfish, is the predominant species (93 percent); and (2) Pterosis miles is the minority species (7 percent). (2) Lionfish can live from 5 to 15 years. (2)

Scorpionfish Venoms and the Mechanisms of Envenomation

All scorpaenids envenomate their victims by erecting the spines on their dorsal, anal, and pelvic fins that pierce their victim's flesh and inject venom down bilateral grooves connected to venom glands on either side of the spines. (4-6) Pectoral fins are not associated with venom glands. (4-6) Lionfish have an extensive envenomating apparatus with 12 to 13 (out of 18) dorsal spines, 2 pelvic spines, and 3 anal spines all having paired basilar venom glands (Figure 2). (4-6) As spines pierce a victim's skin, the integument is torn and spine tips can be broken off leaving retained foreign body fragments in the victim's flesh (Figure 2). (4-6) Although scorpaenid venoms contain similar mixtures of enzymes and proteins, they do differ in potencies with stonefish venom being the most potent and capable of fatal envenomation, and lionfish venom being the least potent. (4-6) Although scorpaenid venoms have not been fully characterized, lionfish venom does contain acetylcholine, several hyaluronidases, and unidentified sodium channel-active toxins capable of blocking neuromuscular transmission. (7,8) Scorpaenid venoms are all heat labile and non-dialyzable, and can cause vasodilation, hypotension, muscular weakness, and neuromuscular paralysis when injected into experimental animals. (7,8) Scorpaenid venoms retain their full potencies for up to 48 hours following the animal's death. (4,9)

In response to fatalities following stonefish envenomations, the Australians developed an equine fragment antigen-binding (Fab) antivenin which is also cross-neutralizing with lionfish and scorpionfish venoms, but is usually reserved for severe stonefish envenomations (stonefish ntivenin, Commonwealth Serum Laboratories Limited, Parkville, Victoria, Australia, 2,000 units per 2 ml ampoule). (9) Public aquariums, such as Sea World[R] and others, that display venomous scorpaenids are encouraged to have antivenin on hand. (4)

The Descriptive Epidemiology of Scorpionfish Injuries

Three retrospective descriptive epidemiological studies of scorpaenid envenomations have been conducted with similar findings. Kizer and co-investigators described fifty-one cases of scorpaenidae envenomation reported to the San Francisco Bay Area Regional Poison Control Center (PCC) during the period, 1979-1983. (4) Forty-five envenomations were caused by lionfish (Pterosis volitans), and the remaining six were caused by the California scorpionfish or sculpin (Scorpaena guttata). (4) Most of the lionfish injuries occurred in homes with saltwater aquariums (82 percent) or in tropical fish stores (18 percent) when victims tried to transfer, catch, or hand-feed a lionfish. (4) In two cases, amateur aquarists were attempting to remove dead lionfish from their home aquariums. (4) Sculpin are prized edible fish, and the sculpin envenomations occurred either in fishermen or scuba divers or in persons cleaning sculpin. (4) All of the sculpin injuries and most of the lionfish injuries (n=44, 98 percent) were on the hand with the four remaining lionfish stings on the elbow. (4) Most cases occurred in males (n=37, 77 percent) with a mean age of 27 years (range=7-55 years). (4) All patients experienced intense pain extending from the wound site to most or all of the extremity with massive swelling of the digit or extremity in most (58 percent) cases. (4) Systemic manifestations of weakness, syncope, dyspnea, and hypotension occurred in six patients (13 percent). (4) All patients received tetanus prophylaxis. (4) There were no deaths in the case series. (4)

Trestrail and al-Mahasneh described 23 cases of lionfish (Pterosis spp.) envenomation reported to the Blodgett Regional PCC in Grand Rapids, Michigan, during the period, January 1979-March 1988. (10) Most cases occurred in the homes of amateur aquarists and in males (91.3 percent) with a mean age of 29.8 years. (10) All envenomations occurred on the fingers or hand and all were symptomatic. (10) There were no deaths in the case series. (10)

In 1996, Aldred and co-investigators described 33 cases of lionfish (Pterosis volitans) envenomation reported to the Chicago Regional PCC over a 2-year period. (11) All injuries occurred on the hands and presented with intense pain which responded to immersion in non-scalding water in most cases. (11) All patients received tetanus prophylaxis; and two patients required hospitalization for systemic reactions and pain control. (11) There were no deaths in the case series. (11)

In summary, well-conducted retrospective epidemiological investigations of lionfish envenomation cases reported to regional PCCs have reached the following conclusions: (1) Lionfish envenomations occur predominantly in male home aquarists on the upper extremity, usually the hand, and cause intense pain and swelling relieved by immersion in non-scalding (up to 45[degrees]C) water; (2) besides home aquarium owners and pet store patrons, other avocations predisposed to scorpaenid envenomation include fishing, fish cleaning, and scuba diving; (3) severe presenting manifestations of pain and edema in the upper extremity may be accompanied by significant, but nonfatal, systemic manifestations that may require hospitalization in a few cases; and (4) even dead lionfish can inflict envenoming injuries.

The Clinical Manifestations of Lionfish Injuries

The clinical manifestation of lionfish injuries may be classified as acute, systemic, subacute, and chronic; all of which were described in the cases reported. The acute presenting manifestations include immediate, intense pain at the wound site with pain extending proximally; initial erythema, ecchymosis, or pallor around the wound with edema extending proximally; and any combination of anesthesia, hypesthesia, or paresthesia. (4-6) The acute systemic manifestations may include nausea, diaphoresis, dyspnea, weakness, cardiac arrhythmias, myocardial ischemia, chest or abdominal pain, hypotension, and syncope. (4-6) Pulmonary edema, tremors, and seizures may occur, but are more common after stonefish envenomation. (9)

There is a definite progression of acute to subacute manifestations of the lionfish injury. This progression has been described as follows: (1) grade one with intense erythematous reaction at the wound site; (2) grade two with bullae formation separating epidermis from dermis; and (3) grade 3 with necrotic ulceration at the injury site associated with increasing extremity edema limiting joint motion proximally. Regional lymphadenitis and adenopathy are uncommon. (9,12) Chronic manifestations may include slowly healing necrotic ulcers at the wound sites, continuing allodynic manifestations, and joint contractures. (3) Late complications may include secondary infections, foreign body granulomas, and peripheral neuropathies. (9,12)

The Management of Lionfish Injuries

The cornerstone of managing lionfish envenomation is immediate immersion of the affected extremity in non-scalding, hot water (up to 45[degrees]C) for 30 to 90 minutes to inactivate the heat labile components of lionfish venom. (9,13) The other general principles of wound management include wound irrigation with warm sterile saline solutions; exclusion of foreign bodies, such as spine integumentary sheaths and/or tips, by inspection and/or radiographs; and tetanus prophylaxis. (4-6) Surgical debridement, incision and drainage, and fasciotomy are not indicated. (4-6) However, some investigators have concluded that the separation of epidermis from dermis in grade 2 and later necrosis in grade 3 envenomations are the results of local toxin infiltration into the dermis and subcutaneous tissues. (3,12,13) As a result, some investigators have recommended immediate drainage of blisters by sterile aspiration or by excision of large bullae in all grade 2 envenomations. (3,10,11)

Oral or intravenous opioids are indicated for pain control unresponsive to hot water immersion, and benzodiazepines may be indicated for anxiety and muscle spasms. Antibiotic prophylaxis is unnecessary and should be selected for the treatment of secondary wound infections as directed by bacterial cultures and antibiotic sensitivity testing. Antibiotic prophylaxis with fluoroquinolones may be indicated in deep or contaminated wounds, or in immunosuppressed patients with cancer, diabetes, liver or renal disease, or on chronic corticosteroid therapy. (12) Stonefish antivenin is rarely indicated for lionfish envenomations unless symptoms are non-responsive to hot water immersions and adjunctive treatments with analgesics and regional anesthetic blocks (4, 9,12)

The Prevention of Lionfish Injuries

The best strategies for the prevention of lionfish injuries include avoidance and recognition that even dead lionfish can cause envenomation for at least 48 hours. Additionally, hypersensitivity to lionfish venom may develop and pose a risk of anaphylaxis following a second lionfish envenomation. (4,9) People preparing lionfish for consumption should cut off all of the dorsal, caudal, and anal fins with their attached spines wearing puncture-proof gloves before fileting the fish (Figure 2).

Controlling Invasive Lionfish: The "Lionfish as Food Campaign"

Lionfish overpopulate and damage reef ecosystems, reduce fish biodiversity and habitat, and drive preferred bait fish away; threating the marine seafood chain in important commercial fisheries. In 2011, lionfish were observed in the Flower Garden Banks National Marine Sanctuary off the coast of Louisiana, a critical supporting reef ecosystem for commercial fisheries in the Gulf of Mexico (Figure 3). (2) In addition to encouraging everyone to report lionfish sightings and to licensing divers to spear lionfish in marine sanctuaries, another effort now underway to control the lionfish population explosion is NOAA's "Lionfish as Food Campaign". (2) Lionfish filets have a light, flaky, white texture like grouper and do not taste "fishy". (2) Recipes abound for preparing lionfish including fried lionfish, grilled lionfish, and lionfish ceviche. (2) Popular lionfish dishes may be found on the menus of many coastal seafood restaurants. (2)

A New Threat from Lionfish: Ciguatera Fish Poisoning (CFP)

Lionfish are reef and structure dwellers that prey on smaller fish, invertebrates, and mollusks, most of which are herbivores that feed on algae growing on corals and can bioconcentrate dinoflagellate toxins, such as gambiertoxins. (2) Gambiertoxins are produced by dinoflagellates of the genus Gambierdiscus and are converted into ciguatoxins during trophic transfer in herbivorous and, later, carnivorous fish. (2) Ciguatoxins are colorless, odorless, and tasteless toxins that remain stable at normal cooking temperatures and for extended periods during freezer storage. (2) CFP results from the consumption of predatory reef fish that have accumulated ciguatoxins, especially amberjack, barracuda, grouper, king mackerel, Spanish mackerel, sea bass, snapper, and surgeon fish. (2,14-16) In 2014, scientists from the FDA reported that of nearly 200 lionfish caught off the US Virgin Islands during 2010-2011, 12 percent contained ciguatoxin that exceeded the FDA guidance level of 0.1 [micro]g/kg of fish meat and could cause CFP. (2) Lionfish may now be added to the list of predatory reef fish that can cause CFP. The attack rate for CFP after consuming a ciguatoxic fish is 80-90 percent. (16)

CFP is a common cause of fish poisoning clusters in the US with 509 outbreaks affecting 508 persons reported to the US Centers for Disease Control and Prevention (CDC) between 1988 and 1992. (15) CFP is diagnosed clinically by a unique combination of acute gastrointestinal (nausea, vomiting, diarrhea, abdominal cramps and pain) and neurologic symptoms (generalized muscular weakness, lightheadedness, circumoral and extremity paresthesias and pruritus, hot-cold temperature reversal and other paradoxical dysesthesias, and painful or loose-feeling teeth) within a mean of five hours after consuming ciguatoxic fish. (14-16) Although most symptoms typically persist for about a week, the neurologic symptoms may last for months and may be worsened or renewed by alcohol consumption, exercise, sexual intercourse, and dietary habits, especially consumption of fish and nuts. (15,16)

There is no specific treatment for CFP. Neurologic manifestations have been treated with antidepressants, anticonvulsants, and sodium channel blockers with variable success. (14-16) The only way to prevent CFP is to avoid eating potentially ciguatoxic fish; especially fish caught in known ciguatoxin-contaminated areas. (15) Vendors should not sell fish to restaurants caught in known ciguatoxin-contaminated waters. CFP outbreaks should be investigated immediately by traceback investigations conducted by public health authorities in order to determine the species and source of ciguatoxic fish. (15,16) Ciguatoxins can be detected in suspected fish samples by in vitro mouse neuroblastoma assay for nonspecific sodium channel toxins with any positive extracts later confirmed as specific ciguatoxins by liquid chromatography-tandem mass spectrometry. (16)

CONCLUSIONS

Although beautiful to watch in an aquarium, lionfish now pose several public health threats that include (1) serving as the second most common cause of venomous fish puncture injuries next to stingrays; (2) interrupting the marine seafood chain on reef systems that support commercial fisheries; and (3) bioconcentrating heat-stable algal toxins capable of causing CFP when cooked ciguatoxic lionfish are consumed as recommended by NOAA's "Lionfish as Food Campaign." New strategies to control the lionfish population explosion in coastal waters and offshore fisheries are needed now to ensure seafood safety and public health in the US. Biological controls, such as parasitic crustaceans and leeches, could introduce another invasive species.

James H. Diaz, MD

REFERENCES

(1.) Schofield PJ. Geographic extent and chronology of the invasion of the non-native lionfish (Pterosis volitans and P. miles) in the Western North Atlantic and Caribbean Sea. Aquatic Invasions. 2009;4:473-479.

(2.) Robertson A, Garcia AC, Flores-Quintana HA, et al. Invasive lionfish (Pterosis volitans): A potential human health threat for ciguatera fish poisoning in tropical waters. Marine Drugs. 2014;12:88-97.

(3.) Patel MR, Wells S. Lionfish envenomation of the hand. J Hand Surg. 1993;18: 523-525.

(4.) Kizer KW, McKinney HE, Auerbach PS. Scorpaenidae envenomation. A five-year poison center experience. J Am Med Assoc. 1985;253:807-810.

(5.) Auerbach PS. Marine envenomations. N Engl J Med. 1991;325:486-493.

(6.) Fernandez I, Valladolid G, Varon J, Sternbach G. Encounters with venomous sea life. J Emerg Med. 2011;40:103-112.

(7.) Cohen AS, Olek AJ. An extract of lionfish (Pterosis volitans) spine tissue contains acetylcholine and a toxin that affects neuromuscular transmission. Toxicon 1989; 27: 1367.

(8.) Kiriake A, Madokoro M, Shiomi K. enzymatic properties and primary structures of hyaluronidases from two species of lionfish (Pterosis antennata and Pterosis volitans). Fish Physiol Biochem. 2014;40:1043-1053.

(9.) Auerbach PS. Envenomation by aquatic vertebrates. In Auerbach PS, Ed., Wilderness Medicine, Fifth Edition, Mosby Elsevier, Philadelphia, PA:1740-1741.

(10.) Trestrail JH III, Al-Mahasneh QM. Lionfish sting experiences of an inland poison center: a retrospective study of 23 cases. Vet Hum Toxicol. 1989;31:173-175.

(11.) Aldred B, Erickson T, Lipscomb J. Lionfish envenomations in an urban wilderness. Wilderness Environ Med. 1996;7:291-296.

(12.) Vetrano SJ, Lebowitz JB, Marcus S. Lionfish envenomation. J Emerg Med. 2002; 23:379-382.

(13.) Auerbach PS, McKinney HE, Rees RE, Heggers JP. Analysis of vesicle fluid following the sting of the lionfish, Pterosis volitans. Toxicon. 1987;25:1350-1353.

(14.) Ciguatera fish poisoning--Florida, 1991. Morb Mort Wkly Rep. 1993;42:417-418.

(15.) Ciguatera fish poisoning--Texas, 1997. Morb Mort Wkly Rep. 1998;47:692-694.

(16.) Ciguatera fish poisoning--New York City, 2010-2011. Morb Mort Wkly Rep 2013;62:61-65.

(17.) Brian Handwerk (April 4, 2011). "Shark's Lionfish Lunch". Available at http://www.news.nationalgeographic.com/news/2011/03/pictures/ 110404-sharks-lionfish-alien-fish-invasive-species-science.

Dr. Diaz is a Professor of Public Health and Preventive Medicine, Program Director, Environmental and Occupational Health Sciences, School of Public Health, Professor of Anesthesiology, School of Medicine, Louisiana State University Health Sciences Center in New Orleans.

Table 1. Family Scorpaenidae Classification by Morphology of Venom
Apparatuses

Subfamily names   Scorpaeninae         Scorpaeninae

Common names      Scorpionfish         Lionfish (Turkeyfish)

Common genera     Rhinopias            Dendrochirus
                  Scorpaenopsis        Pterosis

Geographic        Mostly tropical      Mostly tropical Indian and
distributions     Indian and           Western Pacific Oceans
                  Western Pacific      2 Pterosis species were
                  Oceans               introduced into US waters off
                  Few species in the   of the coast of Southeast
                  Eastern Pacific      Florida in the 1990s and have
                  Ocean from           now spread from coastal North
                  coastal California   Carolina to Texas and
                  to Central           throughout the Caribbean to
                  America              Barbados.

US species        Scorpaena guttata    Pterosis volitans (red
(common names)    (California          lionfish, 93% of US
                  scorpionfish,        population) Pterosis miles
                  sculpin)             (common lionfish, devil
                                       firefish, 7%)

Subfamily names   Synanceinae

Common names      Stonefish

Common genera     Synanceia
                  verrucosa
                  (reef stonefish)
                  Synanceia
                  horrida
                  (estuarine
                  stonefish)

Geographic        Mostly tropical
distributions     Indian and
                  Western Pacific
                  Oceans

US species        Not presently
(common names)    in US coastal
                  waters
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Author:Diaz, James H.
Publication:The Journal of the Louisiana State Medical Society
Article Type:Clinical report
Date:Jul 1, 2015
Words:3332
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