Environmental dermatology: skin manifestations of injuries caused by invertebrate aquatic animals.

Contact between humans and coastal areas has increased in recent decades, which has led to an increase in injuries from aquatic animals. The majority of these present dermatological manifestations, and some of them show typical lesions. The highest percentages of injuries that occur in marine environments are associated with invertebrates such as sea urchins, jellyfish and Portuguese men-of-war (echinoderms and cnidarians). In this review, we discuss the clinical, therapeutic and preventive aspects of injuries caused by marine and freshwater invertebrates, focusing on first aid measures and diagnosis for dermatologists and professionals in coastal areas.

INTRODUCTION

Due to the growing interface between humans and aquatic environments, interest in this topic has increased in recent years. Brazil has a coastline of about 8,500 kilometers and the most extensive freshwater ecosystem in the world.[1-5] Thus, there is a varied fauna, encompassing animals of temperate and tropical waters, including many potentially dangerous animals that come into contact with humans due to the large influx of swimmers to beaches, the increase in commercial and sport fishing, and other activities such as scuba diving and underwater fishing.[1-5]

Toxins are substances produced by animals that, within the body of another animal, react with certain cells and organs, causing deleterious effects. Poisons are toxins that cause harm when ingested, as happens with puffer fish and toads. Venoms are toxins that cause effects after being injected through spikes, fangs or stingers. The action of toxins varies, but the main effects are neurotoxic, proteolytic, myotoxic, hemotoxic (hemolytic) and cytotoxic. The aquatic animals that are dangerous to humans, grouped together according to the frequency and severity of accidents, are: sponges, cnidarians, worms, mollusks, echinoderms, crustaceans, fish and reptiles.[1-5]

EPIDEMIOLOGY

Accidents involving invertebrates aquatic animals (especially marine animals) reach their peak during the summer, when the population of some coastal towns increases approximately tenfold, or more. However, most animals that cause accidents do not vary in number during the year's seasons, and the large number of cases during this period is due to the number of humans in the water, lack of information and precautions regarding these animals. Bathers constitute more than 90% of the victims and the incidence of this type of accident is 0.1%, or 1 in 1,000, in emergency units. This is a high number, and during the holiday season, it happens that up to 3,000 people a day are treated at one emergency unit[1-5] Among the victims, approximately 50% are bathers who step on sea urchins and presenting traumatic accidents, 25% are bathers who have contact with cnidarians (jellyfish and Portuguese men-of-war) and 25% are fishermen injured by venomous fish, such as catfish and stingrays.[1-5]

PHYLUM PORIFERA (Sponges)

Marine sponges are simple animals, with a circular body and "skeleton", consisting of calcium carbonate, silica and spongin. Sponges have a species of irritating slime on the surface of the skeleton, and the spikes of the body contribute to this.[1-5] The sponges associated with lesions in humans are of the genera Neofibularia sp, Tedania ignis (the fire sponge) and Microciona prolifera, the red sponge (Figure 1).

FIGURE 1

Top-left: marine sponge. Below: freshwater sponge (cauxi). Right: details of sponges. Photos: Vidal Haddad Junior

The dermatitis caused by the contact with sponges has an eczematous pattern, appearing rapidly (within 1-3 hours). In the affected areas, there is erythema and edema, forming papules that subsequently give rise to plaques, vesicles, and, more rarely, blisters (Figure 2). Itching is intense and the cure for the dermatitis develops in about two weeks. The most common location is in the hands and there are no systemic complications, but the dermatitis may be associated with complications such as erythema multiforme, severe conjunctivitis, local hyperpigmentation and anaphylactoid reactions.[1-5] Adhesive tape is recommended for the removal of micro spines, along with corticosteroid creams and cold compresses to relieve local inflammation.[2,6] The rare accidents observed by the author concerned biologists who collected sponges.[2]

FIGURE 2

Left: eczema-like plaques on the hand of a biology student who collected marine sponges for research. Right: disseminated excoriated papules in a swimmer after diving in a lake in the Amazon region. Photos: Vidal Haddad Junior

Sponges also exist in freshwater environments and some species can cause irritating skin disorders similar to those caused by marine sponges.[4] Belonging to the class Demospongiae, they are popularly called cauxi in the Amazon region and pó-de-mico (monkey powder) in savannah-like areas cerrados (savannahlike environments), and are found in the ponds of these ecosystems (Figure 1). Lesions caused by freshwater sponges are disseminated, manifesting as pruritic erythematous papules surmounted by vesicles, and may also present exulcerations, crusts and secondary infections,[4] All skin and mucous membranes can come into contact with the spicules of sponges, which occurs in the baths in pools and rivers (Figure 2). Another interesting aspect is the manifestation of lesions, caused by freshwater sponges, in the hands of indigenous Brazilians in the Amazon region, who use the silica "skeleton" of the sponges to confer resistance to ceramics, manipulating them for this purpose. Treatment for injuries caused by marine sponges is effective. If manifestations are severe, it is important to use systemic corticosteroids, 30 to 40mg of prednisone per day for approximately a week, with gradual withdrawal. The problem seems to be common in some regions but there is a lack of additional studies, including definitive proof of the etiology through finding spikes in injuries. A study of human eye injuries (uveitis and leukomas) in riverside people, associated the lesions with the presence of spicules from two freshwater sponges (Drulia uruguayensis and D. ctenosclera). The findings were confirmed by a histopathology exam of the lesions, demonstrating the etiology of the ophthalmic processes.[7,8]

PHYLUM CNIDARIANS (Jellyfish and Portuguese men-of-war)

Cnidarians are gelatinous animals with dimorphic life cycles. They can appear in free or medusa form (jellyfish), reproduced sexually; or in the form of polyps, which are fixed and reproduce asexually. Four types are important for medicine: Anthozoa (corals and anemones that do not appear in medusa form), Hydrozoa, Scyphozoa and Cubozoa (cubomedusae).

These animals have highly specialized defense cells called cnidocytes, which include nematocysts, composed of small distal spicules in a spiral structure and kept under pressure, triggering changes in pressure and/or osmosis, which can lead to the inoculation of venom into the dermis of the victim. A cnidarian with long tentacles can have millions of nematocysts. When an accident happens, many nematocysts initially remain intact in the victim's skin, without discharging its contents.

The venom of nematocysts contains tetramine, 5hydroxytryptamine, histamine and serotonin, as well as thermolabile high molecular weight toxins, capable of changing ionic permeability and causing cardiac dysfunction.[9] The venom can also cause hemolysis and renal failure, which develops in later phases.[10] Nontoxic proteins can trigger allergic processes of varying severity.[1-5] The concentration and potency of the venom varies according to a scale, from corals and anemones to Portuguese men-of-war and some jellyfish.[1-5]

The signs and symptoms of envenomation depend of a toxic action (immediate) and an allergic action (immediate and delayed). Intense and immediate pain occurs in areas that come into contact with the animal, along with a burning sensation (but it should not be called a burn, because is an action of toxins), a linear erythematous papular rash, urticariform, with crossed lines. In this initial stage, there may be horripilation, probably from alteration of the sympathetic nervous system.[1-5] Within a matter of hours, the area may present vesicles, blisters and even superficial necrosis. The pain subsists for hours and systemic phenomena can be installed, such as general disorganization of nerve activity, heart failure (rare), shock, respiratory failure, hemolysis and renal abnormalitie, which are responsible for cardiopulmonary deaths in severe cases. Cubomedusae (Chironex fleckeri, Chiropsalmus quadrumanus and C. quadrigatus, Tamoya haplonema and others) and the Portuguese man-of-war (Physalia physalis and P. utriculus) can cause accidents of this magnitude (Figures 3 and 4).[11-15] There are hundreds of documented deaths caused by contact with cubomedusae worldwide. Most of them are caused by the species Chironex fleckeri, in the Indo-Pacific region.[10] There are also reports of deaths related to accidents with Portuguese men-of-war (Physalia physalis) and cubomedusa Chiropsalmus quadrumanus, in the Atlantic Ocean.[2,16]

FIGURE 3

Linear and long crisscrossed plaques after the contact of a bather with a Portuguese man-of-war. In detail: Physalia physalis, the Portuguese man-of-war. Photos: Shirlei Pacheco and André Rossetto

FIGURE 4

Linear plaques of large diameter and crossed with "frozen" element, which arose after contact with the cubomedusa Chiropsalmus quadrumanus, present on the Brazilian coast (see detail). Photos: Vidal Haddad Junior and Álvaro Migotto

After the accident, immediate allergic reactions can occur, such as angioedema and anaphylaxis. There are late allergic reactions: persistent lesions after 48 hours, new lesions at distance, recurrent reactions (four or more), contact dermatitis or late onset of new lesions. Ingestion of jellyfish is observed in oriental cuisine, and has been associated with gastrointestinal and skin allergies.[17]

Contact accompanied by pain and rounded or small tentacle marks, suggests envenomation by Olindias sambaquiensis, a common hydrozoan in the South and Southeast regions of Brazil, which is constantly associated with serial injuries on our beaches, accounting for about 80% of accidents in these regions (Figure 5).[12,15,18]

FIGURE 5

Rounded or oval plaques and small linear marks indicate envenomation by Olindias sambaquiensis, a common hydrozoan in southeastern and southern regions of Brazil (see detail). Photos: João Luiz Costa Cardoso e Álvaro Migotto

The larvae of the jellyfish Linuche unguiculata, a small scyphomedusa, were involved in the genesis of the seabather's eruption, a pruritic erythematous papular eruption that develops in areas covered by swimsuits (Figure 6). This dermatitis was first described in Brazilian bathers in Ubatuba (São Paulo State).[19] Recently, new cases have been reported on the coast, especially in the South of the country, suggesting that the disease is far more common than previously thought.[20,21]

FIGURE 6

Excoriated papules in areas covered by swimsuits are typical of seabather’s eruption. In detail: Linuche unguiculata, the thimble jellyfish, whose larvae and adult forms cause the dermatitis. Photos: João Luiz Costa Cardoso and Álvaro Migotto

Envenomation by anemones can be severe, though this usually causes mild manifestations. Erythematous, irregular and painful plaques and papules arise at points of contact with the short tentacles of anemones. Fire corals (Millepora sp) are hydrozoans that cause severe and extensive envenoming, and can provoke medical emergencies. True corals cause minor accidents, but can bring about deep wounds in bathers. There is a report of a fatal accident by fulminant hepatic failure, following a diver's contact with an anemone (Condylactis sp).[22]

Accidents involving some hydrozoans, true corals, anemones and fire corals, show no typical pattern. Marks are irregular and can be rounded, oval shaped or without any defined form.[23] These accidents should be emphasized to divers who approach the underwater substrate and experience local pain and burning, as well as rapid onset of lesions.

The most common complication of accidents involving cnidarians is the residual hyperpigmentation, but keloids, atrophy of subcutaneous tissue and gangrene, may also arise.[1-5] Cuts from corals can develop a foreign body granulomatous reaction.

Immunologic methods to aid diagnosis are few: there is a serum test via the enzyme-linked immunosorbent assay (ELISA) method, which shows the etiology of seabather's eruption.[24] Histological exams can help diagnose late allergic phenomena, as well as contact tests. Some species of cnidarians were identified from the recovery nematocysts in human skin, through the adhesive tape method.

Controversy surrounds the treatment of envenomation by cnidarians: in all accidents, compresses of iced sea water or cold packs, with protection using a thin cloth, should be applied, so that freshwater does not reach the wounded area. This measure has a potent analgesic effect and should always be applied, even at beaches, as a routine first aid step.[1-5,12,15] The application of fresh water onto the skin triggers loaded nematocysts by osmosis. However, there is a randomized trial showing that the immersion of the affected area in hot water (45º C) for 20 minutes would be more effective than cold water immersion.[25] Our view is that what interferes with the nociceptive activity of the venom, are extreme temperatures, since cold water also has a positive analgesic effect, as evidenced by earlier studies.[1-5,12,15]

When the animal involved is a cubomedusa (Chironex fleckeri, Carukia barnesi, Tamoya haplonema or Chiropsalmus quadrumanus), it is crucial to apply 5% acetc acid (vinegar), in order to inactivate nematocysts that are still intact on the skin or any remaining tentacles. In cases of envenomation by Portuguese men-ofwar (Physalia physalis) or Olindias sambaquiensis, this course of action is less safe, since in vitro experiments have shown that the nematocysts of some specimens of Portuguese men-of-war fire when placed in solutions of vinegar or alcohol.[26] In our clinical experience, however, the application of vinegar is a beneficial measure for any accident caused by cnidarians on the Brazilian coast.[1-5] [12,15]

Other measures such as the use of antihistamines, urine, alcohol or Coca-Cola®, are not scientifically endorsed and should not be applied, so as to avoid worsening of the condition and generally inadequate treatment. Patients with systemic manifestations (hypotension / hypertension, cardiac arrhythmias, pulmonary edema) should be referred urgently to a hospital, which can be useful if pain persists after first aid measures (in these cases, an intramuscular dipyrone ampoule seems to control pain). Cardiac arrhythmias should be treated with intravenous use of verapamil.

Accidents caused by cnidarians are easy to identify, following the classic pattern of erythematous crossed lines that arise soon after contact, accompanied by intense pain. There is a pattern in the clinical manifestations caused by cnidarians in Brazil and throughout the South Atlantic, as well as North and Central America: few, long and crisscrossed lines, suggesting cubomedusae and Portuguese men-of-war (severe envenomation, excruciating pain and systemic phenomena). The presence of the Portuguese man-ofwar's float inculpates the animal. Rounded skin lesions with impressions of small tentacles without systemic phenomena, are suggestive of accidents caused by Olindias sambaquiensis, a very common hydrozoan on the Atlantic coast of South America.[15]

PHYLUM ANNELIDA (Leeches and polychetas)

Leeches belong to the subclass Hirudinea (Figure 7). These worms, which can reach 10cm in length, are cosmopolitan and found in freshwater (although they may exist in marine and even arboreal environments). The parasite species clings firmly onto creatures via oral and caudal suckers, and jaws equipped with sharp teeth, feeding on blood. A leech can ingest up to ten times its weight in blood, but does not cause major problems in the victims. The therapeutic use of these worms was widespread in antiquity, when bloodletting was carried out in patients, using the species Hirudo medicinalis. The saliva of leeches contains hirudin, an anticoagulant substance that prevents blood clotting in their digestive tract. Allergies and infections may also occur.[2-5]

FIGURE 7

Top-left: leeches. Polychaetes (brushworms and smooth worms). Marine worms cause injury through biting and penetration by the body bristles. Photos: Vidal Haddad Junior

Marine worms are similar to land worms (Figure 7). The most representative are marine brush worms, which can injure unsuspecting divers with bites from powerful jaws, with chitinous teeth, and introduce setae or spicules into the skin, causing edema, papules, itching and pain, which can lead to skin necrosis.

Leeches should be removed by applying alcohol or the heat of a flame, near the animal. Mechanical removal of leeches should be avoided, as there is a risk of trauma. Topical antibiotics should be applied to the affected area for around seven days. Wounds from marine worm bites should be washed extensively, followed by the application of topical antibiotics. The skin harmed by spicules should be dealt with using tweezers and adhesive tape, with the aim of removing the bristles. Marine worms are common on our coast and mussel catchers are often in contact with these animals, though injuries are rare. Other people who experience contact include marine wildlife researchers and divers.[2-5]

PHYLUM MOLLUSCA (Octopus and Conus snails)

Mollusks are organisms that may or may not have shells to protect their bodies. Some gastropods (with only one shell) can inject venom. Among these, the Conus genus causes serious envenomation, inoculating venom via a spike (radula) contained in a proboscis, a tube in the distal end of the body. The venom of Conus snails is composed of low molecular weight neurotoxins that can induce neuromuscular blockades and progressive paralysis, even affecting respiratory muscles, culminating in sporadic death. The action is very quick and it occurs through blocking of receptors of sodium, potassium and calcium channels, present in muscles and nerves.[2-5, 10]

The exact number of proven deaths caused by accidents with Conus is not known, though it is estimated to be about 50. The history of contact with the mollusk associated with muscle weakness points to the occurrence of accidents.[1-5]

The most venomous species of Conus feed on fish. In Brazil, most species feed on worms and other mollusks. Some well-known species such as Conus clerii, Conus regius and Conus jaspideus, depend on the capture of polychaetes (Figure 8). There are two Atlantic Ocean species of large diameter: Conus centurio and Conus ermineus, the latter being clearly piscivorous.[27] Recently, an accident caused by Conus regius was reported in Brazil.[28]

FIGURE 8

Conus regius and Octopus sp., the common octopus. Photos: Vidal Haddad Junior

The blue-ringed octopus (Hapalochlaena sp) belongs to the Cephalopoda class and it inoculates a powerful neurotoxin that blocks sodium channels in axons and causes muscle paralysis similar to that observed in accidents caused by Conus. There are no blue-ringed octopuses in the Atlantic Ocean.

The common octopus (Octopus sp) is found worldwide and it has recently been described as a venomous animal, carrying cephalotoxin, a neurotoxin that helps the octopus to catch its prey (Figure 8).[29] The author noted a case of envenomation in a young woman, following consumption of raw (common) octopus meat (Japanese cuisine), which presented generalized neurotoxicity manifested by paresthesias (including perioral), malaise, dizziness, diarrhea and muscle weakness without paralysis.[29] An injury caused by the "beak" of an octopus in the hand of a patient provoked an area of induration and erythema measuring about 8.0 cm, which persisted for weeks. Suckers in tentacles can cause traumatic purpura, through the strong suction (from published personal communications of the author).

There are no laboratory tests to diagnose accidents caused by Conus snails. In envenomation by Conus and octopuses, it is important to remove the remaining tissues of the animal in the area of the bite/sting, perform local asepsis and if necessary, apply therapeutic measures for neuromuscular paralysis, including the use of artificial respiration, the only effective means of treatment. The severity depends on the installation of the full manifestations and we should also consider the location of the accident, because a lack of medical resources also influences the prognosis.[2-5, 27,28,29]

PHYLUM ECHINODERMATA (Sea urchins, starfish and sea cucumbers)

Echinoderms are animals with rounded bodies and some species exhibit hollow spicules of calcium carbonate on the surface, capable of causing severe traumatic accidents (Figure 9). Some species of starfish (such as the species "crown-of-thorns") and sea urchins are venomous. In sea urchins, the venom has hypotensive and hemolytic neurotoxic and cardiotoxic effects, due to toxins present in the pedicelaria, small tentacles that are located among the spikes.[2,30] Sea cucumbers (Holothuria) produce holothurin, a toxin that irritates the skin and mucous membranes.

FIGURE 9

Top-left: black sea urchins (Echinometra lucunter). Below: spines in the feet of bathers. Photos: Vidal Haddad Junior. Right: hyperkeratotic nodules on the hands of a diver who suffered several injuries caused by black sea urchins (foreign body granuloma). Photo: André Rossetto

In traumatic injuries caused by sea urchins (almost all accidents in Brazil), spines penetrate human skin and break, appearing as small black spots on the skin (Figure 9). It is possible to extract fragments of up to 3.0 cm of the site, but most are small pieces and sometimes only pigments remain at the point of entry of the spicule. The pain is moderate and only occurs by compression.[30,31,32] The plantar regions are commonly affected and spines may serve as a gateway for secondary infections, including tetanus. Most spines are eliminated, but there may nodules with erythematous and verrucous surfaces (foreign body granuloma) that are difficult to resolve.[30,31,32] Accidents caused by venomous echinoderms cause skin inflammation, manifested by erythema, edema, papules, vesicles and occasional necrosis.[2-5]

The species Echinometra lucunter is the most common in Brazil and it causes traumatic accidents, since there are no signs of envenomation after contact. Bathers are the major victims of this accident, but it is common to see freedivers with spicules or late-developing nodules, mainly on the hands, in contrast to swimmers, who suffer foot injuries when walking in shallow waters and small pools between rocks, generally at transition points on beaches. Accidents involving black sea urchins are the most common among all caused by marine animals (about 50%).[1-5,30,31,32]

The removal of spines of sea urchins should be done under local anesthesia. Thus, a superficial scarification with a large-caliber hypodermic needle is performed, and this same needle is used to remove spines. Fragments are brittle and can be difficult to remove, but it is necessary to extract large fragments, due to the risk of granuloma development (Figure 9). Many fragments are expelled by a local inflammatory reaction. All the venomous animals of this phylum have thermolabile venom, making it appropriate to immerse the affected area in hot water, around 50ºC, for 30 to 90 minutes, especially if there is spontaneous pain.[10]

PHYLUM CRUSTACEA (Blue crabs, crabs, shrimps, prawns, barnacles, lobsters and mantis shrimp)

Crustaceans do not produce venom, but can cause severe allergic reactions and injuries from substances in their body.

Traumatic injuries are more common, especially lacerations caused by the claws. Allergic manifestations are not uncommon: contact dermatitis may emerge, as well as urticaria and anaphylactic reactions (Figure 10). The latter seem to be cross reactions associated with tropomyosins present in all crustaceans and astaxanthin, a pigment that gives the reddish color of shrimps, crabs, lobsters (crustaceans), salmon and flamingos.[2-5] Contact dermatitis is manifested by an acute eczematous process. Complications of some allergic diseases can be serious.[2-5] The use of antihistamines and topical corticosteroids controls contact dermatitis.

FIGURE 10

Urticaria caused by ingestion of shrimps. Eczematous process in a fisherman who cleans shrimps. Photos: Vidal Haddad Junior.

Traumatic injuries caused by crustaceans are not serious, but it is interesting to note that irritant dermatitis can be seen on the hands of those who clean shrimps and prawns, and it can be irritative and/or traumatic (Figure 10). Fishermen in the Southeast and Northern regions of Brazil fear the mantis shrimp, a large and aggressive crustacean (up to 30cm), whose sharp claws can cause serious injury to hands, and which has been named thumbsplit in parts of the Caribbean. Treatment for injuries caused by crustaceans is carried out through intense washing of the wound, a tetanus vaccination and topical or systemic antibiotics if infection occurs.

PHYLUM INSECTA (Giant water bugs)

Venomous aquatic insects are rare, but one can point to the Belostomatidae, carnivorous hemiptera, popularly known as giant water bugs (Figure 11). These animals live in freshwater environments and they hunt other arthropods, and even small fish and frogs. There are large species, such as Lethocerus delpontei, which can reach 10cm in length. Accidents caused by these animals have been reported, affecting particularly people who have contact with water streams. The bite inflicted by a proboscis provokes severe pain and in some cases, reversible paralysis of limbs can occur. Some studies associate the sting of these insects to Buruli ulcers, caused by Mycobacterium ulcerans. [2,33]

FIGURE 11

Insects of the Belastomatidae family (giant water bugs) are venomous and can cause painful accidents in humans. Photo: Vidal Haddad Junior

CONCLUSIONS

Injuries caused by aquatic animals are common and have occurred more frequently over the last decades, due to increasing contact between humans and aquatic environments. The animals' main characteristics and the clinical manifestations of trauma and envenomation, are summarized in the table 1, outlining first aid measures for hospitals and healthcare teams operating in areas where the problem exists.

TABLE 1

Algorithm for identification and treatment of injuries caused by aquatic animals (adapted from Haddad V Jr – Potentially Dangerous Aquatic Animals of Brazil: a medical and biologic guide. Editora Roca, São Paulo, 2008)

Puncture wounds			Skin eruptions		Lacerated wounds
Presence of stinger	Presence of local spines	Spines rarely present	Urticariform plaques, edema, erythema, vesicles,necrosis	Eczema	Cianotic or pale edges Fragments of stingers	Lacerations with pain proportional to the wound
**	*	**	**	*	**	*
Marine and freshwater catfish,mandis, stingrays	Sea urchins	Scorpionfish	Jellyfish, Portuguese men-of-war, corals, anemonas	Marine and freshwater sponges, marine worms, sea cucumbers	Marine and freshwater stingrays and catfish,(occasional puncture wounds)	Sharks, barracudas, moray eels, piranhas and other traumatogenic fish
		Toadfish
1=	1	1	2	2	1	3

Moderate pain

Intense pain

Immersion in hot water for 30-90 minutes (about 50 ºC)

Extraction of spicules and fragments of stings or glandular epithelium and infiltration of local anesthesic

Persistence of symptoms in later phases: radiological exam. Tetanus prophilaxy.

Wash the place or make compress with iced marine water (DON'T USE FRESHWATER!)

Apply vinegar (acetic acid): wash the place or make compress

Analgesy (dipirona 1 amp IM).

Intensive washing with research of fragments of bones and stings.

Antibioticoterapy and tetanus prevention.

# In all lacerated wounds, it is necessary the use of antibiotics:

Cephalexin 2,0g/day or Amoxicillin and Clavulanate potassium 1,5g/dia for 10 days.