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Skin Problems Related to Noninfectious Coastal Microorganisms

Skin Problems Related to Noninfectious Coastal Microorganisms

Dermatologic Therapy, Vol. 15, 2002, 10±17 Copyright # Blackwell Publishing, Inc., 2002 Printed in the Á All rights reserved DERMATOLOGIC THERAPY ISSN 1396-0296 Skin problems related to noninfectious coastal microorganisms

y WILLIAM A. BURKE* & PATRICIA A. TESTER *Department of Dermatology, Brody School of Medicine, East Carolina University, Greenville, , and yNational Ocean Service, National Oceanic and Atmospheric Administration, Center for Coastal and Habitat Research, Beaufort, North Carolina

ABSTRACT: While there are a number of coastal microorganisms that can cause infections of the skin, there are many that can cause skin problems that are noninfectious in nature. From cyanobacterial dermatitis to skin problems related to , to skin signs of ciguatera or scombroid poisonings, to ``sea lice''/``seabather's eruption,'' to ``swimmer's itch,'' this article attempts to separate these entities into distinct syndromes caused by a variety of bacteria, and . Treatment and prevention of these diseases are also discussed.

KEYWORDS: bites and stings, , , Dinoflagellata, marine , piscicida, schistosomatidae.

There are many noninfectiouscutaneous Cyanobacteria (blue-green algae) problemsthat are causedby aquatic microor- ganisms such as bacteria, phytoplankton, and Cyanobacteria (blue-green algae) are prokaryotic, zooplankton. While some of these problems are chlorophyll-containing, microscopic filamentous relatively insignificant and require only sympto- and nonfilamentous organisms found in fresh- matic care and reassurance, a few may be fatal. water, estuarine, and marine environments. These It isimportant for cliniciansto recognize the organisms proliferate in areas of high nutrient varied signs and symptoms of these diseases overload and can form blue-green, milky-blue, based on a proper history and physical exam- green, red, or dark-brown ``blooms'' or ``scums'' (1). ination, as well as having a basic understanding While not all cyanobacteria are toxic, some of the causative microscopic flora and fauna. species such as Lyngbya, Microcystis, Anabaena, Skin problemsrelated to bacterial skin infections Aphanizomenon, Cylindrospermopsis, Nodularia, are covered elsewhere in this issue, and only and Oscillatoria/Trichodesmium (Fig. 1) have noninfectious microorganisms will be discussed been shown to produce toxins which may be here. relatively harmful (1±4). These toxins can be hazardousto and health and have been responsible for sporadic animal (, birds, fish) fatalities (5). Cyanobacterial toxins may be tumor promoters, hepatotoxins, neuro- Address correspondence and reprint requests to: William A. Burke, MD, Department of Dermatology, Brody School of toxins, or skin irritants (6,7). Medicine, East Carolina University, 600 Moye Blvd., Brody 3E- Human illness related to cyanobacteria and 113, Greenville, NC 27858-4354, or e-mail: burkew@mail. their toxinsmay be via direct contact (recrea- ecu.edu. tional or other) or ingestion (of water, fish, or

10 Noninfectious coastal microorganisms

presumptive diagnosis. Recreational and occupa- tional exposure as well as possible ingestion need to be considered. There isno proven therapy for cyanobacterial . Treatment of systemic disease is with supportive care, and symptomatic care with antihistamines and topical steroid creams is often used for the cutaneous component (11,12). Re- moval of the bathing suit and showering quickly after leaving the water isimportant in prevention of the dermatitis. Eye stings should be treated with irrigation with tap water followed by ophthalmologic consultation (11). Fig. 1. Filaments of Trichodesmium, a cyanobacter- Skin stings and rashes from cyanobacteria have ium (blue-green alga) (original magnification 200Â). been given many names: ``algae dermatitis,'' ``seabather's eruption,'' ``stinging limu,'' and ``sea- weed dermatitis.'' To avoid confusion, it seems shellfish). In a hemodialysis unit in Brazil, 126 reasonable to term skin eruptions due to toxic patients became seriously ill and 60 of them died cyanobacteria simply ``cyanobacterial dermatitis.'' when water from a lake contaminated with cyanobacterial toxins(microcystins)wasusedat the unit (8). Deathswere primarily from liver Estuarine and marine phytoplankton failure, and ecchymoses were seen in some of these patients (8). Unicellular eukaryotic phytoplankton can cause Skin reactionsfrom cyanobacterial toxinswere skin reactionsÐsome when ingested and some on initially reported from the organism Lyngbya skin contact. A variety of intoxications may occur majuscula, which secretes lyngbyatoxins which when variousendotoxin-producing marine phy- can be irritating to skin and mucous membranes, toplankton (dinoflagellates, as well as a marine causing irritant dermatitis and conjunctivitis ) are filtered and concentrated by (9,10). Thisfilamentousorganismbloomsinto shellfish and later ingested by people. These algal matswhich cover surface waterswhen a shellfish poisoning syndromes include paralytic high nutrient load occurs. Periods of high winds shellfish poisoning, neurotoxic shellfish - and flooding rains can cause these mats to flow ing, amnesic shellfish poisoning, and diarrhetic into coastal and estuarine waters where wave shellfish poisoning. While these intoxications can action breaksthe matsapart into individual be severe and some may lead to death, they microscopic filaments. Bathing suits on persons generally do not affect the skin (13±15). swimming in affected waters filter and collect is caused by eating microscopic -secreting cyanobacterial fila- fish which have bioconcentrated the tropical/ ments under the suits. As the swimmer leaves subtropical epiphytic reef-associated Gambierdis- the water and the water from the bathing suit cus toxicus in their tissue. Several evaporates, toxins are concentrated and skin other epiphytic dinoflagellateshave alsobeen irritation (at timeswith blistering)may occur, implicated. With approximately 50,000 cases most commonly in areas covered by the bathing annually throughout the world, this disease has suit. Eye stings and conjunctivitis have also been become the most common illness related to reported (11). consumption of finfish, primarily due to exporta- Blistering skin reactions around the mouth tion of fish from tropical/subtropical areas to have also been reported possibly due to micro- other partsof the world (16,17). Fishcommonly cystins after contact with water containing toxic implicated include mackerel, jacks, coral trout, Microcystis aeruginosa (12). Affected individuals barracuda, grouper, flowery cod, snapper, reef had many other signs and symptoms, including sharks, moray eel, , and others (16±21). malaise, fever, cough, pleuritic chest pain, ab- Ciguatoxin, maitotoxin, and other toxins asso- dominal pain, nausea, vomiting, confusion, and ciated with G. toxicus are lipid soluble and cold/ pneumonia. It isimportant to take a careful heat stable. history when a patient presents with possible Ciguatera poisoning usually presents within cyanobacterial skin eruptions in order to make a 3±6 hours after ingestion as gastroenteritis

11 Burke & Tester

(diarrhea, abdominal pain, nausea, and vomiting) and neurologic symptoms (weakness, headache, tremor, ataxia) (20,21). Paresthesia of the extre- mitiesand circumoral area aswell ashot-cold temperature reversal are symptoms frequently seen in ciguatera toxicity, and can help separate this illness from other causes of gastroenteritis. Skin problemsinclude severe pruritus(which isa common complaint and which can last for years) (16) and rarely chronic urticaria. Death isquite rare, but may occur due to cardiopulmonary arrest. Treatment of the acute toxicity iswith mannitol infusion (1 g/kg intravenously over 30±45 minutes) (22,23). Chronic symptoms are treated with ami- Fig. 3. Sea surface temperature satellite imageryof triptyline, , , , and the Gulf Stream (dark red) which serves as a method (24±27). of transport to distribute Karenia brevis blooms from the Gulf of Mexico to the U.S. South Atlantic Bight. Another dinoflagellate, Karenia brevis (pre- (Photo courtesyof NOAA.) viously known as Gymnodinium breve) (Fig. 2), can develop into huge bloomscalled ``red tides,'' because of the reddish discoloration it causes in Unlike most dinoflagellates, K. brevis isa affected water. Thisorganismproducesendotox- ``naked'' dinoflagellate and lackspolysaccharide ins that have been classified as . These protective plates of armor. Because of this, heavy toxins can cause massive fish kills, and when wave action and surf can cause its cell mem- filtered and concentrated by shellfish and then branesto rupture, thereby releasingand aero- ingested, neurotoxic shellfish poisoning. K. brevis solizing the endotoxins (29). As the toxins are very migrate to the upper part of the water column and irritating to skin and mucous membranes, it can are transported throughout the Gulf of Mexico cause an irritant dermatitis, conjunctivitis, phar- and the U.S. South Atlantic Bight by major current yngitis, rhinorrhea, sneezing, coughing, and dys- systems (Fig. 3) (28). pnea (17,29). As the toxins also cause smooth muscle contraction, wheezing and asthma may also occur, and this can be a major problem for persons who have already been diagnosed with asthma (30±32). Asthere isno effective treatment for skinand mucousmembrane problemsrelated to K. brevis (except for symptomatic care), avoidance and removal of oneself away from the beach is the best course, as symptoms are quickly reversed. Induced asthmatic attacks are treated with bronchodilators. Another dinoflagellate that hasbeen recently implicated as causing symptoms and skin lesions in humansis (Fig. 4). Discov- ered in 1988 in a university laboratory as a cause of fish kills (33), workers working with cultures of thisorganismreported problemswith concentra- tion and memory, emotional lability, and skin lesions, as well as variety of other symptoms (34). Variouslife cycle stagesarepurported to be toxin producing. Unlike other dinoflagellates, Pfiesteria Fig. 2. Karenia breve, a ``naked dinoflagellate,'' is the isreported to secrete exotoxinsthat enter the primarycausative agent of the ``'' blooms. water, but are not thought to enter the food chain. (Photo courtesyof Steve Kibler, National Oceanic While the lay press has spread much misinfor- Service, NOAA.) mation about Pfiesteria causing skin ulcerations

12 Noninfectious coastal microorganisms

and mid-Atlantic United States, and will hope- fully shed some light on this controversial topic in the near future (38). There is no known treatment for possible Pfiesteria/PCO-related illness. Symptoms of ``burning'' when exposed to estuarine waters resolve rapidly with washing with tap water or within 12 hourswithout treatment (36). Useof visual contrast as a screening tool for Pfiesteria/ PCO-related illness (39) and use of cholestyra- mine in treatment (39±41) should currently be viewed asanecdotal.

Fish poisonings and the skin

Ciguatera is a major cause of fish poisoning in , but as it is due to a toxic dinoflagellate, it Fig. 4. Scanning electron micrograph of the hetero- is discussed above. Another common cause of fish trophic dinoflagellate Pfiesteria piscicida.Ventral poisoning which can affect the skin is termed view of planozygote. (Photo courtesy of Dr. Karen A. scombroid poisoning or histamine fish poisoning. Steidenger, Florida Marine Research Institute.) Thissyndromeiscausedby bacteria which contain the enzyme histadine decarboxylase and which proliferate in improperly stored histadine- and sores in humans, scientific data is lacking. In rich fish. These bacteria break down histadine to a study (35) of persons felt to possibly histamine which, when ingested, leads to a have a Pfiesteria-related illness, a variety of skin histamine intoxication syndrome (42). Fish im- ailmentswere identified, but mostwere thought plicated in histamine poisoning include tuna, to be unrelated to Pfiesteria exposure (36). A few bonito, albacore, mackerel, wahoo, sardines, cases of erythematous papules and patches that anchovies, herring, dolphin fish (mahi mahi), were nondiagnostic were of a mild nature. One amberjack, yellowtail, redfish, bluefish, marlin, symptom that appeared to be significant was the and (42±45). Degradation of histadine sensation of skin ``burning'' on contact with generally occurswhen the fishare not properly water (36). chilled after being caught. Rapid chilling of fish on Several other dinoflagellates, such as crypto- the vessel and keeping the temperature peridiniopsoid species ``brodyi,'' Pfiesteria lower than 0C throughout itsdistributionis schumwayae, and others, appear similar to the best way to prevent unwanted histamine P. piscicida when visualized with a light micro- scope, and this group of organisms has been termed Pfiesteria-complex organisms (PCOs). Whether some of these PCOs are capable of Table 1. CDC criteria for possible - causing human health problems is currently associated syndrome (PEAS) (37) under investigation. Persons are considered to have PEAS if: In order to study illnesses in humans possibly 1. They report developing symptoms within 2 weeks due to Pfiesteria and PCOs, a set of criteria for after exposure to estuarine water. what is now termed ``possible estuary-associated 2. They report memory loss or confusion of any syndrome'' (PEAS) has been established by the duration and/or three or more selected symptoms Centers for Disease Control (CDC) (Table 1) (i.e., headache, skin rash at the site of water contact, (37). Currently Pfiesteria/PCO toxinshave not sensation of burning skin, eye irritation, upper been identified, isolated, or purified in quantities respiratory irritation, muscle cramps, and gastroin- that would allow for diagnostic testing. Because testinal symptoms) that, with the exception of skin of this, proof that PEAS is a real syndrome rash at the site of water contact and sensation of caused by this group of dinoflagellates is burning skin, persist for 2 weeks or more. currently not available. A six-state prospective 3. A health care provider cannot identify another cause for the symptoms. study of this is in progress in the southeastern

13 Burke & Tester formation (45). Once formed, histamine is heat stable and is not affected by cooking. Symptoms of histamine poisoning occur 30±60 minutes after ingestion and include flushing, abdominal cramps, diarrhea, headache, hyperhi- drosis, urticaria, pruritus, heart palpitations, nau- sea, vomiting, angioedema, and rarely, broncho- spasm. Transient visual loss has also been reported (46). Death israre but may occur. This syndrome may be misdiagnosed as anaphylaxis, monosodium glutamate sensitivity, ciguatera poi- soning, allergy, and Salmonella infection (42,44). Treatment of histamine fish poisoning is, as one would expect, with antihistamines, both H1 (, hydroxyzine, ) and H2 antagonists (cimetadine, ranitidine). Sub- cutaneousepinephrine, bronchodilators,and systemic corticosteroids may occasionally be needed. Without treatment, the disease is usually self-limiting and subsides within 8±12 hours. There are many other types of fish poisoning, including pufferfish, ichthyotoxic, hallucinatory, Haff disease, clupeoid, ichthyohemotoxic, barra- Fig. 5. A crab zoea, which contains sharp spicules cuda, and others (47). These diseases only rarely that can irritate human skin. affect the skin and are beyond the scope of this article. concern to bathers. These organisms are generally fish parasites or feed on dead decaying plant material. Estuarine and marine zooplankton The microscopic larvae of cnidarians can cause (``sea lice,'' ``seabather's eruption'') stinging sensations while swimming in waters where these occur. Larvae of some , sea Estuarine/marine zooplankton from a variety of anemones, and even small hydroids have been phyla can cause pruritic, bitelike or stinging suggested as causative and, like cyanobacterial sensations of the skin of people in the water. dermatitis, this has also been termed ``sea lice'' Often collectively termed ``sea lice'' or ``sea- and ``seabather's eruption'' (52±56). Lesions can bather's eruption,'' these reactions are usually vary from erythematousmaculesand papules caused by a wide and diverse group of micro- (Fig. 6) to vesicular or urticarial reactions. These organisms. Some marine zooplankton such as usually begin 2±24 hours after exposure. Depend- some crab larvae have sharp spines (Fig. 5) (48), ing on the causative organism, both covered and which, when concentrated by filtering in a bathing uncovered areas of skin may be affected. The rash suit, can lead to pruritus and skin irritation similar and pruritus usually lasts for 3±7 days, with more to a fiberglass dermatitis (49,50). Microscopic severe cases lasting up to 6 weeks (57). Occasion- copepodsaswell astiny isopodsand amphipods ally, systemic reactions may occur with nausea, can also cause pruritus if large numbers are vomiting, diarrhea, malaise, headache, weakness, filtered by the bathing suit and then the person myalgias, arthralgias, and, especially in children, leaves the water. In addition, some isopods and fever. cymothoidscontain strongbiting mouth partsas The eruption usually begins with a stinging or well aschitinoussetaeon their legswhich allow ``prickly'' sensation while in the water. The them to closely adhere to human skin while biting (Linuche unguiculata) aswell as (51). While thisisrelatively insignificant and feels a sea anemone larva (Edwardsiella lineata) have like the bite of a gnat or biting fly, it can lead to been implicated (52±58). While some of the erythematoushemorrhagic lesionsand may be of stinging sensation in the water might be due to

14 Noninfectious coastal microorganisms

Cercarial dermatitis (``swimmer's itch,'' ``clam-diggers itch,'' ``duck itch'')

Morecommonlyseeninfreshorbrackish water, cercarial dermatitisiscausedby micro- scopic cercarial flatworms, which can be pre- sent in the water in large numbers and can penetrate human skin. These larvae have difficulty penetrating cloth, and the resulting rash is therefore found primarily on uncovered areas of skin (Fig. 7). Waterfowl (especially ducks and geese), as well as some mammals, are the usual hosts for these parasitic flat- worms. Their ciliated miracidia parasitize aqua- tic snails, which are usually found in areas of abundant aquatic vegetation (61). The flatwormsattach themselvesto human skin via a sucker and often begin their penetration into the skin as the skin dries after leaving the water (47). Cutaneousirritation beginsasa ``prickly'' sensation in affected areas, and pruritus worsens as the cercariae burrow further into the skin. As man is an accidental host when animal schistosomes invade the skin, the parasite dies (usually within 24±48 hours). In animal cercarial dermatitis, a papular eruption occurs at the site of penetration and may disappear over days, or the Fig. 6. ``Sea lice'' or ``seabather's eruption'' can be patient may develop an intensely pruritic papular caused bya wide varietyof aquatic microorganisms or papulovesicular eruption, which is thought to and mayinvolve covered or uncovered areas of be due to a delayed hypersensitivity reaction. The skin. rash may last weeks and then resolve (61,62). The pruritic rash may be more severe with repeated exposure, but is only very rarely associated with nematocyst activation, immunologic hypersensi- systemic symptoms or fever (61). tivity may also occur, as sera from affected persons may show specific reactivity to the organism (59). Risk factors for developing this condition include young age (less than 16 years), prior history of a similar rash, and surfing (60). Jellyfish tentacles which have been broken apart by wave action during storms can also cause stinging sensations and a rash. This has also been termed ``sea lice.'' Removal of the bathing suit and showering as soon as possible after leaving the water can be helpful in prevention. Use of specific topical lotionsand protective barrier creamscan, at this point, be viewed asonly anecdotal. Otherwise treatment is generally symptomatic with antihis- tamines and -containing lotions. In cases Fig. 7. Cercarial dermatitis is caused bymicroscopic with severe itching, immunologic mechanisms flatworms that have difficultypenetrating cloth, and may play a role, and use of topical and even the cutaneous eruption typically involves uncovered systemic steroids may be helpful. areas of skin.

15 Burke & Tester

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