Cercarial Dermatitis Transmitted by Exotic Marine Snail Sara V. Brant, Andrew N. Cohen, David James, Lucia Hui, Albert Hom, and Eric S. Loker Cercarial dermatitis (swimmer’s itch) is caused by the document an outbreak of human cercarial dermatitis in San penetration of human skin by cercariae of schistosome par- Francisco Bay that was related to the recent introduction of asites that develop in and are released from snail hosts. an exotic snail, the Japanese bubble snail Haminoea japon- Cercarial dermatitis is frequently acquired in freshwater ica Pilsbury 1895 (Cephalaspidea: Haminoeidae), which habitats, and less commonly in marine or estuarine waters. serves as the intermediate host of a schistosome that is re- To investigate reports of a dermatitis outbreak in San Fran- sponsible for the now annual dermatitis outbreaks. cisco Bay, California, we surveyed local snails for schisto- some infections during 2005–2008. We found schistosomes Cercarial dermatitis (swimmer’s itch) is caused by pen- only in Haminoea japonica, an Asian snail fi rst reported in etration of human skin with cercariae of schistosome para- San Francisco Bay in 1999. Genetic markers place this sites; the condition is common and recurrent in freshwater schistosome within a large clade of avian schistosomes but habitats worldwide. Adult schistosomes typically live in do not match any species for which there are genetic data. It mesenteric blood vessels of birds or mammals and produce is the second known schistosome species to cause dermati- eggs that pass from the host in feces. The eggs then hatch tis in western North American coastal waters; these species and release miracidia, which penetrate and develop in an are transmitted by exotic snails. Introduction of exotic hosts appropriate species of an intermediate snail host. Snail in- can support unexpected emergence of an unknown para- fections culminate in asexual production of numerous cer- site with serious medical or veterinary implications. cariae, which are regularly released into the water where they seek to penetrate the skin of a defi nitive vertebrate host. ne consequence of introduction of exotic species is Penner reported an association between human dermatitis Opossible establishment of new host–parasite associa- and a marine schistosome (13). He established that Litto- tions, potentially resulting in emergence of new diseases rina keenae Rosewater 1978 (Hypsogastropoda: Littorini- (1–3). Exotic parasites can be introduced into new loca- dae) syn. L. planaxis snails collected along the rocky shores tions along with their exotic host species (1,4), sometimes of southern California released schistosome cercariae that causing extinction of indigenous parasites (5). Newly in- caused dermatitis in experimentally exposed human vol- troduced parasites can extend their host ranges into related unteers. Documented cases (1,14–21) have been attributed indigenous host species (6,7), or exotic hosts may play new to species of Austrobilharzia Johnston 1917, the adults of roles in the transmission of indigenous parasites (8). Par- which most commonly infect gulls and shorebirds (14). asites newly supported by these exotic hosts can assume A cercarial dermatitis outbreak in San Francisco Bay considerable human or animal roles as emerging disease was reported in 1954 (1). The Bureau of Vector Control agents (9). of the California Department of Health Services identifi ed San Francisco Bay has been the site of numerous well- the cercariae as Austrobilharzia variglandis (Miller and documented introductions of exotic species (10–12). We Northrup 1926) collected from the eastern Atlantic mud- snail Ilyanassa obsoleta (Say 1822) (Hypsogastropoda: Nassariidae) syn. Nassarius obsoletus at Robert Crown Me- Author affi liations: University of New Mexico, Albuquerque, New morial Beach in 1955 and 1956 (1). I. obsoleta snails were Mexico, USA (S.V. Brant, E.S. Loker); Center for Research on accidentally introduced into San Francisco Bay in commer- Aquatic Bioinvasions, Richmond, California, USA (A.N. Cohen); cial shipments of Atlantic oysters and were observed in the and Alameda County Vector Control Services District, Alameda, bay in 1907 (10,11). A. variglandis schistosomes had been California, USA (D. James, L. Hui, A. Hom) identifi ed as the cause of cercarial dermatitis in coastal wa- DOI: 10.3201/eid1609.091664 ters in the northeastern United States (14). Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 9, September 2010 1357 RESEARCH After the 1954 outbreak, no additional cases of cer- carial dermatitis were reported in San Francisco Bay or elsewhere on the Pacifi c Coast until the summer of 2001 when 36 cases of cercarial dermatitis were reported at Crescent Beach in Surrey, British Columbia, Canada; 44 cases were reported in 2002 (20). The agent again ap- peared to A. variglandis schistosomes carried by I. ob- soleta snails, which are extremely abundant at Crescent Beach. The snail was accidentally introduced into British Columbia in the oyster trade and was fi rst observed in the region in 1952 (20). In June 2005, cercarial dermatitis appeared again in San Francisco Bay. The Alameda County Department of Environmental Health received ≈90 reports of skin irri- tation that occurred after water contact at Robert Crown Memorial Beach where the 1954 outbreak had occurred (The Swimmer Itch Hotline, www.acgov.org/aceh/recre- ational/beaches.htm). Although it was initially assumed that A. variglandis schistosomes, carried by I. obsoleta snails, were the causative agent, preliminary investigations suggested that the intermediate host involved was another exotic species, Haminoea japonica, from Asia. This snail was observed in San Francisco Bay in 1999 (22) and on the eastern shore of the bay, near Robert Crown Memorial Figure 1. San Francisco Bay area, California, USA (A), and locations Beach, in the summer of 2003, where it has become ex- where Haminoea japonica snails were obtained (B). tremely abundant (A.N. Cohen, unpub. data). We describe the morphologic and genetic features of cercariae obtained from H. japonica snails and discuss possible transmission pathways of this parasite in San Francisco Bay. virescens Sowerby 1833 snails collected in August 2005 from Friday Harbor, San Juan Island, Washington. Methods Snails were isolated singly or in groups of 5 in plastic containers in saline water (20–35 parts per thousand [ppt]) Specimen Collection and placed in natural light to induce cercarial shedding. For This study was conducted under the University of New each species, a subset of the larger snails was then dissect- Mexico Institutional Animal Care and Use Committee Pro- ed. Cercariae were photographed, and ethanol-preserved tocol 07UNM011, Animal Welfare Assurance # A4023-01. specimens were measured and compared with published Samples of H. japonica snails were collected by hand at low descriptions of schistosome cercariae. tide from 4 locations (Figure 1): Crab Cove at the north- Gulls are common hosts for schistosomes transmit- ern end of Robert Crown Memorial Beach (37°46′4.18′′N, ted by marine snails. We examined 29 gulls of 4 species 122°16′39.55′′W) in 2005–2008; the southern end of this collected at the Oakland International Airport, ≈7.5 miles beach (37°45′8.81′′N, 122°14′57.33′′W) in 2006 and 2008; southeast of Robert Crown Memorial Beach, as part of the Damon Slough (37°45′14.12′′N, 122°12′21.6′′W) in 2007; airport’s Wildlife Management Program. For each bird, the and Lake Merritt, a tidal lagoon connected to San Francisco mesenteric veins were examined, the intestine was opened, Bay (37°48′22.25′′N, 122°15′22.81′′W) in 2008. All gas- the muscosa was removed, and a sample from the intesti- tropod species observed at Robert Crown Memorial Beach nal wall was placed between 2 glass slides and examined were collected and examined for cercariae. H. japonica for schistosome adults or eggs in the villi (23). Feces were (Figure 2), Philine sp. (Cephalaspidea: Philinidae), and screened for eggs. I. obsoleta snails (all exotic) were collected on tide fl at sediments. The exotic oyster drill Urosalpinx cinerea (Say Sequencing and Phylogenetic Analysis 1822) (Sorbeoconcha: Muricidae) and the native peri- DNA was extracted from fresh or ethanol-preserved winkle Littorina spp. (L. scutulata Gould 1849 or L. plena cercariae, amplifi ed by PCR (Takara Ex Taq; Takara Bio- Gould 1849) were collected from exposed bulwarks and medicals, Otsu, Japan), and sequenced by using published other hard substrates. In addition, we examined native H. primers (24,25). PCR products were purifi ed on Montage 1358 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 16, No. 9, September 2010 Cercarial Dermatitis Transmitted by Marine Snail Life Cycle To obtain adult worms for species identifi cation, we experimentally exposed young parakeets and Gallus gal- lus L. chicks for 30 min to schistosome cercariae from H. japonica snails obtained from San Francisco Bay (Figure 3). Bird hosts were selected according to the method of Leigh (23), who described adult worms derived from cer- cariae from H. antillarum guadalupensis Sowerby snails in Florida. In experiment 1, eight chicks were exposed by standing each chick in salt water (35 ppt) containing cer- cariae. In experiment 2, six parakeets were exposed by ap- plying cercariae to their bare abdomens. In experiment 3, eight parakeets were exposed by standing each bird in salt water (35 ppt) containing cercariae. Figure 2. Haminoea japonica snail. Scale bar = 11 μm. Results Specimens Collected We identifi ed 1 species of schistosome in H. japonica Microcon columns (Millipore, Billerica, MA, USA). Se- snails that had a prevalence of 1.2% as determined by ob- quencing reactions were performed by using the BigDye servation of shedding and 8.7% as determined by dissec- Direct Sequencing Kit Version 3.1 (Applied Biosystems, tion (Table 1). No schistosomes were found in other snails Foster City, CA, USA). examined, including Littorina spp. and I. obsoleta, taxa Phylogenetic analyses of schistosomes obtained from that are known to host schistosomes in California (1,13).