Cercarial Dermatitis, a Neglected Allergic Disease

Appleton CC, Lethbridge RC (1979) Schistosome dermatitis in the swan estuary, Western Australia. Med J Aust 131:141–145 Oda T (1973) Schistosome dermatitis in Japan. In: Morishita K, Komiya Y, Matsubayashi H (eds) Progress in medical parasitology in Japan, vol. 2. Meguro Parasitological Museum, Tokyo, pp 5–53 Cort WW (1928) Schistosome dermatitis in the United States (Michigan). JAMA 90:1027–1029 Matheson S (1930) Notes on Cercaria elvae Miller as the probable cause of an outbreak of dermatitis in Cardiff. Trans R Soc Trop Med Hyg 23:421 Brumpt E (1931) Cercaria ocellata, déterminant la dermatite des nageurs, provient d'une bilharzie des canards. C R Hebd Seances Acad Sci 193:612–614 Vogel H (1930) Zercarien-Dermatitis in Deutschland. Klin Wochenschr 9:883–886 Desportes C (1945) La dermatite des nageurs. Ann Parasitol Hum Comp 20:263–278 Buckley JJC (1938) On dermatitis in Malaya caused by the cercariae of Schistosoma spindale Montgomery, 1906. J Helminthol 16:117–120 Majoros G, Dán Á, Erdélyi K (2010) A natural focus of the blood fluke Orientobilharzia turkestanica (Skrjabin, 1913) (Trematoda: Schistosomatidae) in red deer (Cervus elaphus) in Hungary. Vet Parasitol 170:218–223 Christensen RO, Greene WP (1928) Studies on biological and medical aspects of ”swimmer's itch. Schistosome dermatitis in Minnesota. Minn Med 11:573–575 Skírnisson K, Kolářová L (2005) Swimmer's itch in Landmannaugar, Iceland. Laeknabladid 91:729–736 Kolářová L (2007) Schistosomes causing cercarial dermatitis: a mini-review of current trends on systematics and host specificity and pathogenicity. Folia Parasitol 54:81–87 Neuhaus W (1952) Biologie und Entwicklung von Trichobilharzia szidati n. sp. (Trematoda, Schistosomatidae), einem Erreger von Dermatitis beim Menschen. Z Parasitenkd 15:203–266 Brachs S, Haas W (2008) Swimming behaviour of Schistosoma mansoni cercariae: responses to irradiance changes and skin attractants. Parasitol Res 102:685–690 Haas W (2003) Parasitic worms: strategies of host finding, recognition and invasion. Zoology 106:349–364 Haeberlein S, Haas W (2008) Chemical attractans of human skin for swimming Schistosoma mansoni cercariae. Parasitol Res 102:657–662 Grabe K, Haas W (2004) Navigation within host tissues: cercariae orientate towards dark after penetration. Parasitol Res 93:111–113 Grabe K, Haas W (2004) Navigation within host tissues: Schistosoma mansoni and Trichobilharzia ocellata schistosomula respond to chemical gradients. Int J Parasitol 34:927–934 Haas W, Diekhoff D, Koch K, Schmalfuss G, Loy C (1997) Schistosoma mansoni cercariae: stimulation of acetabular gland secretion is adapted to the chemical composition of mammalian skin. J Parasitol 83:1079–1085 Haas W, Grabe K, Geis C, Päch T, Stoll K, Fuchs M, Haberl B, Loy C (2002) Recognition and invasion of human skin by Schistosoma mansoni cercariae key-role of L-arginine. Parasitology 124:153–167 Haas W, Haeberlein S, Behring S, Zoppelli E (2008) Schistosoma mansoni: human skin ceramides are chemical cue for host recognition of cercariae. Exp Parasitol 120:94–97 Haas W, van de Roemer A (1998) Invasion of the vertebrate skin by cercariae of Trichobilharzia ocellata: penetration processes and stimulating host signals. Parasitol Res 84:787–795 Haas W, Haeberlein S (2009) Penetration of cercariae to living human skin: Schistosoma mansoni vs. Trichobilharzia szidati. Parasitol Res 105:1061–1066 Salter JP, Lim C, Hansell E, Hansell E, Hsieh I, McKerrow JH (2000) Schistosome invasion of human skin and degradation of dermal elastin are mediated by a single serine protease. J Biol Chem 275:38667–38673 Dvořák J, Mashiyama ST, Brasdchi S, Sajid M, Knudsen GM, Hansell E, Lin K-C, Hsieh I, Baghgat M, Mackenzie B, Mezihradský KF, Babbitt PC, Caffrey CR, McKerrow JH (2008) Differential use of protease families for invasion by schistosome cercariae. Biochimie 90:345–358 Kašný M, Mikeš L, Dalton JP et al (2007) Comparison of cysteine peptidase activities in Trichobilharzia regenti and Schistosoma mansoni cercariae. Parasitology 134:1599–1609 Kašný M, Mikeš L, Hampl V, Dvořák J, Caffrey CR, Dalton JP, Horák P (2009) Chapter 4. Peptidases of trematodes. Adv Parasitol 69:205–297 Kašný M, Mikeš L, Dolečková K, Hampl V, Dvořák J, Horák P (2011) Cathepsins B1 and B2 of Trichobilharzia spp., bird schistosomes causing cercarial dermatitis. Adv Exp Med Biol 172:136–154 Mikeš L, Zídková L, Kašný M, Dvořák J, Horák P (2005) In vitro stimulation of penetration gland emptying by Trichobilharzia szidati and T. regenti (Schistosomatidae) cercariae. Quantitative collection and partial characterization of the products. Parasitol Res 96:230–241 Salter JP, Choe Y, Albrecht H, Franklin C, Lim K-C, Craik CS, McKerrow JH (2002) Cercarial elastatase is encoded by a functionally conserved gene family across multiple species of schistosomes. J Biol Chem 277:24618–24624 Dolečková K, Kašný M, Mikeš L, Cartwright J, Jedelský P, Schneider EL, Dvořák J, Mountford AP, Craik CS, Horák P (2009) The functional expression and characterisation of a cysteine peptidase from the invasive stage of the neuropathogenic schistosome Trichobilharzia regenti. Int J Parasitol 39:201–211 Dolečková K, Albrecht T, Mikeš L, Horák P (2010) Cathepsins B1 and B2 in the neuropathogenic schistosome Trichobilharzia regenti: distinct gene expression profiles and presumptive roles throughout the life cycle. Parasitol Res 107:751–755 Horák P, Kovář L, Kolářová L, Nebesářová J (1998) Cercaria-schistosomulum surface transformation of Trichobilharzia szidati and its putative immunological impact. Parasitology 116:139–147 Basch PF (1991) Schistosomes: development, reproduction and host relations. Oxford University Press, Oxford, p 248 Chanová M, Vuong S, Horák P (2007) Trichobilharzia szidati: the lung phase of migration within avian and mammalian hosts. Parasitol Res 100:1243–1247 Morales GA, Helmboldt CF, Penner LR (1971) Pathology of experimentally induced schistosome dermatitis in chickens: the role of Ornithobilharzia canaliculata (Rudolphi 1818) Odhner, 1912 (Trematoda: Schistosomatidae). Avian Dis 15:262–276 Wood LM, Bacha WJ Jr (1983) Distribution of eggs and the host response in chickens infected with Austrobilharzia variglandis (Trematoda). J Parasitol 69:682–688 Horák P, Kolářová L, Dvořák J (1998) Trichobilharzia regenti n. sp. (Schistosomatidae, Bilharziellinae), a nasal schistosome from Europe. Parasite 5:349–357 Hrádková K, Horák P (2002) Neurotropic behaviour of Trichobilharzia regenti in duck and mice. J Helminthol 76:137–141 Horák P, Dvořák J, Kolářová L, Trefil L (1999) Trichobilharzia regenti, a pathogen of the avian and mammalian central nervous systems. Parasitology 119:577–581 Lichtenbergová L, Lassmann H, Jones MK, Kolářová L, Horák P (2011) Trichobilharzia regenti: host immune response in the pathogenesis of neuroinfection in mice. Exp Parasitol 128:328–335 Chamot E, Toscani L, Rougemont A (1998) Public health importance and risk factors for cercarial dermatitis associated with swimming in Lake Leman at Geneva, Switzerland. Epidemiol Infect 120:305–314 Bechtold S, Wintergerst U, Butenandt O (1997) Badedermatitis durch Zerkarien. Monatsschr Kinderheilkd 145:1170–1172 Olivier L (1949) Schistosome dermatitis, a sensitization phenomenon. Am J Hyg 49:290–302 Horák P, Kolářová L, Adema CM (2002) Biology of the schistosome genus Trichobilharzia. Adv Parasitol 2:155–233 Kolářová L, Gottwaldová V, Čechová D, Ševcová M (1989) The occurrence of cercarial dermatitis in Central Bohemia. Zentralbl Hyg Umweltmed 189:1–13 Macfarlane WV (1949) Schistosome dermatitis in New Zealand. Part II. Pathology and immunology of cercarial lesions. Am J Hyg 50:152–167 Bayssade-Dufour C, Martins C, Vuong PN (2001) Histopathologie d'un modèle mammifère et dermatite cercarienne humaine. Med Mal Infect 31:713–722 Bayssade-Dufour C, Vuong PN, René M, Martin-Loehr C, Martins C (2002) Visceral lesions in mammals and birds exposed to agents of human cercarial dermatitis. Bull Soc Pathol Exot 95:229–237 Blažová K, Horák P (2005) Trichobilharzia regenti: the developmental differences in natural and abnormal hosts. Parasitol Int 54:167–172 Haas W, Pietsch U (1991) Migration of Trichobilharzia ocellata schistosomula in the duck and in the abnormal murine host. Parasitol Res 77:642–644 Horák P, Kolářová L (2000) Survival of bird schistosomes in mammalian lungs. Int J Parasitol 30:65–68 Kouřilová P, Hogg KG, Kolářová L, Mountford AP (2004) Cercarial dermatitis caused by bird schistosomes comprises both immediate and late phase cutaneous hypersensitivity reactions. J Immunol 172:3766–3774 Kouřilová P, Syrůček M, Kolářová L (2004) The severity of mouse pathologies caused by the bird schistosome Trichobilharzia regenti in relation to host immune status. Parasitol Res 93:534–542 Olivier L (1953) Observations on the migrations of avian schistosomes in mammals previously unexposed to cercariae. J Parasitol 39:237–243 Kolářová L, Horák P, Čada F (2001) Histopathology of the CNS and nasal infections caused by Trichobilharzia regenti in vertebrates. Parasitol Res 87:644–650 Batten PJ (1956) The histopathology of swimmer's itch. I. The skin lesions of Schistosomatium douthitti and Gigantobilharzia huronensis in the unsensitized mouse. Am J Pathol 32:363–377 Haemmerli U (1953) Schistosomen-Dermatitis am Zürichsee. Dermatologica 107:302–341 Gay P, Bayssade-Dufour C, Grenouillet F et al (1999) Étude expérimentale de dermatites cercariennes provoquées par Trichobilharzia en France. Med Mal Infect 29:629–637 Akdis M, Palomares O, Veen W et al (2012) TH17 and TH22 cells: a confusion of antimicrobial response with tissue inflammation versus protection. J Allergy Clin Immunol 129(6):1438–1449 Lichtenbergová L, Kolbeková P, Kouřilová P, Kašný M, Mikeš L, Haas H, Schramm G, Horák P, Kolářová L, Mountford AP (2008) Antibody responses induced by Trichobilharzia regenti antigens in murine and human hosts exhibiting cercarial dermatitis. Parasite Immunol 30:585–595 Khalil LF (2002) Family Schistosomatidae Stiles and Hassall, 1898. In: Gibson DI, Jones A, Bray RA (eds) Keys to the trematoda, vol. 1. CAB International, Wallingford and The Natural History Museum, London, pp 419–432 Ruth F (2010) Heterobilharzia americana infection and glomerulonephritis in a dog. Am Anim Hosp Assoc 46:203–208 Hoeffler DF (1977) Swimmers' itch (cercarial dermatitis). Cutis 19:461–467 Freudenthal AR, Barbagallo JS (2002) Ghost anemone dermatitis. J Am Acad Dermatol 47:722–726 Freudenthal AR, Joseph PR (1993) Seabather's eruption. N Engl J Med 329:542–544 Appleton CC (1984) Schistosome dermatitis—an unrecognized problem in South Africa? S Afr Med J 65:467–469 Malek EA, Armstrong JC (1967) Infection with Heterobilharzia americana in primates. AmJTrop Med Hyg 16:708–714 Wiedermann G, Aspöck H, Graefe G, Picher O, Peham P (1973) Hauttests mit Schistosoma mansoni-Antigen bei Fällen von Cercarien-Dermatitis. Zentralbl Bakteriol Mikrobiol Hyg A 224:128–132 Kouřilová P, Kolářová L (2002) Variations in immunofluorescent antibody response against Trichobilharzia and Schistosoma antigens in compatible and incompatible hosts. Parasitol Res 88:513–521 Brant SV, Bochte CA, Loker ES (2011) New intermediate host records for the avian schistosomes Dendritobilharzia pulverulenta, Gigantobilharzia huronensis and Trichobilharzia querquedulae from North America. J Parasitol 97:946–949 Jouet D, Ferté H, Depaquit J, Rudolfová J, Latour P, Zanella D, Kaltenbach ML, Léger N (2008) Trichobilharzia spp. in natural conditions in Annecy Lake, France. Parasitol Res 103:51–58 Jouet D, Ferté H, Hologne C, Kaltenbach ML, Depaquit J (2009) Avian schistosomes in French aquatic birds: a molecular approach. J Helminthol 83:181–189 Nassi H (1987) Sur quatre furcocercaires émises par Biomphalaria glabrata en Guadeloupe. Ann Parasitol Hum Comp 62:17–35 Horák P, Kolářová L (2011) Snails, waterfowl and cercarial dermatitis. Freshw Biol 56:779–790 Aldhoun JA, Faltýnková A, Karvonen A, Horák P (2009) Schistosomes in the north: a unique finding from a prosobranch snail using molecular tools. Parasitol Int 58:314–317 Aldhoun JA, Kolářová L, Horák P, Skírnisson K (2009) Bird schistosome diversity in Iceland: molecular evidence. J Helminthol 83:173–180 Athari A, Goha-Dehi S, Rostami-Jalilian M (2006) Determination of definitive and intermediate hosts of cercarial dermatitis-producing agents in Northern Iran. Arch Iran Med 9:11–15 Brant SV, Loker ES (2009) Molecular systematics of the avian schistosome Trichobilharzia (Trematoda: Schistosomatidae) in North America. J Parasitol 95:941–963 Cipriani P, Mattiuci S, Paoletti M, Scialanca F, Nascetti G (2011) Molecular evidence of Trichobilharzia franki Muller and Kimmig, 1994 (Digenea: Schistosomatidae) in Radix auricularia from Central Italy. Parasitol Res 109:935–940 Coady NR, Muzzall PM, Burton TM, Snider RJ, Saxton J, Sergeant M, Sommers A (2006) Ubiquitous variability in the prevalence of Trichobilharzia stagnicolae (Schistosomatidae) infecting Stagnicola emarginata in three northern Michigan lakes. J Parasitol 92:10–15 Farahnak A, Essalat M (2003) A study on cercarial dermatitis in Khutestan province, south western Iran. BMC Publ Health 7:1–4 Ferté H, Depaquit J, Carré S, Villena I, Léger N (2005) Presence of Trichobilharzia szidati and T. franki in Radix auricularia in northeastern France: molecular evidence. Parasitol Res 95:150–154 Fraser SJ, Allan SJ, Roworth M, Smith HV, Holme SA (2009) Cercarial dermatitis in the UK. Clin Exp Dermatol 34:344–346 Guo J, Li CP, Wang KX (2007) Survey on natural nidus of Trichobilharzia in Huainan area. Chin J Parasitol Paras Dis 25:60–61 Jouet D, Skírnisson K, Kolářová L, Ferté H (2010) Final hosts and variability of Trichobilharzia regenti under natural conditions. Parasitol Res 107:923–930 Karamian M, Aldhoun JA, Maraghi S, Hatam G, Farhangmehr B, Sadjjadi SM (2011) Parasitological and molecular study of the furcocercariae from Melanoides tuberculata as a probable agent of cercarial dermatitis. Parasitol Res 108:955–962 Korsunenko AV, Chrisanfova GG, Ryskov AP, Movsessian SO, Vasilyev VA, Semyenova S (2010) Detection of European Trichobilharzia schistosomes (T. franki, T. szidati, and T. regenti) based on novel genome sequences. J Parasitol 96:802–806 Lopatkin AA, Khrisanfova GG, Voronin MV, Zazornova OP, Beér SA, Semenova SK (2010) Polymorphism of the cox1 gene in bird schistosome cercaria isolates (Trematoda, Schistosomatidae) from ponds of Moscow and Moscow oblast. Genetika 46:981–999 Moema EB, King PH, Baker C (2008) Cercariae developing in Lymnaea natalensis Krauss, 1848 collected in the vicinity of Pretoria, Guateng Province, South Africa. Onderstepoort J Vet Res 75:215–223 Sheng SC, Qin ZH, Zhang MQ, Tai Y, Ni SG, Wen JY (2004) Preliminary study on the ecology of Trichobilharzia cercariae in the Huaihe river system. Chin J Parasitol Paras Dis 22:349–352 Soleng A, Mehl R (2011) Geographical distribution of cercarial dermatitis in Norway. J Helminthol 85:345–352 Schets FM, Lodder WJ, de Roda Husman AM (2010) Confirmation of the presence of Trichobilharzia by examination of water samples and snails following reports of cases of cercarial dermatitis. Parasitology 137:77–83 Skírnisson K, Aldhoun JA, Kolářová L (2009) A review on swimmer's itch and the occurrence of bird schistosomes in Iceland. J Helminthology 83:165–171 Valdovinos C, Balboa C (2008) Cercarial dermatitis and lake eutrophication in south-central Chile. Epidemiol Infect 136:391–394 Zbikowska E (2004) Infection of snails with bird schistosomes and the threat of swimmer's itch in selected Polish lakes. Parasitol Res 92:30–35 Larsen AH, Bresciani J, Buchmann K (2004) Increasing frequency of cercarial dermatitis at higher latitudes. Acta Parasitol 49:217–221 Grodhaus G, Keh B (1958) The marine, dermatitis-producing cercaria Austrobilharzia variglandis in California (Trematoda: Schistosomatidae). J Parasitol 44:633–638 Nobile L, Fioravanti ML, Pampiglione S, Calderan M, Marchese G (1996) Report of Gigantobilharzia acotylea (Digenea: Schistosomatidae) in silver gulls (Larus argentatus) of the Venice Lagoon: considerations on its possible etiological role in the human dermatitis observed in the same area. Parassitologia 38:267 Skírnisson K, Kolářová L (2008) Diversity of bird schistosomes in anseriform birds in Iceland based in egg measurements and egg morphology. Parasitol Res 103:43–50 Brant SV (2007) The occurrence of the avian schistosome Allobilharzia visceralis Kolákrová, Rudolfová, Hampl et Skirnisson, 2006 (Schistosomatidae) in the tundra swan, Cygnus columbianus (Anatidae), from North America. Folia Parasitol 54:99–104 Wang CR, Chen J, Zhao JP, Chen AH, Zhai YQ, Li L, Zhu XQ (2009) Orientobilharzia species: neglected parasitic zoonotic agents. Acta Trop 109:171–175 Cort WW, McMullen DB, Olivier L, Brackett S (1940) Studies on schistosome dermatitis. VII. Seasonal incidence of Cercaria stagnicolae Talbot, in relation to the life cycle of its snail host, Stagnicola emarginata angulata (Sowerby). Am J Hyg 32:33–69 Bastert J, Sing A, Wollenberg A, Korting HC (1998) Acquarium dermatitis: cercarial dermatitis in an aquarist. Dermatology 197:84–86 Fölster-Holst R, Disko R, Röwert J, Böckeler W, Kreiselmaier I, Christophers E (2011) Cercarial dermatitis contracted via contact with an acquarium: case report and review. Br J Dermatol 145:638–640 Verbrugge LM, Rainey JJ, Reimink RL, Blankespoor HD (2004) Swimmer's itch: incidence and risk factors. Am J Public Health 94:738–741 Verbrugge LM, Rainey JJ, Reimink RL, Blankespoor HD (2004) Prospective study of swimmer's incidence and severity. J Parasitol 90:697–704 Kolářová L, Horák P, Skírnisson K (2010) Methodical approaches in the identification of areas with a potential risk of infection by bird schistosomes causing cercarial dermatitis. J Helminthol 84:327–335 Curtis LA, Hubbard KM (1990) Trematode infections in a gastropod host misrepresented by observing shed cercariae. J Exp Mar Bio Ecol 143:131–137 Hertel J, Kedves K, Hassan AH, Haberl B, Haas W (2004) Detection of Schistosoma mansoni cercariae in plankton samples by PCR. Acta Trop 91:43–46 Rudolfová J, Hampl V, Bayssade-Dufour C, Lockyer AE, Littlewood DT, Horák P (2005) Validity reassessment of Trichobilharzia species using Lymnaea stagnalis as the intermediate host. Parasitol Res 95:79–89 Dvořák J, Vaňáčová S, Hampl V, Flegr J, Horák P (2002) Comparison of European Trichobilharzia species based on ITS1 and ITS2 sequences. Parasitology 124:307–313 Webster BL, Rudolfová J, Horák P, Littlewood DT (2007) The complete mitochondrial genome of the bird schistosome Trichobilharzia regenti (Plytyhelminthes: Digenea), causative agent of cercarial dermatitis. J Parasitol 93:553–561 Allgöwer R, Matuschka FR (1993) Zur Epidemiologie der Zerkariendermatitis. Bundesgesundheitsblatt 10:399–404 Blankespoor HD, Reimink RL (1991) The control of swimmer's itch in Michigan: past, present and future. Mich Acad 24:7–23 Wulff C, Haeberlein S, Haas W (2007) Cream formulation protecting against cercarial dermatitis by Trichobilharzia. Parasitol Res 101:91–97