Hostname: page-component-cd9895bd7-7cvxr Total loading time: 0 Render date: 2024-12-23T08:40:38.143Z Has data issue: false hasContentIssue false
  • English
  • Français

Direct onshore wind predicts daily swimmer's itch (avian schistosome) incidence at a Michigan beach

Published online by Cambridge University Press:  22 January 2020

Jason P. Sckrabulis Open the ORCID record for Jason P. Sckrabulis [Opens in a new window] ,
Alan R. Flory  and
Thomas R. Raffel
Jason P. Sckrabulis*
Affiliation:
Department of Biological Sciences, Oakland University, 118 Library Drive, Rochester, Michigan, 48309, USA
Alan R. Flory
Affiliation:
Crystal Lake Watershed Association, P.O. Box 89, Beulah, Michigan, 49617, USA
Thomas R. Raffel
Affiliation:
Department of Biological Sciences, Oakland University, 118 Library Drive, Rochester, Michigan, 48309, USA
*
Author for correspondence: Jason P. Sckrabulis, E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Swimmer's itch (SI) is a painful rash caused by skin penetration by free-swimming infectious cercariae of avian schistosomes, snail-borne helminth parasites related to the causative agents of human schistosomiasis. The goal of this study was to determine if commonly collected environmental data could be used to predict daily fluctuations in SI incidence at an inland beach in northwestern Michigan. Lifeguards collected daily data over four summers, including the number of self-reported SI cases, total swimmers, water temperature, wind speed and wind direction. Mixed-effects binomial regression revealed that wind direction, wind speed and time of day were the best predictors of daily SI risk. Swimmers entering the water in the morning or on days with direct onshore wind perpendicular to the shoreline had the greatest SI risk. However, there was a negative effect of wind speed after accounting for direction, where SI risk was greatest on days with a gentle breeze originating directly offshore. These results suggest that at this beach, direct onshore winds generate a surface-water current that causes SI cercariae to aggregate in the shallow waters used by swimmers. Data are needed from additional sites to confirm whether the onshore wind is a generally important driver of SI incidence.

Keywords

Lymnaea catescopium [ = Stagnicola emarginata]Trematode parasitesTrichobilharzia spp
Type
Research Article
Information
Parasitology , Volume 147 , Issue 4 , April 2020 , pp. 431 - 440
Check for updates
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anderson, PA, Nowosielski, JW and Croll, NA (1976) The emergence of cercariae of Trichobilharzia ocellata and its relationship to the activity of its host snail Lymnaea stagnalis. Canadian Journal of Zoology 54, 1481–1487.CrossRefGoogle Scholar
Ataev, G (1991) Temperature influence on the development and biology of rediae and cercariae of Philophthalamus rhionica (Trematoda). Parazitologija 25, 349–359.Google Scholar
Augustine, DL and Weller, TH (1949) Experimental studies on the specificity of skin tests for the diagnosis of schistosomiasis. Journal of Parasitology 35, 461–466.CrossRefGoogle Scholar
Bates, D, Maechler, M, Bolker, B and Walker, S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.CrossRefGoogle Scholar
Brant, SV and Loker, ES (2009) Molecular systematics of the avian schistosome genus Trichobilharzia (Trematoda: Schistosomatidae) in North America. Journal of Parasitology 95, 941–963.CrossRefGoogle Scholar
Brooker, S (2007) Spatial epidemiology of human schistosomiasis in Africa: risk models, transmission dynamics and control. Transactions of the Royal Society of Tropical Medicine and Hygiene 101, 1–8.CrossRefGoogle ScholarPubMed
Buck, JC and Lutterschmidt, WI (2017) Parasite abundance decreases with host density: evidence of the encounter-dilution effect for a parasite with a complex life cycle. Hydrobiologia 784, 201–210.CrossRefGoogle Scholar
Bush, KF, Fossani, CL, Li, S, Mukherjee, B, Gronlund, CJ and O'Neill, MS (2014) Extreme precipitation and beach closures in the Great Lakes region: evaluating risk among the elderly. International Journal of Environmental Research and Public Health 11, 2014–2032.CrossRefGoogle ScholarPubMed
Byers, JE, Holmes, ZC and Blakeslee, AMH (2016) Consistency of trematode infection prevalence in host populations across large spatial and temporal scales. Ecology 97, 1643–1649.CrossRefGoogle ScholarPubMed
Ciddio, M, Mari, L, Gatto, M, Rinaldo, A and Casagrandi, R (2015) The temporal patterns of disease severity and prevalence in schistosomiasis. Chaos: An Interdisciplinary Journal of Nonlinear Science 25, 1–10.CrossRefGoogle ScholarPubMed
Clampitt, PT (1970) Comparative ecology of the snails Physa gyrina and Physa integra (Basommatophora: Physidae). Malacologia 10, 113–151.Google Scholar
Clarke, AH (1981) The Freshwater Molluscs of Canada. Ottawa, Canada: National Museum of Natural Sciences, National Museums of Canada.CrossRefGoogle Scholar
Clements, ACA, Moyeed, R and Brooker, S (2006) Bayesian Geostatistical prediction of the intensity of infection with Schistosoma mansoni in east Africa. Parasitology 133, 711–719.CrossRefGoogle ScholarPubMed
Coady, NR, Muzzall, PM, Burton, TM, Snider, RJ, Saxton, J, Sergeant, M and Sommers, A (2006) Ubiquitous variability in the prevalence of Trichobilharzia stagnicolae (Schistosomatidae) infecting Stagnicola emarginata in three northern Michigan lakes. Journal of Parasitology 92, 10–15.CrossRefGoogle ScholarPubMed
Correa, AC, Escobar, JS, Durand, P, Renaud, F, David, P, Jarne, P, Pointeir, J and Hurtrez-Bousses, S (2010) Bridging gaps in the molecular phylogeny of the Lymnaeidae (Gastropoda: Pulmonata), vectors of fascioliasis. BMC Evolutionary Biology 10, 1–12. doi: 10.1186/1471-2148-10-381.CrossRefGoogle Scholar
Da Costa, C, Dreyfuss, G, Rakotondravao, and Rondelaud, D (1994) Several observations concerning cercarial sheddings of Fasciola gigantica from Lymnaea natalensis. Parasite 1, 44.CrossRefGoogle ScholarPubMed
Feiler, W and Haas, W (1988) Host-finding in Trichobilharzia ocellata cercariae: swimming and attachment to the host. Parasitology 96, 493–505.CrossRefGoogle ScholarPubMed
Fingerut, JT, Zimmer, CA and Zimmer, RK (2003) Larval swimming overpowers turbulent mixing and facilitates transmission of a marine parasite. Ecology 84, 2502–2515.CrossRefGoogle Scholar
Fox, J and Weisberg, S (2011) An R Companion to Applied Regression, 2nd Edn. Thousand Oaks, California: Sage. http://socserv.socsci.mcmaster.ca/jfox/Books/Companion.Google Scholar
Frank, GH (1966) The effect of temperature on the rate of development and emergence of schistosome cercariae. Zoologica Africana 2, 211–221.CrossRefGoogle Scholar
Galaktionov, KV, Bustnes, JO, Bårdsen, B, Wilson, JG, Nikolaev, KE, Sukhotin, AA, Skírnisson, K, Saville, DH, Ivanov, MV and Regel, KV (2015) Factors influencing the distribution of trematode larvae in blue mussels Mytilus edulis in the North Atlantic and Arctic Oceans. Marine Biology 162, 193–206.CrossRefGoogle Scholar
Haas, W and van der Roemer, A (1998) Invasion of the vertebrate skin by cercariae of Trichobilharzia ocellata: penetration processes and stimulating host signals. Parasitology Research 84, 787–795.CrossRefGoogle ScholarPubMed
Haeberlein, S and Haas, W (2008) Chemical attractants of human skin for swimming Schistosoma mansoni cercariae. Parasitology Research 102, 657–662.CrossRefGoogle ScholarPubMed
Halstead, NT, McMahon, TA, Johnson, SA, Raffel, TR, Romansic, JM, Crumrine, PW and Rohr, JR (2014) Community ecology theory predicts the effect of agrochemical mixtures on aquatic biodiversity and ecosystem properties. Ecology Letters 17, 932–941.CrossRefGoogle Scholar
Halstead, NT, Hoover, CM, Arakala, A, Civitello, DJ, De Leo, GA, Gambhir, M, Johnson, SA, Jouanard, N, Loerns, KA, McMahon, TA, Ndione, RA, Nguyen, K, Raffel, TR, Remais, JV, Riveau, G, Sokolow, SH and Rohr, JR (2018) Agrochemicals increase risk of human schistosomiasis by supporting higher densities of intermediate hosts. Nature Communications 9, 1–10. doi: 10.1038/s41467-018-03189-w.CrossRefGoogle ScholarPubMed
Hodasi, JKM (1976) The effects of low temperature on Lymnaea truncatula. Zeitschrift Für Parasitenkunde 48, 281–286.CrossRefGoogle ScholarPubMed
Horák, P, Mikeš, L, Lichtenbergová, L, Skála, V, Soldánová, M and Brant, SV (2015) Avian schistosomes and outbreaks of cercarial dermatitis. Clinical Microbiology Reviews 28, 165–190.CrossRefGoogle ScholarPubMed
Islam, KS (1986) The morphology and life-cycle of Trichobilharzia arcuata n. sp. (Schistosomatidae: Bilharziellinae) a nasal schistosome of water whistle ducks (Dendrocygna arcuata) in Australia. Systematic Parasitology 8, 117–128.CrossRefGoogle Scholar
Jothikumar, N, Mull, BJ, Brant, SV, Loker, ES, Collinson, J, Secor, WE and Hill, VR (2015) Real-time PCR and sequencing assays for rapid detection and identification of avian schistosomes in environmental samples. Applied and Environmental Microbiology 81, 4207–4215.CrossRefGoogle ScholarPubMed
Jousson, O and Bartoli, P (2000) The life cycle of Opecoeloides columbellae (Pagenstecher, 1863) n. comb. (Digenea, Opecoelidae): evidence from molecules and morphology. International Journal for Parasitology 30, 747–760.CrossRefGoogle ScholarPubMed
Kolářová, L, Horák, P and Skírnisson, K (2010) Methodical approaches in the identification of areas with a potential risk of infection by bird schistosomes causing cercarial dermatitis. Journal of Helminthology 84, 327–335.CrossRefGoogle ScholarPubMed
Kube, J, Kube, S and Dierschke, V (2002) Spatial and temporal variations in the trematode component community of the mudsnail Hydrobia ventrosa in relation to the occurrence of waterfowl as definitive hosts. Journal of Parasitology 88, 1075–1086.CrossRefGoogle ScholarPubMed
Kuntz, RE (1947) Effect of light and temperature on emergence of Schistosoma mansoni cercariae. Transactions of the American Microscopical Society 66, 37–49.CrossRefGoogle ScholarPubMed
Laman, TG, Boss, NC and Blankespoor, HD (1984) Depth distribution of seven species of gastropods in Douglas Lake, Michigan. The Nautilus 98, 20–25.Google Scholar
Lawson, JR and Wilson, RA (1980) The survival of the cercariae of Schistosoma mansoni in relation to water temperature and glycogen utilization. Parasitology 81, 337–348.CrossRefGoogle ScholarPubMed
Leighton, BJ, Zervos, S and Webster, JM (2000) Ecological factors in schistosome transmission, and an environmentally benign method for controlling snails in a recreational lake with a record of schistosome dermatitis. Parasitology International 49, 9–17.CrossRefGoogle Scholar
McClelland, WJF (1965) The production of cercariae by Schistosoma mansoni and S. haematobium and methods for estimating the numbers of cercariae in suspension. Bulletin World Health Organization 33, 270–276.Google ScholarPubMed
McCreesh, N and Booth, M (2014) The effect of increasing water temperatures on Schistosoma mansoni transmission and Biomphalaria pfeifferi population dynamics: an agent-based modelling study. PLoS One 9, e101462.CrossRefGoogle ScholarPubMed
Muzzall, PM, Burton, TM, Snider, RJ and Coady, NR (2003) Occurrence, Distribution and Control of the Parasites that Cause Swimmer's Itch in Michigan, Extension Bulletin WQ 58. Michigan State University, Lansing, Michigan: Michigan State University Extension.Google Scholar
Nagelkerke, NJD (1991) A note on the general definition of the coefficient of determination. Biometrika 78, 691–692.CrossRefGoogle Scholar
Najim, AT (1956) Life history of Gigantobilharzia huronensis Najim, 1950. A dermatitis-producing bird blood-fluke (Trematoda-Schistosomatidae). Parasitology 46, 443–469.CrossRefGoogle Scholar
Paull, SH, LaFonte, BE and Johnson, PTJ (2012) Temperature-driven shifts in a host-parasite interaction drive nonlinear changes in disease risk. Global Change Biology 18, 3558–3567.CrossRefGoogle Scholar
Paull, SH, Raffel, TR, LaFonte, BE and Johnson, PTJ (2015) How temperature shifts affect parasite production: testing the roles of thermal stress and acclimation. Functional Ecology 29, 941–950.CrossRefGoogle Scholar
Price, HF (1931) Life history of Schistosomatium douthitti (Cort). American Journal of Hygiene 13, 685–727.Google Scholar
R Core Team (2019) R: A Language and Environment for Statistical Computing. [computer software]. Vienna, Austria: R Foundation for Statistical Computing.Google Scholar
Raso, G, Matthys, B, N'Goran, EK, Tanner, M, Vounatsou, P and Utzinger, J (2005) Spatial risk prediction and mapping of Schistosoma mansoni infections among schoolchildren living in western Côte d'Ivoire. Parasitology 131, 97–108.CrossRefGoogle ScholarPubMed
Rudko, SP, Reimink, RL, Froelich, K, Gordy, MA, Blankespoor, CL and Hanington, PC (2018) Use of qPCR-based cercariometry to assess swimmer's itch in recreational lakes. Ecohealth 15, 827–839.CrossRefGoogle ScholarPubMed
Rudko, SP, Turnbull, A, Reimink, RL, Froelich, K and Hanington, PC (2019) Species-specific qPCR assays allow for high-resolution population assessment of four species avian schistosome that cause swimmer's itch in recreational lakes. International Journal for Parasitology: Parasites and Wildlife 9, 122–129.Google ScholarPubMed
Scherer, R (2018) Propcis: Various confidence interval methods for proportions. [computer software].Google Scholar
Sokolow, SH, Huttinger, E, Jouanard, N, Hsieh, MH, Lafferty, KD, Kuris, AM, Riveau, G, Senghor, S, Thiam, C, N'Diaye, A, Sarr Faye, D and De Leo, GA (2015) Reduced transmission of human schistosomiasis after restoration of a native river prawn that preys on the snail intermediate host. Proceedings of the National Academy of Sciences 112, 9650–9655.CrossRefGoogle ScholarPubMed
Soldánová, M, Selbach, C and Sures, B (2016) The early worm catches the bird? Productivity and patterns of Trichobilharzia szidati cercarial emission from Lymnaea stagnalis. PLoS One 11, e0149678.CrossRefGoogle ScholarPubMed
Spear, RC, Zhong, B, Mao, Y, Hubbard, A, Birkner, M, Remais, J and Qiu, D (2004) Spatial and temporal variability in schistosome cercarial density detected by mouse bioassays in village irrigation ditches in Sichuan, China. The American Journal of Tropical Medicine and Hygiene 71, 554–557.CrossRefGoogle ScholarPubMed
Studer, A and Poulin, R (2013) Differential effects of temperature variability on the transmission of a marine parasite. Marine Biology 160, 2763–2773.CrossRefGoogle Scholar
Sunada, H, Totani, Y, Nakamura, R, Sakakibara, M, Lukowaik, K and Ito, E (2017) Two strains of Lymnaea stagnalis and the progeny from their mating display differential memory-forming ability on associative learning tasks. Frontiers in Behavioral Neuroscience 11, 161.CrossRefGoogle ScholarPubMed
Talbot, SB (1936) Studies on schistosome dermatitis: II. Morphological and life history studies on three dermatitis-producing schistosome cercariae, C. elvae Miller, 1923, C. stagnicolae N. sp., and C. physellae n. sp. American Journal of Epidemiology 23, 372–384.CrossRefGoogle Scholar
Upatham, ES (1974) Dispersion of St. Lucian Schistosoma mansoni cercariae in natural standing and running waters determined by cercaria counts and mouse exposure. Annals of Tropical Medicine and Parasitology 68, 343–352.CrossRefGoogle ScholarPubMed
Valdovinos, C and Balboa, C (2007) Cercarial dermatitis and lake eutrophication in south-central Chile. Epidemiology and Infection 136, 391–394.CrossRefGoogle ScholarPubMed
Verbrugge, LM, Rainey, JJ, Reimink, RL and Blankespoor, HD (2004a) Prospective study of swimmer's itch incidence and severity. Journal of Parasitology 90, 697–704.CrossRefGoogle Scholar
Verbrugge, LM, Rainey, JJ, Reimink, RL and Blankespoor, HD (2004b) Swimmer's itch: incidence and risk factors. American Journal of Public Health 94, 738–741.CrossRefGoogle Scholar
Weber, JE (1983) Steady wind- and wave-induced currents in the open ocean. Journal of Physical Oceanography 13, 524–530.2.0.CO;2>CrossRefGoogle Scholar
Whitfield, PJ, Bartlett, A, Khammo, N and Clothier, RH (2003) Age-dependent survival and infectivity of Schistosoma mansoni cercariae. Parasitology 127, 29–35.CrossRefGoogle ScholarPubMed
Wright, DGS (1974) Responses of cercariae of Trichobilharzia ocellata to white light, monochromatic light, and irradiance reduction. Canadian Journal of Zoology 52, 575–579.CrossRefGoogle ScholarPubMed
Yang, GJ, Gemperli, A, Vounatsou, P, Tanner, M, Zhou, XN and Utzinger, J (2006) A growing degree-days based time-series analysis for prediction of Schistosoma japonicum transmission in Jiangsu province, China. The American Journal of Tropical Medicine and Hygiene 75, 549–555.CrossRefGoogle ScholarPubMed
Żbikowska, E (2005) Do larvae of Trichobilharzia szidati and Echinostoma revolutum generate behavioral fever in Lymnaea stagnalis individuals? Parasitology Research 97, 68–72.CrossRefGoogle ScholarPubMed
Żbikowska, E and Cichy, A (2012) Symptoms of behavioural anapyrexia – reverse fever as a defence response of snails to fluke invasion. Journal of Invertebrate Pathology 109, 269–273.CrossRefGoogle ScholarPubMed
Żbikowska, E and Marszewska, A (2018) Thermal preferences of bird schistosome snail hosts increase the risk of swimmer's itch. Journal of Thermal Biology 78, 22–26.CrossRefGoogle ScholarPubMed
Zhou, YB, Yang, MX, Yihuo, WL, Liu, GM, Wang, HY, Wei, JG and Jiang, QW (2011) Effect of habitat fragmentation on the schistosome-transmitting snail Oncomelania hupensis in a mountainous area of China. Transactions of the Royal Society of Tropical Medicine and Hygiene 105, 189–196.CrossRefGoogle Scholar
Supplementary material: File

Sckrabulis et al. Supplementary Materials

Sckrabulis et al. Supplementary Materials

Download Sckrabulis et al. Supplementary Materials(File)
File 14 MB