Simplifying Schistosome Surveillance: Using Molecular Cercariometry to Detect and Quantify Cercariae in Water.

Avian schistosomes are considered a public health nuisance due to their ability to cause swimmer's itch when accidentally encountering humans rather than their intended avian hosts. Researchers have been monitoring their presence and abundance through snail collections and cercariometry. Cercariometry methods have evolved over the last several decades to detect individual schistosome species from a single water sample, simplifying the monitoring of these parasites. This methodological evolution coincides with the development of the field of environmental DNA (eDNA) where genetic material is extracted from environmental samples, rather than individual organisms. While there are some limitations with using molecular cercariometry, notably the cost and its inability to differentiate between life cycle stages, it substantially reduces the labor required to study trematode populations. It also can be used in complement with snail collections to understand the composition of avian schistosomes in an environment.

Non-resident definitive host presence is sufficient to sustain avian schistosome populations.

To control swimmer's itch in northern Michigan inland lakes, USA, one species of bird, the common merganser (Mergus merganser), has been relocated from several lakes since 2015. Relocation efforts are driven by a desire to reduce the prevalence of the swimmer's itch-causing parasite Trichobilharzia stagnicolae. The intention of this state-sponsored control effort was to interrupt the life cycle of T. stagnicolae and reduce parasite egg contribution into the environment from summer resident mergansers such that infections of the intermediate snail host Stagnicola emarginata declined. Reduced snail infection prevalence was expected to substantially reduce the abundance of the swimmer's itch-causing cercarial stage of the parasite in water. With no official programme in place to assess the success of this relocation effort, we sought to study the effectiveness and impact of the removal of a single definitive host from a location with high definitive host and parasite diversity. This was assessed through a comprehensive, lake-wide monitoring study measuring longitudinal changes in the abundance of three species of avian schistosome cercariae in four inland Michigan lakes. Environmental measurements were also taken at these lakes to understand how they can affect swimmer's itch incidence. This study demonstrates that the diversity of avian schistosomes at the study lakes would likely make targeting a single species of swimmer's itch-causing parasite meaningless from a swimmer's itch control perspective. Our data also suggest that removing the common merganser is not an effective control strategy for the T. stagnicolae parasite, likely due to contributions of the parasite made by non-resident birds, possibly migrants, in the autumn and spring. It appears likely that only minimal contact time between the definitive host and the lake ecosystem is required to contribute sufficient parasite numbers to maintain a thriving population of parasite species with high host specificity.

Evidence of a Putative Novel Species of Avian Schistosome Infecting Planorbella trivolvis.

Freshwater gastropods of the genera Lymnaea Lamarck, 1799, Physa Draparnaud, 1801, Gyraulus Charpentier, 1837, Radix Montfort, 1810, and Stagnicola Jeffreys, 1830 are considered suitable intermediate hosts for avian schistosomes. A large trematode biodiversity survey performed across 3 yr on 6 lakes in Alberta confirmed 3 already-reported snail hosts for 7 North American avian schistosomes; however, the cytochrome c oxidase subunit 1 (COI) nucleotide sequence from 1 cercarial sample (from a single specimen of Planorbella trivolvis) was distinct from all other COI schistosome sequences. As part of a simultaneous, comparable study of P. trivolvis by us in Michigan, we collected another cercarial type from 6 lakes that was 99% similar (COI) to the aforementioned cercarial type. Phylogenetic analyses of the COI and 28S rDNA genes recovered the former cercaria in a clade of avian schistosomes. In Michigan, the feces of a Canada goose (Branta canadensis Linnaeus, 1758) had a miracidium with an identical COI nucleotide sequence. Preliminary swimmer's itch and cercarial emergence studies were performed to determine if the cercariae could cause swimmer's itch and to study the emergence pattern as compared with species of Trichobilharzia Skrjabin and Zakharow, 1920.

Democratizing water monitoring: Implementation of a community-based qPCR monitoring program for recreational water hazards.

Recreational water monitoring can be challenging due to the highly variable nature of pathogens and indicator concentrations, the myriad of potential biological hazards to measure for, and numerous access points, both official and unofficial, that are used for recreation. The aim of this study was to develop, deploy, and assess the effectiveness of a quantitative polymerase chain reaction (qPCR) community-based monitoring (CBM) program for the assessment of bacterial and parasitic hazards in recreational water. This study developed methodologies for performing qPCR 'in the field,' then engaged with water management and monitoring groups and tested the method in a real-world implementation study to evaluate the accuracy of CBM using qPCR both quantitatively and qualitatively. This study found high reproducibility between qPCR results performed by non-expert field users and expert laboratory results, suggesting that qPCR as a methodology could be amenable to a CBM program.

Species-specific qPCR assays allow for high-resolution population assessment of four species avian schistosome that cause swimmer's itch in recreational lakes.

Swimmer's itch is an allergic condition that occurs when the motile and infectious stage of avian schistosomes penetrate the skin of an individual. Flatworm parasites that cause swimmer's itch belong to the family Schistosomatidae. They utilize a variety of different species of bird and mammal as definitive hosts, and rely on different species of snail, in which they complete their larval development to culminate in a motile, aquatic, infectious stage called a cercaria. Recently, qPCR-based assays have been developed to monitor for swimmer's itch-causing trematodes in recreational water. This environmental DNA approach has been useful for quantifying the abundance of the free-living cercaria, the causative agent of swimmer's itch. However, the existing qPCR test amplifies from all known schistosome species, making it excellent for assessing a site for swimmer's itch potential, but not useful in determining the specific species contributing to swimmer's itch or the likely hosts (snail and bird) of the swimmer's itch-causing parasites. Thus, species-specific resolution built into a qPCR test would be useful in answering ecological questions about swimmer's itch cause, and efficacy of control efforts. This paper details bird, snail, and cercaria surveys conducted in the summer of 2018, that culminated in the development and deployment of four species-specific qPCR assays, capable of detecting Trichobilharzia stagnicolae, Trichobilharzia szidati, Trichobilharzia physellae, and Anserobilharzia brantae in recreational water. These assays were used to assess the relative abundance of each parasite in water samples collected from lakes in Northern Michigan.

Evaluation of targeted copper sulfate (CuSO4) application for controlling swimmer's itch at a freshwater recreation site in Michigan.

Swimmer's itch has historically been controlled by applying copper sulfate (CuSO4) to lakes as a way to eliminate snails that serve as the intermediate hosts for swimmer's itch-causing parasites. CuSO4 is still sometimes applied specifically to areas of lakes where swimmer's itch severity is high. It is unclear whether targeted application of chemical molluscicides like CuSO4 is effective for controlling swimmer's itch. Previous research has found that the larval stage of the parasites responsible for swimmer's itch are released from infected snails and are concentrated by onshore and alongshore winds, and thus, may not be affected by such focused applications. In this study, we evaluated the impact of targeted CuSO4 application to a specific recreational swimming area in a lake in Michigan. We measured the effect on snail populations, as well as on the presence/abundance of swimmer's itch-causing parasites using qPCR. Ultimately, while CuSO4 was confirmed to significantly reduce populations of snails within the treatment area, it was found to have no significant impact on swimmer's itch-causing parasites in the water, likely due to the free-swimming larval stages (cercariae) moving into the treatment area from surrounding regions.

Use of qPCR-Based Cercariometry to Assess Swimmer's Itch in Recreational Lakes.

Swimmer's itch (cercarial dermatitis) is a nuisance encountered by bathers and recreational water users worldwide. The condition is caused by the penetration of larval digenean trematodes (cercariae) of the family Schistosomatidae, into the skin, following their release into freshwater from pulmonate snails that serve as the intermediate hosts for these parasites. This study utilizes qPCR-based cercariometry to monitor and quantify cercariae from water samples collected at 5 lakes in northern Michigan. The resolution provided by qPCR facilitated assessment of the environmental and biological drivers of swimmer's itch-causing cercariae concentrations, allowing us to demonstrate that cercarial abundance is greatest at the top of the water column, in locations with prevailing on- and alongshore winds.

Prospective study of swimmer's itch incidence and severity.

This epidemiologic study reports incidence, severity, and risk factors of swimmer's itch (cercarial dermatitis). Daily diaries about water exposures and swimmer's itch symptoms were completed by 40 riparian households at Douglas Lake, Michigan, for July 2000. Minutes spent in the water, minutes in shallow water, location, time of day, preventive action, age, and gender were recorded for all residents and guests. Incidence of swimmer's itch was 6.8 episodes per 100 water-exposure days. Probability of an episode increased with more days of water use and at locations with onshore winds. Episode severity increased with more time in the water and at the same locations. Age and gender had no effect on incidence or severity. In sum, onset and severity of swimmer's itch are affected by how people interact with the lake, not by their demographic features. More studies of human incidence and severity are needed to convince public health agencies to address this problem at recreational lakes. Study designs that combine epidemiologic and biological data will simultaneously inform public health education and biological control programs.

Swimmer's itch: incidence and risk factors.

Swimmer's itch (cercarial dermatitis) affects people engaged in open-water activities. We report incidence and risk factors for a US lake. Water exposures and swimmer's itch experience were reported daily for riparian household residents and guests at Douglas Lake, Michigan, in July 2000. Incidence of swimmer's itch was 6.8 episodes per 100 water exposure days. Positive risks were (1) exposures in shallow water and in areas with onshore winds and (2) more days of lake use in July. Further epidemiological studies will help public health agencies address this bothersome problem at recreational lakes.