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16 pages, 1035 KiB  
Review
Zoonotic Threats: The (Re)emergence of Cercarial Dermatitis, Its Dynamics, and Impact in Europe
by Maria Teresa Bispo, Manuela Calado, Isabel Larguinho Maurício, Pedro Manuel Ferreira and Silvana Belo
Pathogens 2024, 13(4), 282; https://doi.org/10.3390/pathogens13040282 - 26 Mar 2024
Cited by 1 | Viewed by 2586
Abstract
Cercarial dermatitis (CD), or “Swimmer’s itch” as it is also known, is a waterborne illness caused by a blood fluke from the family Schistosomatidae. It occurs when cercariae of trematode species that do not have humans as their definitive host accidentally penetrate human [...] Read more.
Cercarial dermatitis (CD), or “Swimmer’s itch” as it is also known, is a waterborne illness caused by a blood fluke from the family Schistosomatidae. It occurs when cercariae of trematode species that do not have humans as their definitive host accidentally penetrate human skin (in an aquatic environment) and trigger allergic symptoms at the site of contact. It is an emerging zoonosis that occurs through water and is often overlooked during differential diagnosis. Some of the factors contributing to the emergence of diseases like CD are related to global warming, which brings about climate change, water eutrophication, the colonization of ponds by snails susceptible to the parasite, and sunlight exposure in the summer, associated with migratory bird routes. Therefore, with the increase in tourism, especially at fluvial beaches, it is relevant to analyze the current epidemiological scenario of CD in European countries and the potential regions at risk. Full article
(This article belongs to the Special Issue One Health and Neglected Zoonotic Diseases)
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Graphical abstract

Graphical abstract
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<p>Human cercarial dermatitis – infection cycle. 1- Eggs found in the faeces of infected aquatic birds hatch into miracidia upon contact with water. 2- Miracidia then seek out a specific snail host and penetrate its mucosa. 3- Within the snail, the cycle progresses through the sporocyst phase and subsequent generations; 4- Emergence of infectious cercariae. 5- These cercariae penetrate the skin of the definitive avian host, shedding their tail. Then, schistosomula migrate through blood vessels to various organs, where they develop into adult forms, initiating the sexual phase. 6- Free-swimming cercariae may penetrate human skin, leading to dermatitis. 7- The immune system responds with an allergic and inflammatory reaction, involving the recruitment of neutrophils, mast cells, eosinophils, and T lymphocytes; these cells release cytokines to regulate the inflammatory process and aid in elimination of the parasite.</p>
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<p>Map of European countries that registered cases of cercarial dermatitis (bicontinental countries were excluded, except for Russia).</p>
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13 pages, 3175 KiB  
Article
Mammalian and Avian Larval Schistosomatids in Bangladesh: Molecular Characterization, Epidemiology, Molluscan Vectors, and Occurrence of Human Cercarial Dermatitis
by Sharmin Shahid Labony, Md. Shahadat Hossain, Takeshi Hatta, Anita Rani Dey, Uday Kumar Mohanta, Ausraful Islam, Md. Shahiduzzaman, Muhammad Mehedi Hasan, Md. Abdul Alim, Naotoshi Tsuji and Anisuzzaman
Pathogens 2022, 11(10), 1213; https://doi.org/10.3390/pathogens11101213 - 20 Oct 2022
Cited by 3 | Viewed by 2481
Abstract
Schistosomiasis is a neglected tropical disease (NTD) caused by blood flukes (Schistosoma spp.). Schistosomatids affect a wide array of vertebrate hosts, including humans. In the present study, multiple species of schistosomatids were identified by isolating schistosomatid cercariae (SC) from naturally infected snails. [...] Read more.
Schistosomiasis is a neglected tropical disease (NTD) caused by blood flukes (Schistosoma spp.). Schistosomatids affect a wide array of vertebrate hosts, including humans. In the present study, multiple species of schistosomatids were identified by isolating schistosomatid cercariae (SC) from naturally infected snails. We also described different biotic and abiotic factors influencing SC infections in snails and reported human cercarial dermatitis (HCD) for the first time in Bangladesh. A total of 22,012 snails of seven species: Lymnaea auricularia, L. luteola, Indoplanorbis exustus, Physa acuta, Viviparus bengalensis, Brotia spp., and Thiara spp., were collected and examined. Among these snails, 581 (2.6%) belonging to five species: L. luteola, L. auricularia, P. acuta, I. exustus, and V. bengalensis, were infected with SC. The rate of infection was the highest for L. luteola (11.1%), followed by L. auricularia (5.3%), and was the lowest for V. bengalensis (0.4%). Prevalence in snails was the highest in September (16.8%), followed by October (9.5%) and November (8.8%), and was the lowest in colder months, such as January (1.8%) and February (2.1%). Infections with schistosomatids were more common in larger snails and snails collected from sunny areas. We confirmed the presence of Schistosoma indicum, S. incognitum, S. nasale, S. spindale, and Trichobilharzia szidati by PCR and sequencing. Through a questionnaire survey, we detected HCD in 214 (53.5%) individuals, and the infection rate was almost equally distributed across all professions. Collectively, the present results suggest that lymnaeid snails are the main vector for Schistosoma spp. prevalent in Bangladesh, and schistosomatids with zoonotic potential are also prevalent. Full article
(This article belongs to the Special Issue Arthropod- and Gastropod-Borne Diseases in a One Health Perspective)
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Figure 1

Figure 1
<p><b>Study area</b>. Prepared with Landsat satellite images and the Google Earth engine; see ref. [<a href="#B19-pathogens-11-01213" class="html-bibr">19</a>] for detailed method.</p>
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<p><b>Comparative prevalence of SC in different species of snails in Bangladesh.</b> (<b>A</b>) Species of the snails infected by <span class="html-italic">Schistosoma</span> spp. in Bangladesh. (<b>B</b>) Infection rates of SC in different snail species. * <span class="html-italic">p</span> &lt; 0.05 were statistically significant. NS; statistically insignificant (<span class="html-italic">p</span> &gt; 0.05). (<b>C</b>) A microphotograph of SC showing its characteristic features.</p>
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<p><b>Temporal distribution and habitat diversities of Schistosomatid-infected vector snails in Bangladesh.</b> (<b>A</b>) Temporal distribution of infections with schistosomatids in vector snails. (<b>B</b>) Habitat preference of vectors of SC. * <span class="html-italic">p</span> &lt; 0.05 are statistically significant. NS, statistically insignificant (<span class="html-italic">p</span> &gt; 0.05).</p>
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<p><b>Dendrograms showing species-specific clusters of sequences.</b> (<b>A</b>) A 28S rRNA-based dendrogram showing different species of schistosomatids affecting mammals. (<b>B</b>) A cox1 gene-based dendrogram of schistosomatids affecting birds. Phylogenetic trees were constructed using maximum likelihood (ML) methods in MEGA X.</p>
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<p><b>Human cercarial dermatitis was highly prevalent in study areas in Bangladesh</b>. (<b>A</b>) Distributions of HCD across the different professions in the study areas were estimated by a questionnaire-based survey. (<b>B</b>) Skin lesions induced by HCD; left panel, acute HCD and right panel, chronic HCD.</p>
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<p>Schematic diagram showing the complex life cycle of <span class="html-italic">Schistosoma</span> spp. and a demonstration of exposure to cercariae leading to the development of human cercarial dermatitis (HCD). CD, cercarial dermatitis; SkS, skin stage; LuS, lung stage; eLiS, early liver stage; LiS/JuW, liver stage or juvenile worms; C, cercariae; dS, daughter sporocysts; S, sporocyst; M, miracidium.</p>
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12 pages, 1019 KiB  
Article
The Tails of Two Avian Schistosomes: Paired Exposure Study Demonstrates Trichobilharzia stagnicolae Penetrates Human Skin More Readily than a Novel Avian Schistosome from Planorbella
by Nathaniel J. Anderson, Curtis L. Blankespoor and Randall J. DeJong
Pathogens 2022, 11(6), 651; https://doi.org/10.3390/pathogens11060651 - 4 Jun 2022
Cited by 2 | Viewed by 4448
Abstract
A novel schistosome from Planorbella snails currently known as avian schistosomatid sp. C (ASC) was recently described as being capable of causing the papules associated with swimmer’s itch. We conducted a paired study with 24 human volunteers, exposing each of their forearms to [...] Read more.
A novel schistosome from Planorbella snails currently known as avian schistosomatid sp. C (ASC) was recently described as being capable of causing the papules associated with swimmer’s itch. We conducted a paired study with 24 human volunteers, exposing each of their forearms to five drops of water containing cercariae of ASC or Trichobilharzia stagnicolae, and examined the skin for papules 1–3 days later. A mixed effects model showed that only the parasite species significantly affected the number of papules, while prior experimental exposure, swimming history, and swimmer’s itch experience did not. The total number of papules produced by the two species were very different: ASC produced a total of 2 papules from the 298 cercariae used, compared to 49 papules from 160 T. stagnicolae cercariae, a difference factor of more than 43X, which was comparable to the odds ratio of 45.5 computed using the statistical model. A well-known agent of swimmer’s itch, T. stagnicolae, is able to penetrate human skin more frequently than ASC, likely meaning that ASC is only a minor cause of swimmer’s itch where T. stagnicolae is present. We also completed limited experiments that compared the cercarial behavior of the two species in vitro and in situ. A known stimulant of schistosome cercarial penetration, α-linolenic acid, did not stimulate ASC cercariae to initiate penetration-associated behaviors as frequently as T. stagnicolae. However, when placed on esophageal tissue of the known vertebrate host for ASC, Canada goose (Branta canadensis), ASC cercariae were observed penetrating the esophageal epithelium quickly, whereas T. stagnicolae cercariae did not exhibit any penetration behaviors. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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Figure 1

Figure 1
<p>Arms of volunteer at post-exposure follow-up visit. Left arm (top), exposed to five <span class="html-italic">T. stagnicolae</span> cercariae, has four visible papules. Right arm (bottom), exposed to at least 10 ASC cercariae, did not develop any papules.</p>
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<p>Number of papules produced on the arms of volunteers by five drops of cercariae-containing water. For <span class="html-italic">T. stagnicolae,</span> each drop contained 1 cercaria. For ASC, the first four participants received 1 cercaria per drop, but this was increased to 2–3 per drop for all other exposures to increase the chances of demonstrating that ASC can cause swimmer’s itch. Each rhombus represents the number of papules out of five that were observed on an individual arm (open = ASC, filled = <span class="html-italic">T. stagnicolae</span>). Horizontal line indicates mean number of papules per person (0.06 ASC, 1.53 <span class="html-italic">T. stagnicolae</span>).</p>
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<p>Percentage of cercariae of each species that induced papules in 32 exposures of human volunteers. <span class="html-italic">Trichobilharzia</span> <span class="html-italic">stagnicolae</span> induced 49 papules from 160 cercariae (30.6%). The recently described species, ASC, induced 2 papules from 298 cercariae (0.7%).</p>
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<p>Study flow diagram. The recruitment, exclusion, and inclusion of volunteers, descriptive data of participants, and the methods of exposure. Data from the questionnaire (inland lake swimming history, swimmer’s itch history) and the results from exposures (number of papules formed from five drops) were used in the statistical model.</p>
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23 pages, 3544 KiB  
Article
Cercariae of a Bird Schistosome Follow a Similar Emergence Pattern under Different Subarctic Conditions: First Experimental Study
by Miroslava Soldánová, Ana Born-Torrijos, Roar Kristoffersen, Rune Knudsen, Per-Arne Amundsen and Tomáš Scholz
Pathogens 2022, 11(6), 647; https://doi.org/10.3390/pathogens11060647 - 3 Jun 2022
Cited by 4 | Viewed by 2292
Abstract
The emergence of cercariae from infected mollusks is considered one of the most important adaptive strategies for maintaining the trematode life cycle. Short transmission opportunities of cercariae are often compensated by periodic daily rhythms in the cercarial release. However, there are virtually no [...] Read more.
The emergence of cercariae from infected mollusks is considered one of the most important adaptive strategies for maintaining the trematode life cycle. Short transmission opportunities of cercariae are often compensated by periodic daily rhythms in the cercarial release. However, there are virtually no data on the cercarial emergence of bird schistosomes from freshwater ecosystems in northern latitudes. We investigated the daily cercarial emergence rhythms of the bird schistosome Trichobilharzia sp. “peregra” from the snail host Radix balthica in a subarctic lake under both natural and laboratory seasonal conditions. We demonstrated a circadian rhythm with the highest emergence during the morning hours, being seasonally independent of the photo- and thermo-period regimes of subarctic summer and autumn, as well as relatively high production of cercariae at low temperatures typical of northern environments. These patterns were consistent under both field and laboratory conditions. While light intensity triggered and prolonged cercarial emergence, the temperature had little effect on cercarial rhythms but regulated seasonal output rates. This suggests an adaptive strategy of bird schistosomes to compensate for the narrow transmission window. Our results fill a gap in our knowledge of the transmission dynamics and success of bird schistosomes under high latitude conditions that may serve as a basis for elucidating future potential risks and implementing control measures related to the spread of cercarial dermatitis due to global warming. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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Graphical abstract

Graphical abstract
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<p>Daily patterns in cercarial emergence (recalculated to 1 hour) of <span class="html-italic">Trichobilharzia</span> sp. “peregra” from individuals of <span class="html-italic">Radix balthica</span> snails (marked with different line colors) during diel intervals (Sr, sunrise; D, day; Ss, sunset; N, night) under field and laboratory conditions in (<b>a</b>) August 2016, (<b>b</b>) August 2017, (<b>c</b>) August 2018, and (<b>d</b>) October 2018. Cercarial emergence during the longest parts of the natural photoperiod in summer (day interval in August) and autumn (night interval in October) are divided into half and termed as D1, D2 and N1, N2. Note the different number of experimental days in August 2016 (see also <a href="#pathogens-11-00647-t001" class="html-table">Table 1</a>). The emergence data from October 2018 are not shown due to a single snail producing cercariae in similar numbers during a single day (see <a href="#app1-pathogens-11-00647" class="html-app">Appendix A</a> <a href="#pathogens-11-00647-t0A1" class="html-table">Table A1</a>). “ln” refers to ln-transformed number of emerged cercariae per hour.</p>
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<p>Daily patterns in cercarial emergence (mean ± SE, recalculated to 1 h) of <span class="html-italic">Trichobilharzia</span> sp. “peregra” from <span class="html-italic">Radix balthica</span> snails during diel intervals (Sr, sunrise in triangles; D, day in circles; Ss, sunset in diamonds; N, night in squares) under natural photoperiod in field experiments in August 2017 and 2018. Day interval is divided into half and termed as D1 and D2. Note that the mean value of cercarial emergence from two snails is given for the third day of the experiment in August 2017 (see <a href="#app1-pathogens-11-00647" class="html-app">Appendix A</a> <a href="#pathogens-11-00647-t0A1" class="html-table">Table A1</a>). “ln” refers to ln-transformed number of emerged cercariae per hour.</p>
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<p><span class="html-italic">In situ</span> emergence of cercariae of <span class="html-italic">Trichobilharzia</span> sp. “peregra” from naturally infected snails <span class="html-italic">Radix balthica</span>. (<b>a</b>,<b>b</b>) Experimental design conducted in a side stream flowing into Lake Takvatn during the preliminary testing of constructions in 2016. (<b>c</b>,<b>d</b>) Experimental design conducted directly in the lake between 2017–2018.</p>
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27 pages, 2454 KiB  
Review
Scratching the Itch: Updated Perspectives on the Schistosomes Responsible for Swimmer’s Itch around the World
by Eric S. Loker, Randall J. DeJong and Sara V. Brant
Pathogens 2022, 11(5), 587; https://doi.org/10.3390/pathogens11050587 - 16 May 2022
Cited by 9 | Viewed by 7103
Abstract
Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they [...] Read more.
Although most studies of digenetic trematodes of the family Schistosomatidae dwell on representatives causing human schistosomiasis, the majority of the 130 identified species of schistosomes infect birds or non-human mammals. The cercariae of many of these species can cause swimmer’s itch when they penetrate human skin. Recent years have witnessed a dramatic increase in our understanding of schistosome diversity, now encompassing 17 genera with eight more lineages awaiting description. Collectively, schistosomes exploit 16 families of caenogastropod or heterobranch gastropod intermediate hosts. Basal lineages today are found in marine gastropods and birds, but subsequent diversification has largely taken place in freshwater, with some reversions to marine habitats. It seems increasingly likely that schistosomes have on two separate occasions colonized mammals. Swimmer’s itch is a complex zoonotic disease manifested through several different routes of transmission involving a diversity of different host species. Swimmer’s itch also exemplifies the value of adopting the One Health perspective in understanding disease transmission and abundance because the schistosomes involved have complex life cycles that interface with numerous species and abiotic components of their aquatic environments. Given the progress made in revealing their diversity and biology, and the wealth of questions posed by itch-causing schistosomes, they provide excellent models for implementation of long-term interdisciplinary studies focused on issues pertinent to disease ecology, the One Health paradigm, and the impacts of climate change, biological invasions and other environmental perturbations. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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Figure 1
<p>Typical life cycle of an avian schistosome. In this case, <span class="html-italic">Trichobilharzia stagnicolae</span> is commonly implicated in swimmer’s itch outbreaks in oligotrophic lakes in Michigan, in the northern USA. Note the involvement of an avian definitive host such as the common merganser (<span class="html-italic">Mergus merganser</span>) in which adult worms mate and reproduce, resulting in discharge of schistosome eggs into the water. Eggs hatch and release swimming, ciliated miracidia that locate and penetrate the freshwater snail host <span class="html-italic">Stagnicola emarginata</span>. A miracidium transforms into a mother sporocyst that produces multiple daughter sporocysts that migrate to the snail’s digestive gland where they produce numerous cercariae. The cercariae exit the snail, swim, and are carried by currents or wave action, and once they have located a merganser will penetrate the skin and continue the life cycle. People in contact with the water are also at risk of skin penetration by the cercariae, which typically incite a strong inflammatory reaction, swimmer’s itch, and usually, but not always, die in the skin.</p>
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<p>Sequence-based identification of new avian schistosome lineages. The blue line represents avian schistosome species formally described over time. The red line identifies the number of new, distinct lineages of schistosomes identified from molecular signatures, many from cercariae derived from field-collected snails.</p>
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<p>Overview of relationships among members of the Schistosomatidae based on published ~1200 bp of 28S sequence. On the right, numbered sequentially from the top, are shown 25 putative genus-level lineages, 17 of described genera (including <span class="html-italic">Marinabilharzia</span> and <span class="html-italic">Riverabilharzia</span> recently described) and 8 additional probable generic-level lineages. Indicated on the right, also, are conservative numbers of species for the speciose genera. For the avian schistosomes, preliminary sequence data suggest at least 12 additional species remain to be described. Asterisks indicate Bayesian posterior probabilities at &gt;0.95.</p>
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<p>There are several different biological contexts in which swimmer’s itch might occur (see corresponding text for more details). The double headed arrows emphasize the connectedness between the gastropod host and the vertebrate host in any schistosome life cycle that, in more detail, operates as shown in <a href="#pathogens-11-00587-f001" class="html-fig">Figure 1</a> and <a href="#pathogens-11-00587-f005" class="html-fig">Figure 5</a>.</p>
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<p>An alternative version of the life cycle of <span class="html-italic">Trichobilharzia stagnicolae</span> shown in <a href="#pathogens-11-00587-f001" class="html-fig">Figure 1</a>, taking into account at least some of the myriads of circumstances that might impact the parasite and its tendency to cause swimmer’s itch outbreaks. See text for discussion.</p>
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23 pages, 2723 KiB  
Article
Morphological, Behavioral, and Molecular Characterization of Avian Schistosomes (Digenea: Schistosomatidae) in the Native Snail Chilina dombeyana (Chilinidae) from Southern Chile
by Pablo Oyarzún-Ruiz, Richard Thomas, Adriana Santodomingo, Gonzalo Collado, Pamela Muñoz and Lucila Moreno
Pathogens 2022, 11(3), 332; https://doi.org/10.3390/pathogens11030332 - 9 Mar 2022
Cited by 8 | Viewed by 2997
Abstract
Avian schistosomes are blood flukes parasitizing aquatic birds and snails, which are responsible for a zoonotic disease known as cercarial dermatitis, a hypersensitive reaction associated to the cutaneous penetration of furcocercariae. Despite its worldwide distribution, its knowledge is fragmentary in the Neotropics, with [...] Read more.
Avian schistosomes are blood flukes parasitizing aquatic birds and snails, which are responsible for a zoonotic disease known as cercarial dermatitis, a hypersensitive reaction associated to the cutaneous penetration of furcocercariae. Despite its worldwide distribution, its knowledge is fragmentary in the Neotropics, with most of data coming from Argentina and Brazil. In Chile, there are only two mentions of these parasites from birds, and one human outbreak was associated to the genus “Trichobilharzia”. However, the identity of such parasites is pending. The aim of this study was to identify the furcocercariae of avian schistosomes from Southern Chile using an integrative approach. Thus, a total of 2283 freshwater snails from different families were collected from three different regions. All snails were stimulated for the shedding of furcocercariae, but only Chilina dombeyana (Chilinidae) from the Biobío region was found to be parasitized. The morphology and phylogenetic analyses of 28S and COI genes stated two lineages, different from Trichobilharzia, shared with Argentina. This study provides new information on Neotropical schistosomes, highlighting the need for major research on these neglected trematodes, which are considered to be emerging/re-emerging parasites in other parts of the globe as consequence of anthropogenic disturbances and climatic change. Highlights: 1. Two different lineages (Lineage I and II) were described and molecularly characterized (28S and COI genes); 2. Cercaria chilinae I y II are proposed as a synonymous of Lineage II. Thus, a total of four different lineages of avian schistosomes are related to Chilina spp.; 3. Chilina spp. represents an important intermediate host for avian schistosomes in South America, constituting a reservoir de schistosomes with zoonotic potential; 4. Coinfection between the two different lineages was found, a finding previously not reported for avian schistosomes; 5. Expansion in the geographic distribution of Nasusbilharzia melancorhypha from its original record in Argentina, with Chilina dombeyana as an additional intermediate host. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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Figure 1

Figure 1
<p>Microscopic images of the isolated lineages stained with Alum Carmine. (<b>A</b>,<b>B</b>) Lineage I. (<b>A</b>) Furcocercaria <span class="html-italic">in toto</span>, note the similar length of body and tail stem. (<b>B</b>) Well-developed penetration organ in the anterior third of the body with its prominent musculature, which is evident at its base (arrowhead). Note the pigmented eye spots (white arrowhead) posterior to penetration organ. Inserted image: Note the genital primordium (arrowhead) located almost immediately to the posterior border of the acetabulum (asterisk). (<b>C</b>,<b>D</b>) Lineage II. (<b>C</b>) Furcocercaria <span class="html-italic">in toto</span>, note the difference between the length of body and tail stem, which is almost two-fold. (<b>D</b>) Anterior third of body where the penetration organ is evident (arrowhead); however, its muscular development is less when compared with Lineage I. Note the pigmented eye spots (white arrowhead) posterior to penetration organ. Inserted image: Note the evident distance between the acetabulum (asterisk) and the genital primordium (arrowhead), which is situated caudal to the latter, near the posterior end of body.</p>
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<p>SEM images of Lineage I. (<b>A</b>) The penetration organ with a pair of papilla-like structures on the border of the organ (arrowhead). (<b>B</b>) The body cuticle with a porous appearance (asterisk), clearly seen posterior to the acetabulum. (<b>C</b>) The acetabulum is covered on its tip with small, densely grouped spines (arrowhead), which contrasts with the rest of the acetabulum where no spines were seen. (<b>D</b>,<b>E</b>) Posterior third of the body where spines gradually disappear (arrowheads) until they are not seen on the posterior border. (<b>E</b>) Additionally, note the larger spines of the tail stem in comparison with those from the body. (<b>F</b>) The tail stem with a delicate honeycomb-shaped mesh over its tegument.</p>
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<p>SEM images of Lineage II. (<b>A</b>) Ventral view of the body of furcocercariae completely covered with small spines over its tegument. (<b>B</b>) Apical view of the penetration organ with its glandular apertures (arrowhead) and some glandular content over these (asterisks). (<b>C</b>) The basal portion of the penetration organ where these two apertures were seen likely bore small cilia (arrowhead). (<b>D</b>) Inverted acetabulum with some small spines over its border (black arrowhead). Note the presence of two patches lacking spines—one anterior and the other posterior to the acetabulum (asterisks). At the basis of acetabulum, a pair of papillae-like structures are seen (white arrowheads). (<b>E</b>) At the anterior third of the tail stem, a small area lacking spines is evident (arrowhead). (<b>F</b>) Detail of the delicate, honeycomb-shaped mesh over the tegument of the tail stem, which is also seen in (<b>E</b>).</p>
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<p>Maximum likelihood (ML) phylogenetic tree for a subset of schistosomes sequences for (<b>A</b>) 28S and (<b>B</b>) COI genes. (<b>A</b>) This phylogeny was inferred using an alignment of 1699 bp. Calculated substitution models for ML and BI were GTR+F+G4, and <span class="html-italic">M</span><sub>203</sub>, <span class="html-italic">M</span><sub>198</sub>, and <span class="html-italic">M</span><sub>200</sub>, respectively. The best models were chosen using the Bayesian Information Criterion (BIC). (<b>B</b>) This phylogeny was inferred using an alignment of 1188 bp. Calculated substitution models for ML and BI were as follows: TIM2+F+I+G4 (part1), GTR+F+I+G4 (part2), and TIM2+F+I+G4 (part3); <span class="html-italic">M</span><sub>201</sub>, <span class="html-italic">M</span><sub>138</sub>, <span class="html-italic">M</span><sub>162</sub>, <span class="html-italic">M</span><sub>189</sub>, <span class="html-italic">M</span><sub>203</sub>, <span class="html-italic">M</span><sub>134</sub>, and <span class="html-italic">M</span><sub>193</sub> (part1); <span class="html-italic">M</span><sub>29</sub>, <span class="html-italic">M</span><sub>92</sub>, <span class="html-italic">M</span><sub>68</sub>, <span class="html-italic">M</span><sub>71</sub>, <span class="html-italic">M</span><sub>81</sub>, <span class="html-italic">M</span><sub>54</sub>, and <span class="html-italic">M</span><sub>180</sub> (part2); and <span class="html-italic">M</span><sub>125</sub>, <span class="html-italic">M</span><sub>191</sub>, <span class="html-italic">M</span><sub>193</sub>, <span class="html-italic">M</span><sub>200</sub>, <span class="html-italic">M</span><sub>189</sub>, <span class="html-italic">M</span><sub>203</sub>, <span class="html-italic">M</span><sub>166</sub>, and <span class="html-italic">M</span><sub>64</sub> (part3), respectively. The best models were chosen using the Bayesian Information Criterion (BIC). (<b>A</b>,<b>B</b>) Bootstrap values ≥ 70 (left) and posterior probabilities ≥ 0.7 (right) are presented at every node. An asterisk (*) indicates full support (100/1). The generated sequences in the present study are highlighted in bold. Outgroups with more than two sequences were collapsed with the number of sequences detailed between parentheses.</p>
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<p>Maximum likelihood (ML) phylogenetic tree for a subset of schistosomes sequences for 28S-COI concatenated genes. This phylogeny was inferred using an alignment of 2894 bp. Calculated substitution models for ML and BI were as follows: GTR+F+I+G4 (nonCoding), TIM2+F+I+G4 (part1), GTR+F+I+G4 (part2), and TIM2+F+I+G4 (part3); <span class="html-italic">M</span><sub>177</sub>, <span class="html-italic">M</span><sub>198</sub>, <span class="html-italic">M</span><sub>195</sub>, and <span class="html-italic">M</span><sub>203</sub> (nonCoding); <span class="html-italic">M</span><sub>138</sub>, <span class="html-italic">M</span><sub>201</sub>, <span class="html-italic">M</span><sub>162</sub>, <span class="html-italic">M</span><sub>189</sub>, <span class="html-italic">M</span><sub>203</sub>, <span class="html-italic">M</span><sub>193</sub>, and <span class="html-italic">M</span><sub>134</sub> (part1); <span class="html-italic">M</span><sub>29</sub>, <span class="html-italic">M</span><sub>54</sub>, <span class="html-italic">M</span><sub>68</sub>, <span class="html-italic">M</span><sub>81</sub>, <span class="html-italic">M</span><sub>145</sub>, and <span class="html-italic">M</span><sub>160</sub> (part2); and <span class="html-italic">M</span><sub>166</sub>, <span class="html-italic">M</span><sub>191</sub>, <span class="html-italic">M</span><sub>125</sub>, <span class="html-italic">M</span><sub>200</sub>, and <span class="html-italic">M</span><sub>203</sub> (part3), respectively. The best models were chosen using the Bayesian Information Criterion (BIC). Bootstrap values ≥ 70 (left) and posterior probabilities ≥ 0.7 (right) are presented at every node. An asterisk (*) indicates full support (100/1). The generated sequences in the present study are highlighted in bold. Outgroups with more than two sequences were collapsed with the number of sequences detailed between parentheses.</p>
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<p>Map of the regions considered in the present study, specifying the sampled locations.</p>
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13 pages, 26562 KiB  
Review
Clinical Spectrum of Schistosomiasis: An Update
by Cristina Carbonell, Beatriz Rodríguez-Alonso, Amparo López-Bernús, Hugo Almeida, Inmaculada Galindo-Pérez, Virginia Velasco-Tirado, Miguel Marcos, Javier Pardo-Lledías and Moncef Belhassen-García
J. Clin. Med. 2021, 10(23), 5521; https://doi.org/10.3390/jcm10235521 - 25 Nov 2021
Cited by 31 | Viewed by 8151
Abstract
Schistosomiasis is a helminthic infection and one of the neglected tropical diseases (NTDs). It is caused by blood flukes of the genus Schistosoma. It is an important public health problem, particularly in poverty-stricken areas, especially those within the tropics and subtropics. It is [...] Read more.
Schistosomiasis is a helminthic infection and one of the neglected tropical diseases (NTDs). It is caused by blood flukes of the genus Schistosoma. It is an important public health problem, particularly in poverty-stricken areas, especially those within the tropics and subtropics. It is estimated that at least 236 million people worldwide are infected, 90% of them in sub-Saharan Africa, and that this disease causes approximately 300,000 deaths annually. The clinical manifestations are varied and affect practically all organs. There are substantial differences in the clinical presentation, depending on the phase and clinical form of schistosomiasis in which it occurs. Schistosomiasis can remain undiagnosed for a long period of time, with secondary clinical lesion. Here, we review the clinical profile of schistosomiasis. This information may aid in the development of more efficacious treatments and improved disease prognosis. Full article
(This article belongs to the Special Issue Epidemiology, Immunology, and Control of Schistosomiasis)
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<p>Main clinical manifestations of schistosomiasis (acute vs. chronic).</p>
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<p>Intestinal schistosomiasis. Elevated yellow nodules and granular changes in colon suggestive of chronic colitis.</p>
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<p>Eggs of <span class="html-italic">S. mansoni</span> present in the intestinal tract and granuloma (×40).</p>
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<p>Splenic alargement due chronic schistosomiasis in a sub-Saharan patient.</p>
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<p>Fibrosis and calcifications in bladder tissue (×20).</p>
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<p>Terminal hematuria due <span class="html-italic">S. haematobium</span> in a young man from Mali.</p>
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16 pages, 1576 KiB  
Article
First Record of Trichobilharzia physellae (Talbot, 1936) in Europe, a Possible Causative Agent of Cercarial Dermatitis
by Nikolaus Helmer, Hubert Blatterer, Christoph Hörweg, Susanne Reier, Helmut Sattmann, Julia Schindelar, Nikolaus U. Szucsich and Elisabeth Haring
Pathogens 2021, 10(11), 1473; https://doi.org/10.3390/pathogens10111473 - 12 Nov 2021
Cited by 12 | Viewed by 3920
Abstract
Several species of avian schistosomes are known to cause dermatitis in humans worldwide. In Europe, this applies above all to species of the genus Trichobilharzia. For Austria, a lot of data are available on cercarial dermatitis and on the occurrence of Trichobilharzia [...] Read more.
Several species of avian schistosomes are known to cause dermatitis in humans worldwide. In Europe, this applies above all to species of the genus Trichobilharzia. For Austria, a lot of data are available on cercarial dermatitis and on the occurrence of Trichobilharzia, yet species identification of trematodes in most cases is doubtful due to the challenging morphological determination of cercariae. During a survey of trematodes in freshwater snails, we were able to detect a species in the snail Physella acuta (Draparnaud, 1805) hitherto unknown for Austria, Trichobilharzia physellae; this is also the first time this species has been reported in Europe. Species identification was performed by integrative taxonomy combining morphological investigations with molecular genetic analyses. The results show a very close relationship between the parasite found in Austria and North American specimens (similarity found in CO1 ≥99.57%). Therefore, a recent introduction of T. physellae into Europe can be assumed. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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<p>Photomicrographs of two of the measured <span class="html-italic">Trichobilharzia physellae</span> cercariae elucidated by glycerol and stained by borax carmine. Left = ventral, right = lateral. Scale = 100 µm.</p>
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<p>Maximum likelihood (ML) tree of <span class="html-italic">Trichobilharzia</span> species based on mitochondrial <span class="html-italic">cytochrome c oxidase subunit 1</span> gene (<span class="html-italic">CO1</span>) sequences. The Bayesian Inference (BI) tree had the same topology. Bootstrap values ≥70 % (right, in %) and posterior probabilities ≥90 (left) are presented at the nodes. A star indicates full support (100/100). All species except <span class="html-italic">T. physellae</span> are presented as collapsed nodes (if more than one sequence is present). Sequences obtained in this study are in bold. The size of the collapsed nodes reflects the number of sequences (2–5), which is also given in parentheses behind the species names.</p>
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<p>Median-joining network (MJ) based on <span class="html-italic">CO1</span> sequences of <span class="html-italic">T. physellae</span>. NCBI GenBank accession numbers/specimen Lab-IDs representing different haplotypes are given near the dots. The central shared haplotype consists of FJ174514.1, FJ174515.1, FJ174518.1, and FJ174523.1. Haplotypes from the USA were coded at the level of the U.S. states. All haplotypes are marked in different colors and are constituted of one to four sequences (representative circle sizes in the legend). Sequences obtained in the present study are in bold. Orthogonal lines on the connecting lines between the haplotypes indicate the number of mutation steps; black dots indicate missing haplotypes.</p>
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10 pages, 1395 KiB  
Brief Report
Invaders as Diluents of the Cercarial Dermatitis Etiological Agent
by Anna Stanicka, Łukasz Migdalski, Katarzyna Szopieray, Anna Cichy, Łukasz Jermacz, Paola Lombardo and Elżbieta Żbikowska
Pathogens 2021, 10(6), 740; https://doi.org/10.3390/pathogens10060740 - 11 Jun 2021
Cited by 9 | Viewed by 2492
Abstract
Research on alien and invasive species focuses on the direct effects of invasion on native ecosystems, and the possible positive effects of their presence are most often overlooked. Our aim was to check the suitability of selected alien species (the snail Physa acuta [...] Read more.
Research on alien and invasive species focuses on the direct effects of invasion on native ecosystems, and the possible positive effects of their presence are most often overlooked. Our aim was to check the suitability of selected alien species (the snail Physa acuta, the bivalve Dreissena polymorpha, and the gammarid Dikerogammarus villosus) as diluents for infectious bird schistosome cercariae—the etiological factor of swimmer’s itch. It has been hypothesized that alien species with different feeding habits (scrapers, filterers and predators) that cohabit the aquatic environment with intermediate hosts of the schistosomatid trematodes are capable of feeding on their free-swimming stages—cercariae. In the laboratory conditions used, all experimental animals diluted the cercariae of bird schistosome. The most effective diluents were P. acuta and D. villosus. However, a wide discrepancy in the dilution of the cercariae between replicates was found for gammarids. The obtained results confirm the hypothesis that increased biodiversity, even when alien species are involved, creates the dilution effect of the free-living stages of parasites. Determining the best diluent for bird schistosome cercariae could greatly assist in the development of current bathing areas protection measures against swimmer’s itch. Full article
(This article belongs to the Special Issue Advances in Avian Schistosomes and Cercarial Dermatitis)
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<p>Schematic diagram of the experimental procedure.</p>
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<p>Bird schistosome cercariae in beakers (ind/mL, mean values ± SE, <span class="html-italic">n</span> = 3 for each tested replicate) before and after exposure to following experimental invertebrate species: (<b>A</b>) <span class="html-italic">Physa acuta</span> (5 specimens), (<b>B</b>) <span class="html-italic">Dreissena polymorpha</span> (5 specimens), (<b>C</b>) <span class="html-italic">Dikerogammarus villosus</span> (3 specimens).</p>
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<p>Average densities of bird schistosome cercariae remaining (%) after exposure to following experimental invertebrate species: (<b>A</b>) <span class="html-italic">Physa acuta</span> (5 specimens), (<b>B</b>) <span class="html-italic">Dreissena polymorpha</span> (5 specimens), (<b>C</b>) <span class="html-italic">Dikerogammarus villosus</span> (3 specimens).</p>
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11 pages, 1884 KiB  
Article
Descriptive Pathological Study of Avian Schistosomes Infection in Whooper Swans (Cygnus cygnus) in Japan
by Mohamed S. Ahmed, Reda E. Khalafalla, Ashraf Al-Brakati, Tokuma Yanai and Ehab Kotb Elmahallawy
Animals 2020, 10(12), 2361; https://doi.org/10.3390/ani10122361 - 10 Dec 2020
Cited by 3 | Viewed by 3046
Abstract
Cercarial dermatitis, or Swimmer’s itch, is one of the emerging diseases caused by the cercariae of water-borne schistosomes, mainly Trichobilharzia spp. Since the zoonotic potential of Allobilharzia visceralis is still unknown, studies on this schistosome would be helpful to add knowledge on its [...] Read more.
Cercarial dermatitis, or Swimmer’s itch, is one of the emerging diseases caused by the cercariae of water-borne schistosomes, mainly Trichobilharzia spp. Since the zoonotic potential of Allobilharzia visceralis is still unknown, studies on this schistosome would be helpful to add knowledge on its possible role in causing human infections. In the present study, 54 whooper swans (Cygnus cygnus) from rescue/rehabilitation centers in Honshu, Japan, were necropsied to identify the cause of death. Grossly, 33 (61.11%) swans were severely emaciated and 23 (42.59%) had multiple reddened areas throughout the length of the intestine with no worms detected in the internal organs. Microscopically, adult schistosomes were found in the lumen of the mesenteric, serosal, portal, and testicular veins, in the capillaries of the intestinal lamina propria, and in the sinusoids of the adrenal gland, spleen, and liver of 23 (42.59%) swans. Hypertrophy of veins containing adult worms was identified in 15 (27.77%) swans, and vascular lumen obliteration was observed in 8 (14.81%) swans. Mild to severe villous atrophy and superficial enteritis were observed in 8 birds (14.81%), whereas bile pigments and hemosiderin were detected in the livers of 14 (25.92%) and 18 (33.33%) swans, respectively. In three swans (5.55%), schistosome parasites were found in the subcapsular veins of the testes. The schistosomes in the present study were assumed to be A. visceralis based on the microscopical and histological evidence of adult schistosomes found in the lumen of veins as well as the infection pathology, which was very similar to the schistosome-induced pathology previously reported in swans infected by A. visceralis in Europe and Australia. The swans examined herein most likely died from obstructive phlebitis associated with A. visceralis, but further molecular confirmation is required for identification of this species. However, the present study does not provide new data on the zoonotic potential, but only on the pathogenic potential of this schistosome in swans. Furthermore, our study provides a novel contribution to the description of the pathological effects of avian schistosomes infection in whooper swans in Japan. Full article
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<p>Effect of the parasite in the intestine. (<b>A</b>) Adult worms (W) are seen in the thickened walls of the serosal vein (H). Note the normal thickness of the artery (black arrow). (<b>B</b>) Brownish pigment–laden macrophages (white arrow) around the worm (W) in the thickened wall of the mesenteric veins (H). (<b>C</b>) The vein lumen was almost occluded due to marked myointimal hyperplasia in the veins of the muscular layer of the intestine (white star), with perivascular inflammatory reaction (I). (<b>D</b>) Several schistosome eggs (white arrowheads) present in the intestinal lamina propria and surrounded by an inflammatory reaction of lymphocytes and plasma cells (I); the intestinal villi are markedly blunted (g). Hematoxylin and eosin stain (100×).</p>
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<p>Effect of the parasite in the liver. (<b>A</b>) Adult worms (W) present in the thickened walled of the portal vein (H) with hemosiderin pigment deposition (white arrow) and bile duct hyperplasia (b). (<b>B</b>) Schistosome parasite (W) found in the hepatic sinusoids surrounded by degenerated hepatocyte (d) and massive inflammatory reaction (I). Hematoxylin and eosin stain (100×). (<b>C</b>) Emerald green–colored clumps of bile pigment (bi), Hall stain (400×). (<b>D</b>) Macrophages laden with bluish pigment (He), Berlin blue stain (100×).</p>
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<p>Effect of the parasite in the adrenal gland, spleen, and testis. (<b>A</b>, <b>B</b>) Multiple cross-sections of adult worms (W) found in the sinusoids of the adrenal gland surrounded by infiltration of mononuclear inflammatory cells (I). (<b>C</b>) Adult worms (W) found in the splenic veins. Note the oral sucker (Os) and acetabulum (Ac) of the parasite. (<b>D</b>) Multiple cross-sections of adult schistosomes (W) completely occlude the subcapsular veins of the testis and were surrounded by the infiltration of mononuclear inflammatory cells (I). Note the seminal vesicles of the parasite (Sv) and the presence of female (f) in the ventral groove of the male (m) parasite. Hematoxylin and eosin stain (100×).</p>
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