Rodents as intermediate hosts of cestode parasites of mammalian carnivores and birds of prey in Poland, with the first data on the life-cycle of Mesocestoides melesi.

BACKGROUND: Rodents constitute an important part of the diet of many carnivore species. This predator-prey food chain is exploited by helminth parasites, such as cestodes, whose larval stages develop in rodents and then mature to the adult stage in predators. The main aim of our study was to use molecular techniques for identification of cestode species recovered from both intermediate and definitive hosts, with a particular focus on the genus Mesocestoides. METHODS: Larval cestodes were obtained during our long-term studies on rodent helminth communities in the Mazury Lake District in the north-east Poland in 2000-2018. Cestode larvae/cysts were collected from body cavities or internal organs (e.g. liver) during autopsies. Adult tapeworms were derived from nine red foxes, three Eurasian badgers and one Eurasian lynx. PCR amplification, sequencing and phylogenetic analyses were conducted employing three genetic markers: 18S rDNA, mitochondrial (mt) 12S rDNA and the mt cytochrome c oxydase subunit 1 (cox1) gene fragment. RESULTS: Altogether 19 Mesocestoides samples were analyzed, including 13 adult tapeworms from definitive hosts and six larval samples from 4 bank voles and 2 yellow-necked mice. Phylogenetic analyses revealed three well-supported trees of similar topology. In each case the Mesocestoides samples formed two separate clades. All isolates from foxes, the lynx isolate and two isolates from rodents grouped with Mesocestoides litteratus. Four isolates from rodents and all three isolates from Eurasian badgers were resolved in a separate clade, most similar to North American M. vogae (syn. M. corti). Examination of fixed, stained adult specimens from Eurasian badgers revealed consistency with the morphology of Mesocestoides melesi. Therefore, this clade is likely to represent M. melesi, a species first described in 1985 from the Eurasian badger Meles meles. Molecular analysis allowed also the identification of Taenia crassiceps, Hydatigera kamiyai and Cladotaenia globifera among larvae derived from rodents. CONCLUSIONS: Molecular and phylogenetic analyses support the recognition of M. melesi as a valid species. Our data represent the first record of the larvae of this species in rodents. This is the first report on the occurrence of H. kamiyai in rodents from Poland.

The forgotten exotic tapeworms: a review of uncommon zoonotic Cyclophyllidea.

As training in helminthology has declined in the medical microbiology curriculum, many rare species of zoonotic cestodes have fallen into obscurity. Even among specialist practitioners, knowledge of human intestinal cestode infections is often limited to three genera, Taenia, Hymenolepis and Dibothriocephalus. However, five genera of uncommonly encountered zoonotic Cyclophyllidea (Bertiella, Dipylidium, Raillietina, Inermicapsifer and Mesocestoides) may also cause patent intestinal infections in humans worldwide. Due to the limited availability of summarized and taxonomically accurate data, such cases may present a diagnostic dilemma to clinicians and laboratories alike. In this review, historical literature on these cestodes is synthesized and knowledge gaps are highlighted. Clinically relevant taxonomy, nomenclature, life cycles, morphology of human-infecting species are discussed and clarified, along with the clinical presentation, diagnostic features and molecular advances, where available. Due to the limited awareness of these agents and identifying features, it is difficult to assess the true incidence of these 'forgotten' cestodiases as clinical misidentifications are likely to occur. Also, the taxonomic status of many of the human-infecting species of these tapeworms is unclear, hampering accurate species identification. Further studies combining molecular data and morphological observations are necessary to resolve these long-standing taxonomic issues and to elucidate other unknown aspects of transmission and ecology.

Cestode infections in non-human primates suggest the existence of zoonotic cycles in the area surrounding the Strasbourg primatology center.

BACKGROUND: Several cases of infections due to Echinococcus multilocularis, Taenia martis and Taenia crassiceps were recently described in various species of captive non-human primates (NHPs) harbored in the Strasbourg Primate Center (SPC). Furthermore, one of the first cases of human cysticercosis due to T. martis was described in the Strasbourg region. These data suggest the existence of zoonotic cycles of tapeworm infections in the direct environment of the SPC. The aim of our study was to assess the prevalence of larval cestode infections among intermediate and definitive hosts in the close neighborhood of the center. We analyzed carnivore mammal fecal samples as well as rodent carcasses, collected inside or near the SPC, using PCR. Furthermore, we performed serology for Echinococcus spp. and Taenia spp. on NHP sera. RESULTS: We found that 14.5% (95% CI [8.6; 20.4]) of 138 carnivore feces were positive for E. multilocularis-DNA, as well as 25% (95% CI [5.5; 57.2]) of 12 rodent carcasses, and 5.1% (95% CI [1.4; 8.7]) for T. martis or T. crassiceps. Of all NHPs tested, 10.1% (95% CI [3.8; 16.4]) were seropositive for Echinococcus spp. and 8.2% (95% CI [1.3; 15.1]) for Taenia spp. CONCLUSIONS: Our data support the existence of zoonotic cycles of larval cestode infections in the direct environment of the primatology center affecting NHPs harbored in the SPC, potentially threatening the human population living in this area. Since this zoonotic risk is borne by local wildlife, and given the severity of these infections, it seems necessary to put in place measures to protect captive NHPs, and further studies to better assess the risk to human populations.

Revealing trophic transmission pathways of marine tapeworms.

Parasites are important components of natural systems, and among their various roles, parasites strongly influence the flow of energy between and within food webs. Over 1000 tapeworm species are known to parasitise elasmobranchs, although full life cycles are resolved for fewer than 10 of them. The lack in resolution stems from the inability to distinguish larval from adult stages using morphology alone. Molecular elucidation of trophic transmission pathways is the next step in understanding the role of hosts and parasites within food webs. We investigated the parasite assemblage of New Zealand's rough skate, Zearaja nasuta. Skates and their prey items (obtained from the skates' stomachs) were dissected for the recovery of adult and larval tapeworms, respectively. A fragment of the 28S rDNA region was amplified for worm specimens with the aim to confirm species identity of parasites within rough skates and to uncover trophic transmission pathways that exploit the predation links between rough skates and their prey. We identified seven species of tapeworms from four tapeworm orders. Four trophic transmission pathways were resolved between three prey items from skates stomachs and skates, and one pathway between larval tapeworm sequence from a New Zealand sole and skate, i.e. a genetic match was found between larval tapeworms in prey and adult worms in skates. We report the first case of an adult trypanorhynch parasitising rough skate. These findings contribute to our limited understanding of cestode life cycles as well as providing insights into the importance of predator-prey relationships for parasite transmission.

Raillietiniaisis in a Toddler From Hawaii: A Case of Mistaken Tapeworm Identity.

We present the first reported case from the United States of human infection with the intestinal cestode Raillietina, a parasite primarily of rodents and poultry. As the differential diagnosis between the morphologically similar Dipylidium caninum was challenging, we discuss the biology, epidemiology, and clinical management of this rare parasite.

Topical or oral fluralaner efficacy against flea (Ctenocephalides felis) transmission of Dipylidium caninum infection to dogs.

BACKGROUND: Dipylidium caninum is a common tapeworm of dogs contracted from ingestion of fleas containing the infective cysticercoid stage. Fluralaner is a systemically distributed isoxazoline class insecticide that delivers highly effective activity against fleas and ticks for up to 12 weeks after a single oral or topical treatment. This study evaluated the impact of this flea insecticidal efficacy on the transmission of D. caninum to dogs. METHODS: Dogs were weighed and treated with a cestocide and then randomly assigned to 3 groups of 8. Fluralaner was administered topically (at the commercial dose) to one group and orally to another group while the third received topically administered sterile water. All dogs were subsequently infested with about 100 D. caninum infected Ctenocephalides felis at 7, 14, 21, 28, 35, 42, 49, 56, 63, 70, 77 and 83 days after treatment. Visual proglottid inspections and counts were conducted daily from 35 to 113 days post-treatment. Post-treatment D. caninum incidence was calculated for each group and compared between treated and untreated groups. RESULTS: All 8 dogs in the placebo-treated group became infected with D. caninum while no shed proglottids were observed at any point during the post-treatment period from any dog in either fluralaner treated group. CONCLUSIONS: The insecticidal efficacy of a single treatment of either orally or topically administered fluralaner prevented D. caninum transmission from infected fleas to susceptible dogs for up to 12 weeks following administration.

Tour around the globe: The case of invasive tapeworm Atractolytocestus huronensis (Cestoda: Caryophyllidea), a parasite of common carp.

The monozoic tapeworm Atractolytocestus huronensis Anthony, 1958 (Cestoda: Caryophyllidea), an intestinal parasite of the common carp, is characterized by its invasive character and potential to colonize new territories. It was initially described from North America and has also been found in several European countries. The most recent findings of A. huronensis originated from China and South Africa; however, no data on genetic relationships of these populations were available. The current study provides the first molecular characterisation of A. huronensis from South Africa and China using a partial sequence of mitochondrial cytochrome c oxidase subunit 1 (cox1) and a complete ribosomal ITS2 spacer. Ribosomal and mitochondrial data were applied for phylogenetic analyses in order to assess the genetic interrelationships among global A. huronensis populations. Divergent intragenomic copies of ribosomal ITS2 were detected in all analysed specimens; the structure and frequency of the ITS2 variants of tapeworms from China and South Africa corresponded with the data on ITS2 paralogues observed previously in A. huronensis from Slovakia, the United States and the United Kingdom. The phylogenetic analysis of cox1 indicated that A. huronensis exist in two slightly differentiated clusters; one cluster was supported by all phylogenetic approaches (NJ, ML, BI) and was represented by samples from China, the USA and the UK. A second cluster was represented by tapeworms from continental Europe (Slovakia, Hungary, Romania, Croatia) and South Africa. Haplotype network analysis revealed that the highest population diversity occurs in China. The results provide useful pilot information about the interrelationships of A. huronensis on four continents and indicate that China, or the eastern Palaearctic, served as the original source population for the global expansion of this invasive tapeworm. Data on the origin and distribution of the common carp, the only specific host of A. huronensis, are also discussed.

Plerocercoids of the cestode Diphyllobothrium ditremum in brown trout Salmo trutta: substantial increase in infection after establishment of European minnow Phoxinus phoxinus.

This study focuses on plerocercoids of the cestode Diphyllobothrium ditremum in brown trout Salmo trutta from the subalpine lake Øvre Heimdalsvatn in south-central Norway. Salmo trutta was the only fish species in this lake until European minnow Phoxinus phoxinus was registered in 1969. The P. phoxinus population increased substantially in the following years. In contrast with the 1969-1972 period, when plerocercoids of D. ditremum were practically absent in S. trutta, there was a high prevalence and intensity of infection in the 2013 S. trutta samples. Because the life cycle of D. ditremum involves two larval stages, in copepods and salmonids and mature worms in piscivorous birds, such as mergansers and loons, a change in feeding ecology of S. trutta or changes in population densities of copepods, fish or birds might have influenced the infection pattern. No relationships between D. ditremum infection and muscle-tissue δ15 N signature or Hg concentration were found, indicating that infection is not a result of piscivory or cannibalism. Furthermore, consumption of copepods by S. trutta during summer and autumn was low. On the other hand, the number of piscivorous birds has increased, probably due to the presence of P. phoxinus as a new and numerous prey. An increased number of final D. ditremum hosts may have produced a higher output of cestode eggs, resulting in more infected copepods that in turn are consumed by S. trutta. Indirectly, P. phoxinus may therefore have caused the observed increased infection in S. trutta and thereby imposed further negative effects on S. trutta in high mountain areas.

Preventive efficacy of NexGard Spectra® against Dipylidium caninum infection in dogs using a natural flea (Ctenocephalides felis) infestation model.

The efficacy of a monthly oral endectocide product, NexGard Spectra® (Merial), a combination of afoxolaner and milbemycin oxime, was evaluated in a flea (Ctenocephalides felis) challenge model for the prevention of Dipylidium caninum tapeworm infection in dogs. The efficacy of treatment with NexGard Spectra® was assessed in 10 dogs following weekly flea infestation with metacestode naturally infected fleas and compared with that in 10 untreated control dogs. The 100 fleas deposited weekly on each dog were not removed until Day 35, allowing enough time for their ingestion. The microscopical analysis of 30 fleas from the flea batches before each weekly challenge demonstrated that 10-33% of the fleas were infected by D. caninum cysticercoid larvae. The arithmetic mean flea count recorded was 47.7 for the 10 untreated dogs and 0 for the 10 treated dogs at Day 35. Based on the daily collection of expelled D. caninum proglottids by dogs during the 70 days of the study, 70% (7/10) of the control dogs and 0% (0/10) of the treated dogs were infected with D. caninum (p < 0.0031). Through its efficacy against fleas, NexGard Spectra® treatment provided indirect prevention of D. caninum infestation. No treatment-related adverse events were observed in dogs during this study.

To each his own: no evidence of gyrodactylid parasite host switches from invasive poeciliid fishes to Goodea atripinnis Jordan (Cyprinodontiformes: Goodeidae), the most dominant endemic freshwater goodeid fish in the Mexican Highlands.

BACKGROUND: Goodeid topminnows are live-bearing fishes endemic to the Mexican Highlands (Mesa Central, MC). Unfortunately, in the MC, environmental degradation and introduced species have pushed several goodeid species to the brink of extinction. Invasive fishes can introduce exotic parasites, and the most abundant goodeid, blackfin goodea Goodea atripinnis Jordan, is parasitised by six exotic helminths. Poeciliids are widely dispersed invasive fishes, which exert negative ecological effects on goodeids. Poeciliids host several species of the monogenean genus Gyrodactylus von Nordmann, 1832, including pathogenic, invasive parasites. Here, we looked for evidence of Gyrodactylus species switching hosts from poeciliids to goodeids. METHODS: Fish were collected in rivers draining the MC into both sides of the continental divide. Hosts were screened for gyrodactylid parasites in localities where G. atripinnis and poeciliids occurred sympatrically. Gyrodactylus specimens were characterised morphologically (attachment apparatus) and molecularly (internal transcribed spacer region, ITS). A Bayesian phylogenetic tree using ITS sequences established relationships between gyrodactylids collected from goodeid fishes and those from parasites infecting poeciliids. RESULTS: Gyrodactylids were collected from G. atripinnis in six localities on both sides of the watershed where exotic poeciliids occurred sympatrically. Morphological and molecular analyses indicated the presence of four undescribed species of Gyrodactylus infecting this goodeid host. Gyrodactylus tomahuac n. sp., the most abundant and geographically widespread species, is described here. The other three Gyrodactylus spp. are not described, but their ITS sequences are used as molecular data presented here, are the only available for gyrodactylids infecting goodeid fishes. Morphological and molecular data suggest that two distinct groups of gyrodactylids infect goodeids, one of which shares a common ancestor with gyrodactylids parasitizing poeciliids. CONCLUSIONS: No evidence was found of gyrodactylids switching hosts from invasive poeciliids to endemic goodeids, nor vice versa. Moreover, considering that G. atripinnis is known to host both Gyrodactylus lamothei Mendoza-Palmero, Sereno-Uribe & Salgado-Maldonado, 2009 and Gyrodactylus mexicanus Mendoza-Palmero, Sereno-Uribe & Salgado-Maldonado, 2009, with the addition of G. tomahuac n. sp. and the three undescribed Gyrodactylus spp. reported, at least six gyrodactylids may infect this host. This would make monogeneans the second most abundant parasite group infecting G. atripinnis, which to date is known to harbour 22 helminth species: nine digeneans, five nematodes, four cestodes, three monogeneans and one acanthocephalan.

Parasitism by larval tapeworms genus Spirometra in South American amphibians and reptiles: new records from Brazil and Uruguay, and a review of current knowledge in the region.

Spargana are plerocercoid larvae of cestode tapeworms of the genus Spirometra, Family Diphyllobothriidae, parasitic to frogs, reptiles, birds and mammals. This parasitic disease in humans can be transmitted through the use and consumption of amphibians and reptiles. The available knowledge about Spirometra in South America is scarce, and there are only a few reports on the occurrence of sparganum in amphibians and reptiles, many of them published in old papers not easily available to researchers. In this work we present a review on this topic, provide new records in two species of amphibians and 7 species of reptiles from Brazil and Uruguay respectively. We also summarize current knowledge of Spirometra in the continent, along with an updated of host taxonomy. We could gather from the literature a total of 15 studies about amphibian and reptile hosts, published between 1850 and 2016, corresponding to 43 case reports, mostly from Brazil (29) and Uruguay (8), Argentina (3), Peru (2), and Venezuela (1); the majority of them related to reptiles (five lizards and 26 snake species), and 14 corresponded to amphibians (9 anurans). Plerocercoid larvae were located in different organs of the hosts, such as subcutaneous tissue, coelomic cavity, peritoneum, and musculature. The importance of amphibians and reptiles in the transmission of the disease to humans in South America is discussed. Relevant issues to be studied in the near future are the taxonomic characterization of Spirometra in the region and the biological risk of reptile meat for aboriginal and other rural communities.

Definitive Hosts of Versteria Tapeworms (Cestoda: Taeniidae) Causing Fatal Infection in North America.

We previously reported fatal infection of a captive Bornean orangutan with metacestodes of a novel taeniid tapeworm, Versteria sp. New data implicate mustelids as definitive hosts of these tapeworms in North America. At least 2 parasite genetic lineages circulate in North America, representing separate introductions from Eurasia.

New evidence of a lateral transfer of monogenean parasite between distant fish hosts in Lake Ossa, South Cameroon: the case of Quadriacanthus euzeti n. sp.

Species of the monogenean genus Quadriacanthus mainly infect fish belonging to the Siluriformes, especially the genera Clarias, Heterobranchus or Bagrus, and their host specificity is strict (oioxenous) or narrow (stenoxenous). An examination of the gills of 19 Papyrocranus afer from Lake Ossa, South Cameroon, revealed for the first time the presence of a species of Quadriacanthus from a fish host belonging to the Notopteridae. The morphology and the size of sclerotized parts of haptor and the male and female copulatory complexes suggest that this monogenean is a new species named Quadriacanthus euzeti n. sp. The fish genus Papyrocranus differs taxonomically from the usual fish hosts of Quadriacanthus and hence the presence of a species belonging to this genus on the gills of this host suggests the occurrence of a lateral transfer of Quadriacanthus from species belonging to Clarias or Bagrus which live sympatrically with P. afer in Lake Ossa.

Invaded Invaders: Infection of Invasive Brown Treesnakes on Guam by an Exotic Larval Cestode with a Life Cycle Comprised of Non-Native Hosts.

BACKGROUND: Multiple host introductions to the same non-native environment have the potential to complete life cycles of parasites incidentally transported with them. Our goal was to identify a recently detected parasitic flatworm in the invasive Brown Treesnake (Boiga irregularis) on the remote Pacific island of Guam. We considered possible factors influencing parasite transmission, and tested for correlations between infection status and potential indicators of host fitness. We used genetic data from the parasite and information about the native ranges of other possible non-native hosts to hypothesize how it arrived on Guam and how its life cycle may be currently supported. METHODS: We identified the parasite by comparing larval morphology and mtDNA sequences with other Pseudophyllid tapeworms. We assessed probability of infection in individual snakes using logistic regression and examined different factors influencing presence of parasites in hosts. RESULTS: We identified the parasite as the pseudophyllid cestode Spirometra erinaceieuropaei, with all sampled worms from multiple snakes sharing a single mtDNA haplotype. Infection appears to be limited to the only freshwater watershed on the island, where infection prevalence was high (77.5%). Larger snakes had a higher probability of being infected, consistent with the chronic nature of such infections. While infection status was positively correlated with body condition, infected snakes tended to have lower intra-peritoneal fat body mass, potentially indicating a negative effect on energy stores. CONCLUSIONS: We discovered that B. irregularis inhabiting a small area of forested habitat in a freshwater watershed on Guam are often infected by a novel parasite of Asian origin. While further work is needed, this species of Spirometra, itself a non-native species, likely depends on a suite of recently introduced hosts from different parts of the world to complete the life cycle. This baseline study provides little evidence of any effects on host fitness, but additional data are needed to more thoroughly explore the consequences of infection in this invasive snake population.

Helminths and helminthoses in Central Europe: diseases caused by cestodes (tapeworms).

The second part of the overview "Helminths and helminthoses in Central Europe" is dedicated to the cestodes (tapeworms) and the diseases caused by cestodes. The overview comprises the spectrum of the most relevant species, describes their incidence, geographic distribution and the most important clinical symptoms and highlights the possibilities of diagnosis, treatment and prophylaxis of cestode-caused diseases.

[Dipylidium caninum infection in an infant: one case report].

This paper reports the diagnosis and therapy of one case of Dipylidium caninum infection in an infant.

Culinary delights and travel? A review of zoonotic cestodiases and metacestodiases.

Due to increased globalization, food-borne parasitic infections are becoming more prevalent worldwide, including in countries where these parasites and parasitic diseases had previously been well controlled or eradicated. Improved sanitation, health education, and establishment of appropriate food safety mechanisms can go a long way towards the control of many these infections. However, food-borne parasitic infections are still common diseases in developing countries, especially in rural areas. As many of today's travelers are looking to explore more distant locations and partake in the local cuisine, they may be at greater risk of acquiring a food-borne parasitic infection, including those caused by a number of adult and larval tapeworms. This review discusses fish and meat-borne tapeworms and zoonotic metacestodiases of public health importance to both developing and developed countries, with a focus on infection prevention in travelers.

Spirometra (Pseudophyllidea, Diphyllobothriidae) severely infecting wild-caught snakes from food markets in Guangzhou and Shenzhen, Guangdong, China: implications for public health.

Sparganosis is a zoonotic disease caused by the spargana of Spirometra, and snake is one of the important intermediate hosts of spargana. In some areas of China, snake is regarded as popular delicious food, and such a food habit potentially increases the prevalence of human sparganosis. To understand the prevalence of Spirometra in snakes in food markets, we conducted a study in two representative cities (Guangzhou and Shenzhen), during January-August 2013. A total of 456 snakes of 13 species were examined and 251 individuals of 10 species were infected by Spirometra, accounting for 55.0% of the total samples. The worm burden per infected snake ranged from 1 to 213, and the prevalence in the 13 species was 0∼96.2%. More than half (58.1%) of the spargana were located in muscular tissue, 25.6% in subcutaneous tissue, and 16.3% in coelomic cavity. The results indicated that Spirometra severely infected snakes in food markets in Guangzhou and Shenzhen, implying that eating snakes has great health risk and improper cooking methods may increase the risk of Spirometra infection in humans in China. Additional steps should be considered by the governments and public health agencies to prevent the risk of snake-associated Spirometra infections in humans.