Larval Cestode Research Articles

Transmission ecology of taeniid larval cestodes in rodents in Sweden, a low endemic area for Echinococcus multilocularis.

Although local prevalence of Echinococcus multilocularis may be high, this zoonotic parasite has an overall low prevalence in foxes and rodents in Sweden. To better understand opportunities for E. multilocularis transmission in the Swedish environment, the aim of this study was to investigate other taeniid cestodes and to relate observed patterns to E. multilocularis. Cestode parasites were examined in fox feces and rodents caught in different habitats from four regions of Sweden. Arvicola amphibius and Microtus agrestis were parasitized with Versteria mustelae, Hydatigera taeniaeformis s. l., and E. multilocularis, whereas Myodes glareolus and Apodemus spp. were parasitized with V. mustelae, Taenia polyacantha, H. taeniaeformis s.l., and Mesocestoides spp. Rodents caught in field habitat (Ar. amphibius, Mi. agrestis) were more likely (OR 10, 95% CI 5-19) to be parasitized than rodents caught in forest habitat (My. glareolus, Apodemus spp.). The parasite preference for each rodent species was present regardless of the type of background contamination from fox feces. These results further support the importance of both ecological barriers and individual species susceptibility in parasite transmission, and indicate that future monitoring for E. multilocularis in the Swedish environment should focus in field habitats where Mi. agrestis and Ar. amphibius are abundant.

The role of chewing lice (Phthiraptera: Philopteridae) as intermediate hosts in the transmission of Hymenolepis microps (Cestoda: Cyclophyllidea) from the willow ptarmigan Lagopus lagopus (Aves: Tetraonidae).

The cestode Hymenolepis microps is an intestinal parasite of tetraonid birds, including the willow ptarmigan (Lagopus lagopus). This parasite is able to maintain a high prevalence and intensity throughout the year, even in a subarctic environment in bird populations with relatively low host densities, indicating effective transmission routes. Willow ptarmigan consume mainly vegetal material and active consumption of invertebrates is confined to the first two or three weeks of life. Ptarmigan are infected by different species of ectoparasites, of which two species of feather lice, Lagopoecus affinis and Goniodes lagopi, are the most abundant. In this study, we explored the hypothesis that feather lice may be suitable intermediate hosts for H. microps. We applied histological techniques and light microscopy to investigate lice for the presence of larval cestode stages (cysticercoids). We found 12 cysticercoid-like structures inside chewing lice collected on L. lagopus hosts harbouring H. microps. In addition, a polymerase chain reaction (PCR) screening of Ischnocera lice DNA, targeting the 18S rRNA gene of the cestode, showed positive results for two different short fragments of the 18S rRNA gene of H. microps which were sequenced from lice collected on birds. Both independent lines of evidence support the hypothesis that Ischnocera lice might be suitable intermediate hosts in the life cycle of H. microps in L. lagopus.

Proteolytic enzymes and their inhibitors in cestodes

The review summarizes the available published data on proteases and their inhibitors in cestodes. The intricate physiological relationships between a parasite and its host are confirmed by the ability of cestodes to produce their own proteolytic enzymes or to adsorb and utilize host proteases, on the one hand, and to secrete inhibitors of these enzymes, on the other. It is likely that the protease inhibitors primarily confront the host immune response in larval cestodes versus adult worms, living in the vertebrate intestine, where they mainly protect the parasites from hydrolysis by intestinal proteinases. In addition, the presence of the parasite in the intestine often entails changes in the activity of host proteolytic enzymes.

Using the small subunit of nuclear ribosomal DNA to reveal the phylogenetic position of the plerocercoid larvae of Spirometra tapeworms

Although medically important, the systematics of Spirometra and the taxonomic position of S. erinaceieuropaei remain unclear. In this study, the 18S rDNA gene of S. erinaceieuropaei sparganum from naturally infected frogs caught in 14 geographical locations of China was sequenced. In addition, all available 18S sequences of the family Diphyllobothriidae in the Genbank database were included to reconstruct the phylogeny of diphyllobothriid tapeworms. The secondary structure model of the 18S rDNA was also predicated to further explore the sequence variation. Phylogenetic analyses were performed using maximum parsimony (MP), maximum likelihood (ML) and Bayesian inference (BI) methods. The intraspecific divergences of 18S rDNA in Chinese sparganum isolates ranged from 0.0 to 0.4%. Regions of V2, V4 and V7 were the most variable regions in the secondary structure of 18S rDNA. With the exception of genera Duthiersia and Probothriocephalus, other genera (i.e., Adenocephalus, Diphyllobothrium, Diplogonoporus, Duthiersia, Schistocephalus and Spirometra) selected in the Diphyllobothriidae shared similar topologies of V2, V4 and V7 structures. The topology of generated phylogenetic trees revealed close relationships among Adenocephalus, Digramma, Diphyllobothrium, Diplogonoporus, Ligula, Sparganum and Spirometra. The exact phylogenetic position of Spirometra species should be further analyzed with more sampling and more useful molecular markers.

Influence of Triaenophorus nodulosus plerocercoids (Cestoda: Pseudophyllidea) on the occurrence of intestinal helminths in the perch (Perca fluviatilis).

Concurrent infections of helminths in vertebrates are widespread and may demonstrate synergistic, antagonistic or negligible levels of interactions between species that share a common site. However, indirect interactions between species that occur in different organs of a host are poorly documented, particularly in fish. Plerocercoids of Triaenophorus nodulosus are common liver infections of European perch (Perca fluviatilis). These larval cestodes cause extensive liver damage, resulting in systemic pathologies that include alteration of the physiochemical environment of the intestine. Perch harbour a wide range of intestinal helminths whose occurrence may be potentially influenced by the concurrent presence of T. nodulosus plerocercoids. The present study, using an existing dataset, investigated the effects of T. nodulosus on the infection levels of four common perch helminths - Acanthocephalus lucii, Camallanus lacustris, Proteocephalus percae and Bunodera luciopercae. The prevalences of A. lucii and C. lacustris were significantly reduced in fish infected by T. nodulosus, although the mean intensity of infections remained unaffected for any helminth species, while the mean abundance of C. lacustris was significantly reduced in plerocercoid-affected perch. Differences in site selection and individual interactions between the four helminth species in the intestine of T. nodulosus-infected and non-infected perch were rarely observed.

Larval trypanorhynch cestodes in teleost fish from Moreton Bay, Queensland

During a helminthological examination of teleost fish of Moreton Bay (Qld, Australia), 976 fish from 13 orders, 57 families and 133 species were examined and nine species of trypanorhynch metacestodes were identified. Callitetrarhynchus gracilis (Rudolphi, 1819) was the most frequently encountered species, found in 16 species of fish, with Callitetrarhynchus speciosus (Linton, 1897), Pterobothrium pearsoni (Southwell, 1929), Otobothrium alexanderi Palm, 2004, Otobothrium mugilis Hiscock, 1954, Otobothrium parvum Beveridge & Justine, 2007, Proemotobothrium southwelli Beveridge & Campbell, 2001, Pseudotobothrium dipsacum (Linton, 1897) and Heteronybelinia cf. heteromorphi Palm, 1999 occurring in fewer host species and at lower prevalences. Comparisons are made with studies elsewhere in the world and specifically within the South-west Pacific. Of the best studied regions in the South-west Pacific (Heron Island, Lizard Island, New Caledonia and now Moreton Bay), the fauna from Moreton Bay was found to be the most distinctive, with fauna from the three reef locations sharing 35–48% of species between sites and just 12–24% with Moreton Bay. The fauna of trypanorhynch cestodes from Lizard Island and New Caledonia was found to be the most similar.

Histopathological changes of rodent liver infected with a larval cestodes recorded at Sohag, Egypt

Histopathological changes of rodent liver infected with a larval cestodes recorded at Sohag, Egypt

Hematological and Serological Investigation of Dogs during Experimental Echinococcosis.

To study the hematological findings of dogs infected with echinococcosis and the possibility of using in vitro reared Echinococcus granulosus excretory-secretory antigen (ES-Ag) as a reagent for serological diagnosis of canine echinococcosis. Eight dogs were infected orally with protoscoleces, extracted from ovine fertile hydatid cysts. Two additional dogs were infected with Cysticercus tenuicollis, obtained from infested sheep. The hematological parameters of dogs were determined with the ADVIA 2120i automatic hematology analyzer with a blood smear staining module. Adult E. granulosus and/or Taenia hydatigena that were collected from small pieces of the open gut and the larval cestodes that were extracted from infested sheep during slaughter were cultured in an incomplete RPMI-1640 medium. The parasite-ES-Ag-containing supernatant was used as an antigen in enzyme linked immunosorbent assay (ELISA) to detect antibodies in the sera of infected dogs. A significant increase in hemoglobin concentration and erythrocyte count was found during the infection, as well as an increasing proportion of lymphocytes and segmented neutrophils, accompanied by a significant reduction of the leukocyte count and a growth of both the absolute and the relative eosinophil count. ELISA found a strengthening antigenicity of echinococcus preparations during infection. This property was more pronounced in the protoscoleces ES-Ag, compared to the eponymous antigen of an adult parasite. The latter gave specificity to ELISA, which allowed differentiating it from the similar antigen of the closely related tapeworm T. hydatigena. In vitro reared adult E. granulosus ES-Ag can be used as an antigen in the serological diagnosis of canine echinococcosis. Hematological parameters and serological results have predictive value in the screening of dogs for echinococcosis; however, in some individuals, they may reflect the state of resistance to invasion.

Mass Death of Predatory Carp, Chanodichthys erythropterus, Induced by Plerocercoid Larvae of Ligula intestinalis (Cestoda: Diphyllobothriidae).

We describe here the mass death of predatory carp, Chanodichthys erythropterus, in Korea induced by plerocercoid larvae of Ligula intestinalis as a result of host manipulation. The carcasses of fish with ligulid larvae were first found in the river-edge areas of Chilgok-bo in Nakdong-gang (River), Korea at early February 2016. This ecological phenomena also occurred in the adjacent areas of 3 dams of Nakdong-gang, i.e., Gangjeong-bo, Dalseong-bo, and Hapcheon-Changnyeong-bo. Total 1,173 fish carcasses were collected from the 4 regions. To examine the cause of death, we captured 10 wondering carp in the river-edge areas of Hapcheon-Changnyeong-bo with a landing net. They were 24.0-28.5 cm in length and 147-257 g in weight, and had 2-11 plerocercoid larvae in the abdominal cavity. Their digestive organs were slender and empty, and reproductive organs were not observed at all. The plerocercoid larvae occupied almost all spaces of the abdominal cavity under the air bladders. The proportion of larvae per fish was 14.6-32.1% of body weight. The larvae were ivory-white, 21.5-63.0 cm long, and 6.0-13.8 g in weight. We suggest that the preference for the river-edge in infected fish during winter is a modified behavioral response by host manipulation of the tapeworm larvae. The life cycle of this tapeworm seems to be successfully continued as the infected fish can be easily eaten by avian definitive hosts.

Heavy metal accumulation in Lacistorhynchus dollfusi (Trypanorhyncha: Lacistorhynchidae) infecting Citharichthys sordidus (Pleuronectiformes: Bothidae) from Santa Monica Bay, Southern California.

The accumulation of heavy metals in macroparasites of fish has been widely studied in freshwater environments. Less is known about metal uptake in cestodes parasitizing marine fish. Lacistorhynchus dollfusi is a common larval cestode parasite of Pacific sanddab (Citharichthys sordidus), a flatfish species inhabiting Santa Monica Bay. The ability of this cestode to concentrate metals in its tissues was compared with metal levels in its sanddab host. Fish and cestode tissue were analysed for 14 elements using Inductively Coupled Plasma Mass Spectrometry. The elements analysed were silver (Ag), arsenic (As), cadmium (Cd), chromium (Cr), copper (Cu), iron (Fe), mercury (Hg), potassium (K), lead (Pb), rubidium (Rb), selenium (Se), strontium (Sr), titanium (Ti) and zinc (Zn). Three of the 14 metals (Cu, Hg and Zn) were significantly greater in concentration in L. dollfusi compared with their levels in the liver, intestine and muscle of their fish host. They ranked in concentration from highest to lowest as follows: Zn > Cu > Hg. The ability of the cestode L. dollfusi to uptake metals at higher concentrations than its host warrants its consideration as a candidate for a heavy metal accumulation indicator of pollution exposure in Pacific sanddab.

Metazoan parasites of Brama australis from southern Chile: a tool for stock discrimination?

The metazoan parasites of 403 specimens of the southern ray's bream Brama australis from three localities in southern Chile (Lebu 36° 70' S; 73° 40' W, Calbuco 41° 50' S; 73° 08' W and Punta Arenas 53° 10' S; 70° 50' W) were recorded. More than 23 400 parasite specimens belonging to 12 taxa were registered. Metazoan parasites were dominated by the copepod Hatschekia conifera, constituting 97% of the total number of parasites; the larval cestode Hepatoxylon trichiuri was the second most important parasite (2·1% of the total number of parasites). The remaining 10 species constituted <1% of the metazoan parasites. Parasitological evidence, based on univariate and multivariate analysis, does not support the existence of discrete stocks in the studied zone.

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

BackgroundMultiple 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.MethodsWe 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.ResultsWe 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.ConclusionsWe 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.

Environmental and anthropogenic factors affecting the probability of occurrence of Oncomegas wageneri (Cestoda: Trypanorhyncha) in the southern Gulf of Mexico.

BackgroundUnderstanding the environmental and anthropogenic factors influencing the probability of occurrence of the marine parasitic species is fundamental for determining the circumstances under which they can act as bioindicators of environmental impact. The aim of this study was to determine whether physicochemical variables, polyaromatic hydrocarbons or sewage discharge affect the probability of occurrence of the larval cestode Oncomegas wageneri, which infects the shoal flounder, Syacium gunteri, in the southern Gulf of Mexico.MethodsThe study area included 162 sampling sites in the southern Gulf of Mexico and covered 288,205 km2, where the benthic sediments, water and the shoal flounder individuals were collected. We used the boosted generalised additive models (boosted GAM) and the MaxEnt to examine the potential statistical relationships between the environmental variables (nutrients, contaminants and physicochemical variables from the water and sediments) and the probability of the occurrence of this parasite. The models were calibrated using all of the sampling sites (full area) with and without parasite occurrences (n = 162) and a polygon area that included sampling sites with a depth of 1500 m or less (n = 134).ResultsOncomegas wageneri occurred at 29/162 sampling sites. The boosted GAM for the full area and the polygon area accurately predicted the probability of the occurrence of O. wageneri in the study area. By contrast, poor probabilities of occurrence were obtained with the MaxEnt models for the same areas. The variables with the highest frequencies of appearance in the models (proxies for the explained variability) were the polyaromatic hydrocarbons of high molecular weight (PAHH, 95 %), followed by a combination of nutrients, spatial variables and polyaromatic hydrocarbons of low molecular weight (PAHL, 5 %).ConclusionsThe contribution of the PAHH to the variability was explained by the fact that these compounds, together with N and P, are carried by rivers that discharge into the ocean, which enhances the growth of hydrocarbonoclastic bacteria and the productivity and number of the intermediate hosts. Our results suggest that sites with PAHL/PAHH ratio values up to 1.89 promote transmission based on the high values of the prevalence of O. wageneri in the study area. In contrast, PAHL/PAHH ratio values ≥ 1.90 can be considered harmful for the transmission stages of O. wageneri and its hosts (copepods, shrimps and shoal flounders). Overall, the results indicate that the PAHHs affect the probability of occurrence of this helminth parasite in the southern Gulf of Mexico.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-015-1222-6) contains supplementary material, which is available to authorized users.

Molecular Identification of Zoonotic Tissue-Invasive Tapeworm Larvae Other than Taenia solium in Suspected Human Cysticercosis Cases.

Rarely, zoonotic Taenia species other than Taenia solium cause human cysticercosis. The larval stages are morphologically often indistinguishable. We therefore investigated 12 samples of suspected human cysticercosis cases at the molecular level and surprisingly identified one Taenia crassiceps and one Taenia serialis (coenurosis) infection, which were caused by tapeworm larvae normally infecting rodents and sheep via eggs released from foxes and dogs.

Immunity and immune modulation elicited by the larval cestode Mesocestoides vogae and its products.

Larval cestodes (metacestodes) induce long-lasting infections leading to considerable pathology in humans and livestock. Their survival is typically associated with Th2-biased immune responses and immunosuppressive effects and depends on the parasite's ability to excrete/secrete antigens with immunoregulatory properties. Here, Mesocestoides vogae, a natural parasite of mice, is proposed as a new model species for the identification and characterization of cestode-derived immunomodulatory factors. We followed the kinetics of immune parameters after infection with M.vogae or exposure to their excretory/secretory (ES) products in a permissive strain of mice. Besides, a dominant IL-10 production and accumulation of macrophages and eosinophils expressing mRNA for Fizz-1, YM1 and Arg-1, mice showed minimal IFN-γ and transient IL-4 production at early time points with a complete loss at later stages of infection. We found that serum-free ES products without host contamination directly induced M2 macrophages and suppressed IFN-γ production invivo and invitro. This study highlights the use of the M.vogae as a cestode infection model and its ES products as a valuable tool for the identification of new therapeutic targets for the control of larval cestodiasis.

Seasonal occurrence of some larval stages of endoparasites in three cyprinids from the Nwanedi-Luphephe dams, the Limpopo River System, South Africa

Abstract This study provides information on seasonal occurrence of developmental stages of endoparasites infecting three cyprinids in the Nwanedi-Luphephe dams, Limpopo River System. Labeobarbus marequensis (Smith, 1841), Barbus trimaculatus Peters, 1852 and Barbus radiatus Peters, 1853 were investigated seasonally from January 2008 to October 2008. The following larvae of metazoan parasites were collected: Diplostomum sp. from the eyes of L. marequensis and B. trimaculatus; Ornithodiplostomum sp. from the gills of B. trimaculatus; Posthodiplostomum sp. from muscle, skin and fins of B. trimaculatus and B. radiatus; third-stage Contracaecum larvae (L3) from the mesentery fats and on the liver lobes of L. marequensis and B. trimaculatus and gryporynchid cestode larvae from the outer intestinal wall of B. radiatus. All the flukes encountered were metacercariae. Diplostomum sp. and Contracaecum sp. dominated the parasite communities. Their prevalence exhibited seasonal fluctuations with maxima in summer. Factors likely to influence fish infection such as the body size of fish and their condition factors were also briefly considered in this study.

Spatial variability of helminth parasites and evidence for stock discrimination in the round sardinella, Sardinella aurita (Valenciennes, 1847), off the coast of Tunisia.

Three digeneans - Parahemiurus merus (Linton, 1910), Aphanurus stossichii (Monticelli, 1891) and Lecithochirium sp. - and one tetraphyllidean cestode larva were used as biological tags to discriminate the stock of Sardinella aurita (Valenciennes, 1847). In total, 579 fish were examined in five zones off the Tunisian coast, including Bizerte and Kelibia in the north, Mahdia in the east, Gabes and Zarzis in the south. Discriminant analyses used for the separation of S. aurita allowed for the identification of two discrete stocks. Sardinella aurita from Bizerte, Kelibia and Zarzis clumped together as a single stock. Parahemiurus merus and A. stossichii were the most important species in determining the location of sampled fish from these regions. Specimens from Mahdia and Gabes were grouped as one stock characterized by the presence of Lecithochirium sp. and larvae of the Tetraphyllidea. These results were corroborated by comparing the parameters of prevalence and mean abundance of parasites among zones. The separation of S. aurita between localities after pooling specimens from Bizerte, Kelibia and Zarzis and separately pooling those from Mahdia and Gabes also allowed the identification of two discrete stocks, one in offshore waters from Bizerte, Kelibia and Zarzis characterized by the digeneans P. merus and A. stossichii and one in inshore waters from Mahdia and Gabes characterized by Lechithochirium sp. and tetraphyllidean larvae.

Thirty-Seven Human Cases of Sparganosis from Ethiopia and South Sudan Caused by Spirometra Spp.

Thirty-seven unusual specimens, three from Ethiopia and 34 from South Sudan, were submitted since 2012 for further identification by the Ethiopian Dracunculiasis Eradication Program (EDEP) and the South Sudan Guinea Worm Eradication Program (SSGWEP), respectively. Although the majority of specimens emerged from sores or breaks in the skin, there was concern that they did not represent bona fide cases of Dracunculus medinensis and that they needed detailed examination and identification as provided by the World Health Organization Collaborating Center (WHO CC) at Centers for Disease Control and Prevention (CDC). All 37 specimens were identified on microscopic study as larval tapeworms of the spargana type, and DNA sequence analysis of seven confirmed the identification of Spirometra sp. Age of cases ranged between 7 and 70 years (mean 25 years); 21 (57%) patients were male and 16 were female. The presence of spargana in open skin lesions is somewhat atypical, but does confirm the fact that populations living in these remote areas are either ingesting infected copepods in unsafe drinking water or, more likely, eating poorly cooked paratenic hosts harboring the parasite.

Does cestode infection affect reproduction of the endangered golden venus chub, Hemigrammocypris neglectus?

The effects of larval cestode (Neogryporhynchus cheilancristrotus) infection on the reproduction of golden venus chub Hemigrammocypris neglectus and their population growth were estimated by analysis of the relationships between the abundance of cestodes and the breeding behavior of male chubs, as well as the fecundity of female chubs. N. cheilancristrotus causes a prominent abdominal distention in H. neglectus because of a hypertrophied hepatopancreas. Cestode infection displayed no negative relationship to chasing behavior by males of females or to the number of prenatal eggs in females. Thus, we conclude that cestode infection has little effect on the population growth of the host fish through reproductive behavior/fecundity, despite the prominent pathological change in the hepatopancreas.

Sparganosis –a rare case report

Sparganosis is a parasitic infection caused by the plercercoid larvae of diphyllobothroid tapeworms belonging to the genus Spirometra. It is a rare disease of human as man is not a natural host of spirometra species. Diagnosis of latter is difficult as it mimics other conditions that commonly cause subcutaneous or visceral fluid collection. Here we report a case of Sparganosis in a man who presented with a swelling over left cheek. It was confirmed by pathological and microbiological examination. To the best of our knowledge, this is the first case from Central India where sparganum was isolated from a swelling.