Anoplocephala perfoliata in Horses in Sweden: Prevalence,Infection Levels and Intestinal Lesions

Distal ileum, caecum and proximal colon of 470 horses were examined for helminths during 1 year at an abattoir in central Sweden. The infection levels of the horse tapeworm Anoplocephala perfoliata, their stage of development, site of attachment and gross pathological lesions caused by the worm were recorded. Faecal samples from 395 of the horses were examined specifically for tapeworm segments and eggs in order to correlate these findings with the numbers in the alimentary canal. In total 65% of the horses were infected with A. perfoliata and the mean intensity of infection was 79 worms per infected horse with a maximum of 912. The level of infection was significantly higher in (1) 3rd and 4th than in 1st and 2nd quarter of the year; (2) older horses than in yearlings; (3) females than in males and geldings; (4) thoroughbreed and cold-blooded horses than in Swedish standardbreeds and ponies. The level of infection was unaffected by the usage of anthelminthics against nematodes. Of the horses examined 51% had 1-100 worms whereas 14% were infected with more than 100 worms. Of the tapeworm positive horses 72% had mixed infections with both adult and juvenile worms, 20% solely juveniles, and 8% solely adults. The severity of intestinal lesions exacerbated by increasing numbers of A. perfoliata. About 11% of the intestines examined had severe lesions, but there was no history of acute abdominal distress in any of the horses included in this study. Although the number of detectable eggs was significantly higher for horses heavily infected with A. perfoliata, the egg recovery among infected horses was only 35%. An additional field survey comprising 218 horses on 88 premises in central and southern parts of Sweden showed that the prevalence of A. perfoliata egg positive horses was the same as found on faecal examination during the abattoir survey.     

Eradication of Taenia solium cysticercosis: a role for vaccination of pigs.

Neurocysticercosis due to Taenia solium is an important cause of human morbidity and mortality, particularly in Latin America and parts of Africa and Asia. The disease has been recognised as potentially eradicable. Emphasis has been placed on control of the parasite through mass chemotherapy of human populations to remove tapeworm carriers. This strategy does not control the source of tapeworm infections, cysticercosis in pigs, and parasite transmission may continue due to incomplete chemotherapy coverage of human tapeworm carriers or because of immigration of tapeworm carriers into control areas. Exceptionally effective, practical vaccines have been developed against cysticercosis in sheep and cattle and a recent trial has proved recombinant antigens to be effective against Taenia solium cysticercosis in pigs. A new strategy for eradication of Taenia solium is proposed, based principally on a combined approach of chemotherapy of human tapeworm carriers and vaccination of all pigs at risk of infection.     

Resistance against heterogeneous sequential infections: experimental studies with a tapeworm and its copepod host

Parasite heterogeneity is thought to be an important factor influencing the likelihood and the dynamics of infection. Previous studies have demonstrated that simultaneous exposure of hosts to a heterogeneous mixture of parasites might increase infection success. Here this view is extended towards the effect of parasite heterogeneity on subsequent infections. Using a system of the tapeworm Schistocephalus solidus and its copepod intermediate host, heterogeneity of the tapeworm surface carbohydrates is investigated, i.e. structures that are potentially recognized by the invertebrate host's immune system. With lectin labelling, a significant proportion of variation in surface carbohydrates is related to differences in worm sibships (i.e. families). Tapeworm sibships were used for experimental exposure of copepods to either homogeneous combinations of tapeworm larvae, i.e. worms derived from the same sibship or heterogeneous mixtures of larvae, and copepods were subsequently challenged with an unrelated larva to study re-infection. Contrary to expectation, neither an effect of parasite heterogeneity on the current infection, nor on re-infection were found. The effect of parasitic heterogeneity on host immunity is therefore complex, potentially involving increased cross-protection on the one hand, with higher costs of raising a more heterogeneous immune response on the other.     

Fish tapeworm infections (diphyllobothriasis) in Canada,particularly British Columbia.

Although the risk of diphyllobothriasis is generally low in Canada, fish tapeworm infections seem to have become more frequent in recent years. This increase is probably a consequence of the growing popularity of raw or inadequately cooked ethnic fish dishes or of a preference for lightly cooked fish, especially salmon. Only freshwater fish become infected with the larvae, but not everyone may realize that salmon can acquire the parasites before they leave their native lakes and rivers for the sea. If fish known to be sources of the tapeworms are to be eaten raw they should first be well frozen or salted to kill the larvae. Physicians should regard fish tapeworm infection as a notifiable disease. In Canada niclosamide, the drug of choice, is available from the manufacturer on a patient-by-patient basis.     

Acetic acid induced ulceration in rats is not affected by infection with Hymenolepis diminuta

Analysis of rodent models of inflammatory bowel disease, airways hyper-reactivity, diabetes, and multiple sclerosis has shown that infection with helminth parasites can significantly reduce the severity of the disease. Here, we assessed whether rats infected with the tapeworm Hymenolepis diminuta were protected from gastric ulceration induced by the serosal application of acetic acid. All rats gavaged with infective cysticercoids harbored adult worms when assessed 6 wk later, and acetic acid evoked the expected gastric ulceration. However, infection with H. diminuta did not affect the degree of gastric ulceration at either 3 or 7 days post-acetic acid application, as gauged by ulcer area or histopathology. While the data do not dismiss the possibility that infection with other helminths could be anti-ulcerogenic, they illustrate that 'helminth therapy' for inflammatory disease is likely to be both disease- and helminth-specific.     

Effective protection against experimental Taenia solium tapeworm infection in hamsters by primo-infection and by vaccination with recombinant or synthetic heterologous antigens

The disease caused by Taenia solium is progressively being recognized as a growing global threat for public human health and pig husbandry that requires the development of effective control measures. A central participant in the taeniasis/cysticercosis transmission network is the human carrier of the adult tapeworm because of its great potential in spreading the infection. Herein, evidence is presented that a primary infection of golden hamsters with orally administered T. solium cysticerci improved the host's resistance against a secondary infection. Likewise, previous vaccination increased the hamster's resistance. Similar high levels of protection (> 78%) were induced by systemic or oral vaccination with the S3Pvac anticysticercosis synthetic peptide vaccine or the highly immunogenic recombinant chimera based on the protective peptide KETc1 bound to Brucella spp. lumazine synthase (BLS-KETc1). Increased resistance after primo-infection and vaccination possibly results from changes in the immune conditions prevailing in the host's intestine. The contribution to protection from the KETc1 and BLS epitopes in a chimeric vaccine is under study. Preventive vaccination of definitive hosts of T. solium against the tapeworm, the most relevant step in the taeniasis/cysticercosis transmission, may greatly impact the dynamics of endemic disease and has not been studied or tried previously.     

The pig as an intermediate host for Taiwan Taenia infection

Eggs (1000-100,000/animal) of Taiwan Taenia were inoculated per os into 14 Small-Ear-Miniature (SEM), 19 Landrace-Small-Ear-Miniature (L-SEM), and 5 Duroc-Yorkshire-Landrace (DYL) pigs. These animals were sacrificed 7-107 days after infection. Thirty-four pigs were found to be infected with Taiwan Taenia cysticerci and the infection rates of SEM, L-SEM, and DYL were 86%, 89% and 100% respectively. The cysticerci recovery rates of SEM, L-SEM and DYL pigs were 27.2%, 1.7% and 0.27% respectively. Cysticerci were recovered only from the livers and none were found in muscles, viscera or other parts of the carcasses. More cysticerci were located in the liver parenchyma (71%) than on the liver surface (29%). Taiwan Taenia cysticerci were smaller than those of classical T. saginata or T. solium. Moreover, Taiwan Taenia cysticerci had 2 rows of rudimentary hooklets on the scolex. The results of this study indicate that young pigs are good intermediate hosts for Taiwan Taenia and that the SEM pig is a satisfactory host for experimental studies with this tapeworm. These results were similar to other studies with different geographic strains of the T. saginata-like tapeworm in the Far East. These strains appear to be the same and possibly a new species.     

Effects of tapeworm infection on male reproductive success and mating vigor in the red flour beetle,Tribolium castaneum

Parasites may exert negative effects on host survivorship and reproductive success. The effects of parasites on female host fitness have been well documented; however, the effects of parasites on the reproductive success of male hosts and particularly the underlying mechanisms that alter male fitness are not well understood. Previous studies demonstrated that infection by rat tapeworm (Hymenolepis diminuta) reduced the fitness of male red flour beetles (Tribolium castaneum) in an environment of female mate choice and strong male-male competition. The present study determined the role of female mate choice and male insemination capacity on observed fitness reduction of male beetles by the tapeworm parasites. We found that infected males showed reduced mating vigor and consequently inseminated fewer females than did uninfected males. Specifically, tapeworm infection reduced the number of offspring sired by a male by 14-22% even when male-male competition and female mate choice were absent. Further, the insemination capacity of males diminished by 30% because of infection. Female beetles did not discriminate against infected males in precopulatory mate choice experiments. Copulatory courtship, a determinant of postcopulatory female choice, was not significantly different between infected and uninfected males. Hence, we concluded that female beetles did not show either pre- or postcopulatory choice against tapeworm-infected males. Therefore, tapeworm-induced reduction in the reproductive success of male beetles possibly results from altered reproductive biology, such as lower mating vigor and decreased sperm quantity or quality.     

Diphyllobothrium latum infection after eating domestic salmon flesh.

Diphyllobothrium latum infection in human is not common in Korea and only thirty seven cases have been reported since 1921. We report two cases of fish tapeworm infection after ingestion of raw cherry salmon (Oncorhynchus masou) caught in the domestic river. Among four family members who ate together raw salmon flesh six months ago, just two, mother and daughter, were infected. It is our expectation that the salmon associated tapeworm infections would be enlisted as one of the major parasitic problems with the growing consumption of salmon in Korea.     

New Insights in Cysticercosis Transmission

Taenia solium infection causes severe neurological disease in humans. Even though infection and exposure to swine cysticercosis is scattered throughout endemic villages, location of the tapeworm only explains some of the nearby infections and is not related to location of seropositive pigs. Other players might be involved in cysticercosis transmission. In this study we hypothesize that pigs that carry nematodes specific to dung beetles are associated with cysticercosis infection and/or exposure. We carried out a cross-sectional study of six villages in an endemic region in northern Peru. We euthanized all pigs (326) in the villages and performed necropsies to diagnose cysticercosis. For each pig, we counted cysticerci; measured anti-cysticercus antibodies; identified intestinal nematodes; tabulated distance to nearest human tapeworm infection; and recorded age, sex, productive stage, and geographic reference. For the purpose of this paper, we defined cysticercosis infection as the presence of at least one cysticercus in pig muscles, and cysticercosis exposure as seropositivity to anti-cysticercus antibodies with the presence of 0–5 cysticerci. Compared to pigs without nematode infections, those pigs infected with the nematode Ascarops strongylina were significantly associated with the presence of cysticerci (OR: 4.30, 95%CI: 1.83–10.09). Similarly, pigs infected with the nematode Physocephalus sexalatus were more likely to have cysticercosis exposure (OR: 2.21, 95%CI: 1.50–3.28). In conclusion, our results suggest that there appears to be a strong positive association between the presence of nematodes and both cysticercosis infection and exposure in pigs. The role of dung beetles in cysticercosis dynamics should be further investigated.     

Sex, parasites and resistance--an evolutionary approach

Immune systems are among the most diverse biological systems. An evolutionary arms race between hosts and rapidly evolving pathogens is supposed to be a reason for this diversity, and might explain why most eukaryotic hosts and parasites reproduce sexually. In this review, I will focus on possible benefits of sexual reproduction in hosts and parasites, using a model system consisting of a tapeworm and its two intermediate hosts, copepods and sticklebacks. We found that the hermaphroditic tapeworms can increase their infection success by reproducing sexually with a partner (outcrossing), instead of reproducing alone. The defence system of the copepods provides highly specific discrimination of antigenic characteristics of the tapeworms. This supports the finding that tapeworms benefit from outcrossing, but contradicts the conventional notion that the immune system of invertebrates, in contrast to vertebrates, is not able to react with specificity. Finally, sticklebacks seem to benefit from optimal diversity in their specific immune system. Previous studies showed that female sticklebacks prefer mates, which sire offspring with an optimal diversity in the MHC (genes involved in antigen presentation). We now found that these individuals suffer less from tapeworm infection. Furthermore, they are able to reduce the expression of an unspecific immune trait, thereby possibly avoiding harmful side effects of a highly activated, unspecific immune system.     

Identification of the copepod intermediate host of the introduced broad fish tapeworm, Diphyllobothrium latum, in Southern Chile

The broad fish tapeworm, Diphyllobothrium latum, is an exotic species in both Chile and Argentina, and until now, its copepod host has remained unknown in South American waters. The objective of this study was to identify calanoid copepod species that may be intermediate hosts for D. latum in Lake Panguipulli, Chile. In this lake, the highest levels of infection by this tapeworm occur in the introduced rainbow trout, Oncorhynchus mykiss. Of the 2 calanoid copepods found in Lake Panguipulli, Diaptomus diabolicus and Boeckella gracilipes, only D. diabolicus became infected on experimental exposure to coracidia. Prevalence (mean intensity) of experimental infection in adult copepods was 73.2% (2.8 procercoids per host). Diaptomus diabolicus has been demonstrated to be a new intermediate host; this is the first record of a copepod host for D. latum in South America.     

Modulation of caudal intestinal permeability in the rat during infection by the tapeworm Hymenolepis diminuta.

Bidirectional movement of solutes between the intestinal lumen and systemic circulation is restricted by tissue barriers that may be altered under conditions such as intestinal infection. In a study using an in vitro everted sac preparation to assess small intestinal permeability in a lumen-to-serosa direction, 51Cr-EDTA movement was compared regionally in the jejunum and ileum of rats infected and uninfected by tapeworms. Whereas jejunal segments showed no significant differences in permeability to 51Cr-EDTA at 6, 15, or 32 days postinfection (dpi), ileal segments displayed an increased permeability on 15 and 32 dpi, but not 6 dpi. The alterations in permeability were not reversed 1 wk after removal of the tapeworm from the intestine. In conclusion, the strictly lumen-dwelling tapeworm infection allows increased movement of molecules from the lumen into ileal, but not jejunal, tissues by 15 dpi.     

Guanosine 3',5'-cyclic monophosphate: a tapeworm-secreted signal molecule communicating with the rat host's small intestine

Tapeworms alter the physiological environment of the host's small intestinal lumen by contracting the intestinal smooth muscle, thereby slowing the transit of intestinal contents. We hypothesize that parasite-to-host molecular signaling is responsible for the specific patterns of small intestinal smooth muscle contraction observed both during tapeworm infection and after the infusion of tapeworm-secreted molecules into the intestinal lumen of unanesthetized rats. Of the tapeworm-secreted compounds tested, only lumenal infusion of guanosine 3',5'-cyclic monophosphate (cGMP) induced contractile patterns that mimic those observed during tapeworm infection. The response to cGMP occurred in a concentration-dependent fashion. Our study clearly demonstrates that cGMP can serve as an extracellular signal molecule regulating small intestinal motility mechanisms in vivo.     

Protecting Free-Living Dormice: Molecular Identification of Cestode Parasites in Captive Dormice (Muscardinus avellanarius) Destined for Reintroduction

The success of any population translocation programme relies heavily on the measures implemented to control and monitor the spread of disease. Without these measures, programmes run the risk of releasing immunologically naïve species or, more dangerously, introducing novel infectious agents to native populations. As a precaution, a reintroduction programme for the common or hazel dormouse, Muscardinus avellanarius, in England screens dormice before release following captive breeding. Using PCR sequencing of a range of genes, we tested whether the same species of tapeworm(s) were present in captive and free-living dormice. Whilst only Rodentolepis straminea were identified in free-living dormice, cestode ova found in a captive individual produced a molecular match closely related to Hymenolepis microstoma and a previously unrecorded Rodentolepis species. To prevent putting at risk the free-living population, we recommended the continued treatment of dormice showing tapeworm infection before release. Our work demonstrates how molecular techniques can be used to inform reintroduction programmes, reduce risk from disease and increase chances of reintroduction success.

     

Lack of preference for infective faeces in Hymenolepis diminuta-infected beetles (Tenebrio molitor)

The beetle-tapeworm life cycle provides a convenient system to study how host behaviour influences the probability of re-infection because initial and secondary infections can be tracked. The beetle, Tenebrio molitor, is infected with the tapeworm Hymenolepis diminuta when it ingests rat faeces containing tapeworm eggs, which upon hatching undergo five morphologically distinct stages while developing inside the beetle. In a series of preference trials, both individual and groups of previously infected beetles were exposed to baits of infective (faeces with eggs) and uninfective faeces. Beetles did not differ in the amount of time spent or in the number of occurrences at each bait type, suggesting that infected beetles show no preference for infective faeces. This may be a host adaptation to avoid further infection, parasite manipulation to avoid competition for host resources, or both. Further, once infected, beetles are no more or no less likely to become re-infected than uninfected beetles. An analysis of the mean and variance of infection suggests that some individuals are highly susceptible to and some are highly resistant to infection, with males being more variable than females. This could explain the higher load of cysticercoids observed in males.     

A review of taeniasis and cysticercosis in the Lao People's Democratic Republic

Taeniasis and cysticercosis are important but underreported parasitic zoonoses in the Lao People's Democratic Republic (Lao PDR). Reports of human and pig cysticercosis are rather limited and based largely on anecdotal evidence. To date, no structured surveys of disease prevalence or incidence have been reported. However, one unpublished pilot survey of pig cysticercosis in a slaughterhouse in northern Laos estimated prevalence to be 1.7%, without speciation of parasite cysts. Over the past 20 years, nine surveys of intestinal helminthic infection have been conducted; the prevalence of human taeniasis ranged from 0 to 14.0%. The study designs and sample sizes varied greatly, however a high degree of spatial and age variation in taeniasis prevalence was evident. These results are however inconclusive as the species of tapeworm infecting the people was not determined. To further our knowledge of taeniasis and cysticercosis in Lao PDR, structured community-based surveys in high-risk areas are required in combination with the use of sensitive and specific diagnostic tests capable of identifying the pork tapeworm, Taenia solium. This will enable the development and implementation of control measures that are both appropriate and sustainable if T. solium is shown to be a public health threat.     

A possible nuclear DNA marker to differentiate the two geographic genotypes of Taenia solium tapeworms

Cysticercosis caused by infection with embryonated eggs of the pork tapeworm Taenia solium is an important cause of neurological disease worldwide. Based on the phylogenetic analysis of mitochondrial DNA, the pathogen has been divided into two geographic clades, corresponding to Afro-American and Asian genotypes. In this study the genotyping of T. solium was carried out by using the nuclear DNA sequences of the immunodiagnostic antigen genes Ag1V1 and Ag2. The two geographic genotypes were supported by the Ag2 sequences, especially showing unique substitutions in each of the genotypes. It seems likely that the Ag2 may be a novel nuclear DNA marker to distinguish the two geographic genotypes of T. solium.     

Protecting Free-Living Dormice: Molecular Identification of Cestode Parasites in Captive Dormice (<Emphasis Type="Italic">Muscardinus avellanarius</Emphasis>) Destined for Reintroduction

The success of any population translocation programme relies heavily on the measures implemented to control and monitor the spread of disease. Without these measures, programmes run the risk of releasing immunologically naïve species or, more dangerously, introducing novel infectious agents to native populations. As a precaution, a reintroduction programme for the common or hazel dormouse, Muscardinus avellanarius, in England screens dormice before release following captive breeding. Using PCR sequencing of a range of genes, we tested whether the same species of tapeworm(s) were present in captive and free-living dormice. Whilst only Rodentolepis straminea were identified in free-living dormice, cestode ova found in a captive individual produced a molecular match closely related to Hymenolepis microstoma and a previously unrecorded Rodentolepis species. To prevent putting at risk the free-living population, we recommended the continued treatment of dormice showing tapeworm infection before release. Our work demonstrates how molecular techniques can be used to inform reintroduction programmes, reduce risk from disease and increase chances of reintroduction success.     

Inflammatory responses in the intestine during tapeworm infections. Mucosal mast cells and mucosal mast cell proteases in Sprague-Dawley rats infected with Hymenolepis diminuta.

Comparative studies were made of two populations of Sprague-Dawley rats infected with Hymenolepis diminuta. The time course of infection, the development of mucosal mastocytosis and the levels of rat mucosal mast cell (MMC) protease (RMCP II) in serum and in jejunal mucosal tissues were monitored at intervals after infection with 40 cysticercoids of the tapeworm. Worm expulsion patterns differed markedly between the two populations, rats of New Zealand origin showing an abrupt and clear-cut loss of worms, rats of English origin showing a more gradual decline over a longer time period. In both populations, however, numbers of MMC and levels of tissue RMCP II were positively correlated with time after infection and negatively correlated with worm numbers. In only one of the three experiments (using English strain rats over a short time period) did levels of serum RMCP II change with time. In the other two experiments, in which English-strain and New Zealand-strain rats were used, there were no correlations between serum RMCP II and time, numbers of MMC, numbers of worms or levels of tissue RMCP II. The absence of correlation between serum RMCP II and worm loss in these experiments implies that MMC have no direct role in expulsion of H. diminuta. The data do show, nevertheless, that this purely luminal tapeworm is fully capable of activating the mucosal T lymphocyte-MMC precursor axis to elicit a mucosal mastocytosis.