Pseudophyllidean Cestode Research Articles

The Global Prevalence of Diphyllobothrium in Dogs, and Cats: A Systematic Review and Meta-analysis

Background: Fish tapeworms of the genus Diphyllobothrium are pseudophyllidean cestodes transmitted through the consumption of raw or inadequately cooked fish. Objective: The current systematic review and meta-analysis aim to estimate the global prevalence of Diphyllobothrium in dogs and cats based on published literature. Methods: Multiple English databases (PubMed, Scopus, ProQuest, Web of Science, and Google Scholar) were explored for relevant papers published until December 2021. Findings: Among the 37 studies that were included, 32 documented Diphyllobothrium infection in dogs and five in cats. The pooled prevalence (95% confidence interval) was 0.060% (0.030%-0.100%). The analysis based on country showed that the highest pooled prevalence in dogs and cats was observed in Bangladesh (0.250%, 0.149%-0.366%) and Indonesia (0.254%, 0.182%-0.333%), respectively. Based on the continent, Africa (0.109%, 0.017%-0.264%) and Asia (0.060%, 0%-0.345%) were the most common regions for infection in dogs and cats, respectively. Among different diagnostic methods, the highest pooled prevalence was related to molecular (0.661%, 0.573%-0.743%) and parasitological techniques (0.041%, 0%-0.217%) for dogs and cats’ studies, respectively. Conclusion: The findings show the importance of establishing a prevention and control measure focused on improving regular deworming and enhancing awareness of parasitic zoonotic diseases to minimize the transmission risk.

NEW RECORD OF LIGULA INTESTINALIS (LINNAEUS, 1758) (CESTODA: PSEUDOPHYLLIDEA) INFECTION IN HYPSELOBARBUS THOMASSI FROM THE WESTERN GHATS OF KERALA

The tapeworm Ligula intestinalis (L.) is the most common species of the genus Ligula and is widely distributed throughout the northern hemisphere (Dubinina, 1980). It has recently been also reported from southwestern Australia (Morgan, 2003; Chapman et al., 2006). This pseudophyllidean cestode presents a complex life cycle with a cyclopoid or diaptomid copepod as first intermediate host and planktivorous fish as second intermediate host. Fish-eating birds serve as the final host in which L. intestinalis quickly reaches sexual maturity and releases eggs. The worms acquire maturity in 3-5 days in the bird host and infected piscivorous birds are scarcely observed in natural conditions (Loot et al., 2001). The most conspicuous stage within the life cycle is the plerocercoid. Although it develops in the abdominal cavity of the second intermediate host and has a considerable effect on fish health, fecundity and behaviour. As a result it can cause heavy losses in freshwater pisciculture (Arme and Owen, 1968; Carter et al., 2005). Particularly reported from cyprinid fish, L. intestinalis has been shown to utilize a broad range of hosts, including other fish families such as Catostomidae, Salmonidae or Galaxiidae (Dubinina, 1980; Chapman et al., 2006).

Ligula intestinalis

Ligula intestinalis is a common pseudophyllidean cestode found in freshwater ecosystems worldwide. It has a complex life cycle involving a planktonic copepod as first intermediate host, a planktivorous fish as second intermediate host, and a fish-eating bird as the final host. The most conspicuous stage within the life cycle is the plerocercoid, which develops in the abdominal cavity of the fish host and has a substantial effect on its health, fecundity, and behaviour. It can cause epizootic cycles of mass mortality within fish populations.

Genome of the fatal tapeworm Sparganum proliferum uncovers mechanisms for cryptic life cycle and aberrant larval proliferation

The cryptic parasite Sparganum proliferum proliferates in humans and invades tissues and organs. Only scattered cases have been reported, but S. proliferum infection is always fatal. However, S. proliferum’s phylogeny and life cycle remain enigmatic. To investigate the phylogenetic relationships between S. proliferum and other cestode species, and to examine the mechanisms underlying pathogenicity, we sequenced the entire genomes of S. proliferum and a closely related non–life-threatening tapeworm Spirometra erinaceieuropaei. Additionally, we performed larvae transcriptome analyses of S. proliferum plerocercoid to identify genes involved in asexual reproduction in the host. The genome sequences confirmed that the S. proliferum has experienced a clearly distinct evolutionary history from S. erinaceieuropaei. Moreover, we found that nonordinal extracellular matrix coordination allows asexual reproduction in the host, and loss of sexual maturity in S. proliferum are responsible for its fatal pathogenicity to humans. Our high-quality reference genome sequences should be valuable for future studies of pseudophyllidean tapeworm biology and parasitism.

Schistocephalus solidus parasite prevalence and biomass intensity in threespine stickleback vary by habitat and diet in boreal lakes

Trophically-transmitted parasites can affect intermediate host behaviors, resulting in spatial differences in parasite prevalence and distribution that shape the dynamics of hosts and their ecosystems. This variability may arise through differences in physical habitats or biological interactions between parasites and their hosts, and may occur on very fine spatial scales. Using a pseudophyllidean cestode (Schistocephalus solidus) and the threespine stickleback (Gasterosteus aculeatus) as a model parasite–host complex, we investigated the association of infection with host diet composition and stomach fullness in different habitats of two large lakes in southwest Alaska. To become infected, the fish must consume pelagic copepods infected with the parasite’s procercoid stage, so we predicted higher infection rates of fish in offshore habitats (where zooplankton are the primary prey) compared to fish from the littoral zone. Sticklebacks collected from the littoral and limnetic zones were assayed for parasites and their stomach contents were classified, counted, and weighed. Contrary to our prediction, permutational multivariate analysis of variance and principal components analysis revealed that threespine sticklebacks in the littoral zone, which consumed a generalist diet (pelagic zooplankton and benthic invertebrates), had higher parasite prevalence and biomass intensity than conspecifics in the limnetic zone, which consumed zooplankton. These results, consistent in two different lakes, suggest that differences in parasite prevalence between habitats may have been determined by a shift in host habitat due to infection, differential host mortality across habitats, differential procercoid prevalence in copepods across habitats, or a combination of the three factors. This paradoxical result highlights the potential for fine spatial variability in parasite abundance in natural systems.

Lineage-specific expansion and loss of tyrosinase genes across platyhelminths and their induction profiles in the carcinogenic oriental liver fluke, Clonorchis sinensis.

Tyrosinase provides an essential activity during egg production in diverse platyhelminths by mediating sclerotization of eggshells. In this study, we investigated the genomic and evolutionary features of tyrosinases in parasitic platyhelminths whose genomic information is available. A pair of paralogous tyrosinases was detected in most trematodes, whereas they were lost in cyclophyllidean cestodes. A pseudophyllidean cestode displaying egg biology similar to that of trematodes possessed an orthologous gene. Interestingly, one of the paralogous tyrosinases appeared to have been multiplied into three copies in Clonorchis sinensis and Opisthorchis viverrini. In addition, a fifth tyrosinase gene that was minimally transcribed through all developmental stages was further detected in these opisthorchiid genomes. Phylogenetic analyses demonstrated that the tyrosinase gene has undergone duplication at least three times in platyhelminths. The additional opisthorchiid gene arose from the first duplication. A paralogous copy generated from these gene duplications, except for the last one, seemed to be lost in the major neodermatans lineages. In C. sinensis, tyrosinase gene expressions were initiated following sexual maturation and the levels were significantly enhanced by the presence of O2 and bile. Taken together, our data suggest that tyrosinase has evolved lineage-specifically across platyhelminths related to its copy number and induction mechanism.

THE OCCURRENCE OF Ligula intestinalis IN ITS FISH HOST Rutilus rutilus (L.) AND THE EFFECTS OF PARASITE ON THE FISH GROWTH (BÜYÜKÇEKMECE RESERVOIR, TURKEY)

Roach Rutilus rutilus (Linnaeus, 1758) is a very common fish species for Turkish inland waters, especially in Buyukcekmece Reservoir (Istanbul). The species is one of the most caught fish species and holds economic consumption value even though it is mostly infected by Ligula intestinalis (Linnaeus, 1758), a pseudophyllidean cestode causing severe pathological effects on fishes. The aim of the study was to determine the presence of L. intestinalis plerocercoids in its fish host R. rutilus and investigate the effects of the parasite on the condition of the fish. With this purpose, the fish specimens have captured from Buyukcekmece Reservoir with using gillnets having different mesh sizes (10×10 mm, 20×20 mm, 30×30 mm, 40×40 mm and 50×50 mm) from March 2009 to February 2010. The fork length and body weight of fish specimens (n=1857) were varied between 6.0–29.2 cm and 2.53 – 561.00 g, respectively. In total, 4.52% of specimens were infected by the plerocercoids. Infection by L. intestinalis was observed during summer, autumn and winter months but not spring. P arasite-host index (PSI %), prevalence (%) and mean intensity of plerocercoids for infected fishes were calculated, monthly. PSI (%) was estimated maximum in January as 18.49% while prevalence (%) was 32.31% in July and mean intensity of plerocercoids is 6.0 in October. Statistically s ignificant differences between K values of non-infected and infected specimens among length groups and months were recorded (Mann-Whitney U Test, p<0.05 ) . Results showed that, L. intestinalis plerocercoids seem to be affected significantly on the condition and body health of its host R. rutilus .

A waterborn zoonotic helminthiase in an Italian diver: a case report of a cutaneous Sparganum infection and a review of European cases

Many waterborne helminthes are opportunistic parasites that can travel directly from animals to man and may contain forms capable of penetrating the skin. Among these, Sparganum is the pseudophyllidean tapeworm that belongs to the genus Spirometra, which is responsible for parasitic zoonosis; it is rarely detected in Europe and is caused by the plerocercoid infective larva. Thus far, only six cases of cutaneous and ocular sparganosis have been reported in Europe; two and four cases have occurred in France and Italy, respectively. Herein, we describe a new case of sparganosis in Italy that affected a male diver who presented to the Bambino Gesù Children’s Hospital of Rome. The patient’s skin biopsy was submitted to the Parasitology department who, in consultation with Pathology, concluded that the morphologic and microscopic findings were those of Sparganum spp. larvae. The patient recovered following a single dose of 600 mg praziquantel.

Studies on pseudophyllidean cestode genus Ptychobothrium loennberg, 1889 (cestoda: ptychobothriidae, luhe, 1902) from freshwater fish Mastacembelus armatus (lacepede, 1800)

The present study deals with description of a new species of Pseudophyllidean Cestode genus Ptychobothrium, Loennberg,1889 collected from intestine of freshwater fish, Mastacembelus armatus (Lacepede, 1800) at Mahur, Dist. Nanded M.S. India during February, 2011 to January, 2013. Ptychobothrium vitellaris Sp.Nov. comes closer to all known species of genus Ptychobothrium, Loennberg, 1889 in general topography of organs but differs due to sessile Scolex, paired bothria, apical disk at anterior end of scolex, Neck absent, Mature Proglottids broader than long, Cirrus pouch pyriform, Testes 40-45 in numbers, Ovary bilobed and Vitellaria follicular.

Human Infections with Spirometra decipiens Plerocercoids Identified by Morphologic and Genetic Analyses in Korea.

Tapeworms of the genus Spirometra are pseudophyllidean cestodes endemic in Korea. At present, it is unclear which Spirometra species are responsible for causing human infections, and little information is available on the epidemiological profiles of Spirometra species infecting humans in Korea. Between 1979 and 2009, a total of 50 spargana from human patients and 2 adult specimens obtained from experimentally infected carnivorous animals were analyzed according to genetic and taxonomic criteria and classified as Spirometra erinaceieuropaei or Spirometra decipiens depending on the morphology. Morphologically, S. erinaceieuropaei and S. decipiens are different in that the spirally coiled uterus in S. erinaceieuropaei has 5-7 complete coils, while in S. decipiens it has only 4.5 coils. In addition, there is a 9.3% (146/1,566) sequence different between S. erinaceieuropaei and S. decipiens in the cox1 gene. Partial cox1 sequences (390 bp) from 35 Korean isolates showed 99.4% (388/390) similarity with the reference sequence of S. erinaceieuropaei from Korea (G1724; GenBank KJ599680) and an additional 15 Korean isolates revealed 99.2% (387/390) similarity with the reference sequences of S. decipiens from Korea (G1657; GenBank KJ599679). Based on morphologic and molecular databases, the estimated population ratio of S. erinaceieuropaei to S. decipiens was 35: 15. Our results indicate that both S. erinaceieuropaei and S. decipiens found in Korea infect humans, with S. erinaceieuropaei being 2 times more prevalent than S. decipiens. This study is the first to report human sparganosis caused by S. decipiens in humans in Korea.

Reports on cestode genus Senga (Dollfus, 1934) (Ptychobothridae, Luhe, 1902) of Mastacembelus armatus from Marathwada region Maharashtra, India

The present investigation deals with biosystematic studies of Pseudophyllidean tapeworm Senga i.e. S. satarensis, S. madhavae, S. mangalbai and S.microrostellata collected from intestine of a Mastacembelus armatus at various places of Marathwada Region (M.S.) India during the period of May, 2012 to Oct., 2013. The worm of present study come closer to all known species of this genus in general topography of organ but differs due to morphometeric measurements and morphological characteristics. The Senga satarensis (Bhure et.al., 2011) comes closer to known species of the genus Senga Dollfus, 1934 in general topography of organ but differs due to taxonomic characters as scolex pear shaped, rostellum bearing 28-30 rostellar hooks, neck absent, testes 175-200 in numbers, cirrus pouch oval, ovary bilobed, vagina runs posteriorly, genital pores oval, vitellaria granular, uterus saccular and egg elongated. The Senga madhavae (Bhure et.al.,2010) comes closer to known species of this genus in general topography of organ but differs due to scolex triangular, rostellum bearing 40-44 rostellar hooks, neck absent, mature proglottids five to six times broader than long, testes 200-220 in numbers, cirrus pouch oval, ovary dumb-bell shaped, genital pores oval in shape, vitellaria granular, uterus saccular and egg elongated. The Senga mangalbai (Bhure et.al.,2011) comes closer to all the known species of this genus in general topography of organ but differs due to scolex conical, hooks 38-42 in numbers, absence of neck, testes 70-80 in numbers, ovary bilobed, each lobe nut shaped and vitellaria granular. The Senga microrostellata (Bhure et.al.,2014) comes closer to all known species of this genus in general topography of organ but differs due to scolex triangular, bothria sessile, rostellum armed with 18-20 hooks which is single circled, absence of neck, mature proglottids 8-9 times broader than long, testes 250-300 in numbers, cirrus pouch elongated, vagina runs posteriorly, ovary dumb-bell shaped, uterus sacular filled with non-operculated eggs and Vitellaria follicular.

The Pampas fox (Lycalopex gymnocercus) as new definitive host for Spirometra erinacei (Cestoda: Diphyllobothriidae)

Spirometra erinacei, Faust, Campbell and Kellogg, 1929, is a pseudophyllidean cestode of the family Diphyllobothriidae. The genus Spirometra is cosmopolitan and these parasites infect carnivores, specially felids and canids. In Argentina, S. erinacei and S. mansonoides have been reported sporadically only in domestic definitive hosts. The Pampas fox, Lycalopex gymnocercus, is the most abundant native carnivore in southern South America, where it inhabits grasslands and open woodlands and areas highly modified by extensive ranching and agricultural activities. This report describes the first finding of S. erinacei infecting Pampas fox, and provides an estimate prevalence of this cestode in rural areas of southern Buenos Aires province, Argentina based on 78 complete Pampas fox intestine samples analysis. This study found a 15.4% of prevalence of S. erinacei in small intestine (adult stage) and a 21.8% in fecal samples (egg stage). In the present work, the first case of S. erinacei in a wild definitive host from Argentina was reported expanding the list of definitive hosts of S. erinacei in South America.

Subcutaneous sparganosis, a zoonotic cestodiasis, in two cats

Sparganosis is a zoonotic cestodiasis of human beings and animals caused by plerocercoid or second-stage larvae (sparganum) of pseudophyllidean tapeworms in host tissues. Cats are among definitive hosts in which the larva develops to adult stage in the intestines. Reports on larval infection involving various tissues and organs in cats are scarce. Rare single case reports of visceral sparganosis in cats are previously documented. The present report documents an unusual subcutaneous sparganosis in 2 Domestic Shorthair cats from southern Georgia. Veterinary clinicians should consider sparganosis as differential diagnosis for subcutaneous cyst-like masses in cats. As infected animals and animal tissues are sources of human infection, sparganosis warrants public awareness and due precaution to avoid human infection.

Parasitic infections of the African dwarf crocodile (Osteolaemus tetraspis) and the ornate Nile monitor (Varanus ornatus) from Nigeria

The parasitic infections of market derived Osteolaemus tetraspis from the rainforest and Varanus ornatus from locations in the savanna-mosaic and the rainforest of southern Nigeria were investigated. Parasites recovered from O. tetraspis included members of the Pentastomida, Trematoda and Nematoda. An undescribed pentastomid belonging to the family Sebekidae was recovered from O. tetraspis. The same parasite was also found to parasitize V. ornatus from the rainforest. Other parasites found in O. tetraspis were Pseudoneodiplostomum thomasi, Dujardinascaris sp. and larva of a Camallanus sp. Varanus ornatus from the rainforest and the derived savanna had some parasites including Duthiersia fimbriata, an unidentified pseudophyllidean cestode and Tanqua tiara in common. Cosmocerca ornata and Oswaldocruzia hoepplii were restricted to hosts from the derived savanna while the unidentified trematode occurred only in lizards from the rainforest. The unidentified pseudophyllidean cestode bears a close resemblance to Probothriocephalus, a cestode previously reported only from deep water teleosts. Pseudoneodiplostomum thomasi and Duthiersia fimbriata are new locality records for Nigeria.

Castration of Female Ninespine Stickleback by the Pseudophyllidean Cestode Schistocephalus pungitii: Evolutionary Significance and Underlying Mechanism

Parasitic castration may result from manipulation of host energy allocation away from reproduction, which should result in castration of lightly infected hosts as well as heavily infected ones. Castration also may result from nutrient theft alone, which incidentally influences host energy allocation to reproduction and should cause reproduction to end in heavily infected hosts. Although the pseudophyllidean cestode Schistocephalus pungitii is a castrator of ninespine stickleback fish (Pungitius pungitius), the cause and significance of castration remain unknown. We used predictions about reproductive capacity in lightly and heavily infected hosts and host size (age) at which castration occurs to address these questions. In Airolo Lake, Alaska, we found that inhibition of reproduction in ninespine stickleback occurs in small fish before the size (age) of sexual maturity and is not instantaneous. Castration was observed in lightly and heavily infected adult-size hosts. Infected fish do not reach the same size as uninfected fish, possibly because of growth inhibition or selective predation. Castration in infected adult-size female ninespine stickleback appears to be the result of adaptive manipulation of host energy allocation by the parasite, but it could result from an energy budget readily influenced by parasitism.

Functional expression and characterization of a cytosolic copper/zinc-superoxide dismutase of Spirometra erinacei

Spirometra erinacei is a pseudophyllidean tapeworm which inhabits the intestines of cats and dogs. The infections are usually asymptomatic in these animals, but the infection of the plerocercoid larvae of the parasite, spargana, cause sparganosis in other vertebrates, including human. In this study, we identified a gene encoding the copper/zinc-superoxide dismutase of S. erinacei (SeCuZn-SOD) and partially characterized the biochemical and functional properties of the enzyme. The open reading frame of SeCuZnSOD was 465 bp that encodes 154 amino acids. The characteristic amino acid residues and motifs required for coordinating copper and zinc enzymatic function were well conserved. The genomic length of the SeCuZnSOD was 1,985 bp consisting of three exons that are separated by two introns. SeCuZnSOD is a typical cytosolic form which shares similar biochemical properties, including broad pH optima and inhibition profile by KCN and H(2)O(2), with cytosolic Cu/Zn-SODs of other organisms. SeCuZnSOD was functionally expressed in both S. erinacei plerocercoid larvae and adult worms, and its expression level was significantly increased when the plerocercoid larvae were treated with paraquat. The enzyme may play essential roles for survival of the parasite not only by protecting itself from endogenous oxidative stress, but also by detoxifying oxidative killing of the parasite by host immune effector cells.

Endoparasitism in captive wild‐caught snakes indigenous to Kerala, India

In this preliminary survey, coprologic examination of six different captive snake species housed in three different herpetariums of Kerala state was conducted from July 2005 to January 2006, to study the prevalence of endoparasites. Of the 25 snakes examined, 22 (88%) were found infected. On the basis of morphology and morphometry, Capillaria spp. (72%), strongyle (28%), spirurid (20%), Strongyloides/Rhabdias spp. (16%), ascarid (12%), pseudophyllidean tapeworm (8%), acanthocephalan (4%) and pentastomid (12%) ova were identified. The occurrence of ova of Hymenolepis spp. as pseudoparasite was also noticed.

Proliferative sparganosis in a dog

A 21-month-old spayed female Border Collie was examined because of progressive right forelimb lameness, signs of pain, and subcutaneous edema. The dog lived in a fenced yard in Tampa, Fla, that contained a small area of marshy terrain. The subcutis and intermuscular fascia contained multiple cystic cavities filled with larval cestodes (plerocercoids or spargana) and cloudy red fluid. Parasites were identified morphologically and by DNA sequence analysis as pseudophyllidean cestodes, most likely Sparganum proliferum. The dog developed a progressively worsening fever, dyspnea, mature neutrophilia, and hypoproteinemia. Septic pleuritis and peritonitis complicated the later stages of the disease. Treatment with praziquantel, fenbendazole, and nitazoxanide failed to control the proliferation and dissemination of larval cestodes. The dog was euthanatized after 133 days of treatment. At necropsy, numerous parasitic tissue cysts were present in the subcutis and intermuscular fascia; these cysts were most abundant in the soft tissues of the forelimbs and cervical musculature. The pleural and peritoneal cavities contained multiple larval cestodes and were characterized by neutrophilic inflammation and secondary bacterial infection. Findings indicated that clinical signs associated with proliferative sparganosis in dogs may be rapidly progressive and that the condition may be refractory to antiparasitic treatment. Veterinarians should be aware of this zoonotic, water-borne agent.

An immunocytochemical, histochemical and ultrastructural study of the nervous system of the tapeworm Cyathocephalus truncatus (Cestoda, Spathebothriidea)

This study is the first detailed study of the organisation of the neuromuscular system of Cyathocephalus truncatus (Cestoda, Spathebothriidea). Five techniques have been used: (1) immunocytochemistry, (2) staining with TRITC-conjugated phalloidin, (3) NADPHdiaphorase histochemistry, (4) confocal scanning laser microscopy and (5) transmission electron microscopy. The patterns of nerves immunoreactive (IR) to antibodies towards serotonin (5-HT) and the invertebrate neuropeptide FMRFamide are described in relation to the musculature. The patterns of NADPHdiaphorase positive nerves and 5-HT-IR nerves are compared. The fine structure of the nervous system (NS) is described. The organisation of NS in the non-segmented, polyzoic C. truncatus differs clearly from that in the non-segmented, monozoic Caryophyllaeus laticeps and shows distinct similarities with the NS in pseudophyllidean cestodes. This supports the hypothesis that taxon Caryophyllidea and Spatheobothriidea form independent lineages within Eucestoda.

Growth and energetics in the stickleback–Schistocephalus host–parasite system: a review of experimental infection studies

Summary Three-spined sticklebacks in natural lacustrine populations are often infected with plerocercoids of the indirectly transmitted pseudophyllidean cestode Schistocephalus solidus. Field studies typically show infections to be associated with reduced host condition, gonadogenesis and energy reserves, though infection phenotypes can vary considerably both between and within host populations. Experimental infection studies allow the impact of infections on hosts to be studied under a variety of rearing conditions, and so can be used to determine the environmental component of infection phenotypes. Here, we review recent laboratory studies undertaken by our group, examining the growth and condition of experimentally infected fish reared under conditions that differed in terms of absolute ration, temporal pattern of feeding and level of competition between fish. We compare infection phenotypes generated in our experimental studies with those of fish sampled in field based studies. Experimental studies in which infected fish were reared under competition for limited food resources, or were fed a restricted diet, generated infection phenotypes that most closely resembled those found in the majority of natural populations. When access to food was unrestricted, however, infected fish were able to sustain high growth rates and lay down energy reserves. If experimental studies are to be used to understand the impact of infection under natural conditions, husbandry protocols that closely match field conditions must be designed. We suggest that a full understanding of the impact of parasites on their hosts can only be gained by integrating controlled laboratory experiments with detailed field studies. The stickleback‐Schistocephalus system is ideally suited to examining these questions, and we provide several suggestions for future research.