Aberrant sparganosis in cat caused by Spirometra mansoni (Cestoda: Diphyllobothriidae): a case report.

BACKGROUND: Sparganosis is a rare zoonotic disease caused by plerocercoid larvae of the genera Spirometra or Sparganum (Cestoda: Diphyllobothriidae). The larvae of Spirometra generally do not undergo asexual reproduction, whereas those of Sparganum can induce proliferative lesions in infected tissues. This paper presents an unusual case of proliferative sparganosis due to infection with Spirometra mansoni in a cat, normally considered a definitive host of the species. CASE PRESENTATION: A 9-year-old male domestic cat was presented with a mass on the right side of the face that underwent progressive enlargement for 1 month. The morphological and histopathological examinations revealed multiple asexual proliferative cestode larvae in the lesions, suggestive of proliferative sparganosis. Next-generation sequencing analysis of formalin-fixed and paraffin-embedded specimens of surgically excised tissue indicated that the worm was Spirometra mansoni. CONCLUSION: Although S. mansoni a common tapeworm species found in the small intestine of domestic cats and dogs in Japan, proliferative sparganosis is extremely rare. This is the first confirmed case of proliferative sparganosis due to infection with S. mansoni in cat.

Identification of a Clinical Spirometra mansoni Plerocercoid Isolate Using Molecular and Morphological Data.

Sparganosis has been a neglected parasitic zoonosis for a long time. The accurate identification of Spirometra tapeworms in clinical practice is poorly understood. A case of breast sparganosis was reported in Henan Province of central China. One plerocercoid approximately 3.5 cm in length was collected from the patient. The clinical isolate was identified as Spirometra mansoni based on the barcoding sequences of mitochondrial cytochrome c oxidase subunit 1 (cox1). Finally, the epidemiology of sparganosis in central China was reviewed. Comprehensive public health education should be carried out, and the risky habit of eating live tadpoles must be discouraged in Henan Province.

Molecular identification of Spirometra infections in companion animals and wildlife in Japan.

Spirometra infections in companion animals and wildlife in Japan have been diagnosed based on the morphology of the adult worms and eggs, and the etiological agent has been mainly ascribed to Spirometra erinaceieuropaei. However, recent studies have revealed that two other species, Spirometra mansoni and Spirometra asiana, coexist in Japan. Spirometra asiana is a new species recently discovered in Japan. Although morphological discrimination between these two species is difficult, molecular identification is useful. Therefore, to understand which species commonly parasitizes companion animals and wildlife in Japan, a preliminary study was performed based on mitochondrial DNA analysis. Eleven adult worms examined were identified as S. mansoni, suggesting that S. mansoni infects companion animals and wildlife commonly than S. asiana in Japan.

Molecular identification of sparganum of Spirometra mansoni isolated from the abdominal cavity of a domestic cat in Vietnam.

Cats normally play a role of the definitive host in which the plerocercoid (sparganum), the second larval form of Spirometra spp., develops into an adult in the intestines. However, some cases of cats with visceral or subcutaneous sparganosis were sporadically reported worldwide. We herein documented the discovery of a sparganum in abdominal cavity of a domestic cat during a surgery of dystocia. The larva was molecularly identified as Spirometra mansoni, belonging to Type I, that was recently misidentified to be S. erinaceieuropaei in several Asian countries. This is the first report for sparganum of S. mansoni in the cat. The future study is necessary to provide further insights into the species of Spirometra causing sparganosis and spirometrosis in humans and other animals.

Integrated transcriptomic and proteomic analyses of plerocercoid and adult Spirometra mansoni reveal potential important pathways in the development of the medical tapeworm.

BACKGROUND: Spirometra mansoni can parasitize animals and humans through food and water, causing parasitic zoonosis. Knowledge of the developmental process of S. mansoni is crucial for effective treatment; thus, it is important to characterize differential and specific proteins and pathways associated with parasite development. METHODS: In this study, we performed a comparative proteomic analysis of the plerocercoid and adult stages using a tandem mass tag-based quantitative proteomic approach. Additionally, integrated transcriptomic and proteomic analyses were conducted to obtain the full protein expression profiles of different life cycle stages of the tapeworm. RESULTS: Approximately 1166 differentially expressed proteins (DEPs) were identified in adults versus plerocercoids, of which 641 DEPs were upregulated and 525 were downregulated. Gene Ontology (GO), Clusters of Orthologous groups (COG) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses indicated that most DEPs related to genetic information processing and metabolism of energy in adults seem to be more activated. In the plerocercoid stage, compared to metabolism, genetic information processing appears more dynamic. Protein-protein interaction (PPI) revealed six key proteins (phosphomannomutase, glutathione transferase, malate dehydrogenase, cytoplasmic, 40S ribosomal protein S15, ribosomal protein L15 and 60S acidic ribosomal protein P2) that may play active roles in the growth and development of S. mansoni. Finally, the combination of transcriptomic and proteomic data suggested that three pathways (ubiquitin-mediated proteolysis, phagosome and spliceosome) and five proteins closely related to these pathways might have a significant influence in S. mansoni. CONCLUSIONS: These findings contribute to increasing the knowledge on the protein expression profiles of S. mansoni and provide new insights into functional studies on the molecular mechanisms of the neglected medical tapeworm.

Molecular Characteristics of the Fatty-Acid-Binding Protein (FABP) Family in Spirometra mansoni-A Neglected Medical Tapeworm.

The plerocercoid larva of the tapeworm Spirometra mansoni can parasitize humans and animals, causing serious parasitic zoonosis. The molecular characteristics and adaptive parasitism mechanism of Spirometra tapeworms are still unknown. In this study, 11 new members of the fatty-acid-binding protein (FABP) family were characterized in S. mansoni. A clustering analysis showed 11 SmFABPs arranged into two groups, and motif patterns within each group had similar organizations. RT-qPCR showed that SmFABPs were highly expressed in the adult stage, especially in gravid proglottid. A high genetic diversity of SmFABPs and relative conservation of FABPs in medical platyhelminthes were observed in the phylogenetic analysis. Immunolocalization revealed that natural SmFABP is mainly located in the tegument and parenchymal tissue of the plerocercoid and the uterus, genital pores, and cortex of adult worms. rSmFABP can build a more stable holo form when binding with palmitic acid to protect the hydrolytic sites of the protein. A fatty acid starvation induction test suggested that SmFABP might be involved in fatty acid absorption, transport, and metabolism in S. mansoni. The findings in this study will lay the foundation to better explore the underlying mechanisms of FABPs involved in Spirometra tapeworms as well as related taxa.

Spirometra mansoni sparganosis identified by metagenomic next-generation sequencing: a case report.

A 30-year-old male patient had a cyst on the left hip and progressive enlargement for more than 2 months. Combined blood tests, magnetic resonance imaging, and pathology findings, cysticercosis infection was suspected. However, the treatment for cysticercosis was ineffective. We conducted a metagenomic next-generation sequencing (mNGS) analysis on the formalin-fixed, paraffin-embedded specimen of the patient's surgically excised tissue, and the results suggested Spirometra mansoni, mNGS was further confirmed by polymerase chain reaction and phylogenetic analysis of cytochrome c oxidase subunit 1 (cox1) gene. Based on these results, we found that mNGS provided a better method of diagnosing parasitic infections.

Biochemical characterization of mitochondria from adult worms and plerocercoid larvae of Spirometra mansoni shows mixed populations of anaerobic and aerobic mitochondria.

The mitochondria of adult and plerocercoid Spirometra mansoni were characterized in isolated mitochondria and in situ by electron microscopic histochemistry with special attention to the respiratory chain. Although the specific activities of the constituent enzyme complexes of succinate oxidase are fairly similar in adult and plerocercoid mitochondria, those of succinate oxidase and NADH-FRD are approximately 4- and 25-fold higher in adult mitochondria than in plerocercoid mitochondria, respectively. Quinone analysis by high performance liquid chromatography and mass spectrometry showed that adult and plerocercoid mitochondria contained both rhodoquinone-10 and ubiquinone-10 at concentrations of 4.98 and 0.106 nmol mg-1 for adult, and 0.677 and 0.137 nmol mg-1 for plerocercoid, respectively. Inhibition studies on the succinate-oxidase system of adult mitochondria showed that they possessed both cyanide-sensitive and -insensitive succinate oxidases, the latter of which produces hydrogen peroxide. Adult mitochondria, when NADH was used as a substrate, were shown to produce hydrogen peroxide, and the production of hydrogen peroxide decreased to undetectable levels in the presence of fumarate. The specific activities of NADH-fumarate reductase and cytochrome c oxidase were significantly higher in mature proglottids than in immature and gravid proglottids. Isopycnic density-gradient centrifugation analyses and in situ electron microscopic histochemistry revealed that both adult and plerocercoid mitochondria were heterogeneous in terms of respiratory function and physicochemical properties. The physiological significance of adult and plerocercoid mitochondria is discussed in relation to the oxygen tension of their parasitic habitats.

Presence of Spirometra mansoni, Causative Agent of Sparganosis, in South America.

We report molecular identification of an adult Spirometra mansoni tapeworm retrieved from a crab-eating fox (Cerdocyon thous) in Colombia, confirming presence of this parasite in South America. This tapeworm is the causative agent of human sparganosis, commonly reported from Southeast Asia, and represents the second congeneric species with known zoonotic potential in the Americas.

Case Report: Moving Tumor-Like Foci Behind Refractory Epilepsy-Cerebral Sparganosis Successfully Treated by Surgery After Failure of Praziquantel Treatment.

Cerebral sparganosis is clinically non-specific and easily misdiagnosed, exposing patients to the risk of severe brain damage and neurological dysfunction caused by actively migrating larvae. Diagnostic biomarkers from typical cases can help to establish an early diagnosis and proper treatment. We present a 25-year-old woman who suffered from 9 years of refractory epilepsy and was misdiagnosed with glioma and subjected to surgery. The postoperative pathology confirmed granuloma, and the tumor-like foci reappeared 3 months later. Along with the "tunnel sign" on MRI, cerebral sparganosis was suspected and confirmed by positive serum and cerebrospinal fluid antibodies against Spirometra mansoni. The patient visited us after a failure of four cycles of praziquantel treatment, recurrent seizures and hemiplegia with basal ganglia foci. Craniotomy was not carried out until the larva moved to the superficial lobe on follow-up MRIs, and pathology revealed sparganosis granuloma. The patient became seizure-free and recovered myodynamia but had long-lasting cognitive dysfunction due to severe brain damage. This case indicated the importance of tunnel signs and moving tumor-like foci on MRI as diagnostic clues of cerebral sparganosis. An early diagnosis is vitally important to avoid severe neural dysfunction by the long-living and moving larvae. Surgical removal of the larva is a critical remedy for cases failed by praziquantel treatment.

Identification of an enolase gene and its physiological role in Spirometra mansoni.

Enolase is a crucial enzyme involved in the glycolytic pathway and gluconeogenesis in parasites. It also has been reported to function as a plasminogen receptor and may be involved in tissue invasion. In this study, the biochemical properties of the enolase of Spirometra mansoni (Smenolase) were investigated. The Smenolase gene was found to cluster closely with the enolase genes of Clonorchis sinensis and Echinococcus granulosus, and some functional motifs were identified as conserved. Smenolase was confirmed to be a component of the secretory/excretory products (ESPs) and a circulating antigen of spargana. Recombinant Smenolase expressed in vitro was able to bind to human plasminogen. Smenolase was detected in the eggs, testicles, and vitellaria of adult worms and the tegument of spargana. The transcription level of Smenolase was highest at the gravid proglottid stage. When spargana were cultured with glucose of different concentration in vitro, it was observed that the expression levels of Smenolase in the low-glucose groups were consistent with that of Smenolase in vivo. These results indicate that Smenolase is a critical enzyme involved in supplying energy to support the development and reproduction of the parasite, and it may also play a role in sparganum invasion.

A case of human breast sparganosis diagnosed as Spirometra Type I by molecular analysis in Japan.

A 92-year-old Japanese woman presented with a mass in the left breast, and sparganosis was suspected by biopsy of the mass. The mass disappeared once, but it reappeared at the same site one year later. For a definitive diagnosis, the mass was surgically removed, and a sparganum-like worm was detected. The causative agent was confirmed as Spirometra Type I (most probably Spirometra mansoni) by mitochondrial DNA analysis. The serological examination also proved the case as sparganosis. Considering the presence of two Spirometra species (Type I and II) in Asia, particularly Japan, molecular analysis of the causative agents is highly recommended to understand the epidemiology, infection sources, and pathogenicity in humans in both species, if the parasite specimens are available.

Spirometra species from Asia: Genetic diversity and taxonomic challenges.

Despite considerable controversy concerning the taxonomy of species within the genus Spirometra, human sparganosis and spirometrosis mainly in Asia and Europe has long been confidently ascribed to Spirometra erinaceieuropaei. Recently, the mitochondrial genomes of purported "S. erinaceieuropaei", "Spirometra decipiens" and "Spirometra ranarum" from Asia have been determined. However, it has been pointed out that the morphological criteria used for identifying these species are unsuitable and thus these identifications are questionable. In the present study, therefore, Spirometra samples from Asia were re-examined based on mitochondrial cytochrome c oxidase subunit 1 gene sequences and the identification of these species was discussed. Haplotype network and phylogenetic analyses revealed that: i) two distinct Spirometra species, Type I and Type II, are present in Asia and neither of which is close to likely European "S. erinaceieuropaei"; ii) Type I is genetically diverse and widely distributed, however Type II is known so far from Japan and Korea; iii) "S. decipiens" and "S. ranarum" reported from Asia are conspecific with Type I; iv) Type I is probably conspecific with Spirometra mansoni, and Type II may represent an undescribed species.

[Prevalence of Spirometra mansoni infections in hosts in Jiangsu Province].

OBJECTIVE: To investigate the prevalence of Spirometra mansoni infections in hosts in Jiangsu Province, so as to provide the scientific basis for the management of sparganosis mansoni. METHODS: From 2018 to 2019, nine counties (cities, districts) were randomly selected from Jiangsu Province as the survey sites, and 100 healthy individuals were randomly selected to perform the serological test of S. mansoni infections and the detection of S. mansoni eggs. The procercoids were detected in the intermediate host Cyclops, and the S. mansoni eggs were identified in the stool samples of the definitive hosts cats and dogs. RESULTS: The prevalence of S. mansoni human infections was 0 (0/900) in the 9 survey sites of Jiangsu Province, and the sero-prevalence of the specific IgG antibody against S. mansoni was 1.22% (11/900). The positive rate of procercoids was 0.33% (3/900) in Cyclops. In addition, the S. mansoni egg-positive rate was 1.48% (2/135) in cats and dogs. CONCLUSIONS: Sparganosis mansoni is prevalent in Jiangsu Province. Health education pertaining to the damages of sparganosis mansoni and the route of S. mansoni infections should be improved.

Prevalence of Spirometra mansoni infections in hosts in Jiangsu Province / 中国血吸虫病防治杂志

Objective To investigate the prevalence of Spirometra mansoni infections in hosts in Jiangsu Province, so as to provide the scientific basis for the management of sparganosis mansoni. Methods From 2018 to 2019, nine counties (cities, districts) were randomly selected from Jiangsu Province as the survey sites, and 100 healthy individuals were randomly selected to perform the serological test of S. mansoni infections and the detection of S. mansoni eggs. The procercoids were detected in the intermediate host Cyclops, and the S. mansoni eggs were identified in the stool samples of the definitive hosts cats and dogs. Results The prevalence of S. mansoni human infections was 0 (0/900) in the 9 survey sites of Jiangsu Province, and the sero-prevalence of the specific IgG antibody against S. mansoni was 1.22% (11/900). The positive rate of procercoids was 0.33% (3/900) in Cyclops. In addition, the S. mansoni egg-positive rate was 1.48% (2/135) in cats and dogs. Conclusions Sparganosis mansoni is prevalent in Jiangsu Province. Health education pertaining to the damages of sparganosis mansoni and the route of S. mansoni infections should be improved.

A case of mammary sparganosis due to infection with Spirometra mansoni.

The authors report the case of a 56-year-old woman with mammary sparganosis due to infection with a plerocercoid tapeworm larva of Spirometra mansoni. Magnetic resonance imaging revealed an area of heterogeneous density in outer upper quadrant of the right breast, with a high likelihood of malignancy. During surgery for the removal of a granuloma, the parasite was discovered and excised. The authors review the pathological and imaging features of mammary sparganosis.

Subcutaneous sparganosis mimicking soft tissue tumor: a case report.

BACKGROUND: Sparganosis is a rare parasitic disease of humans caused by invasion of human tissue by plerocercoid tapeworm larvae (spargana) of the genus Spirometra species. This parasite commonly invades subcutaneous tissue but can appear in any tissue of the body. CASE PRESENTATION: Here, we report a case of a 33-year-old woman presented with a migrating painful swelling and erythema in right thigh for 6 months, which was initially misdiagnosed as soft tissue tumor. Magnetic resonance imaging revealed a multiple elongated tubular tracts in the medial aspect of right thigh, from which a long, wrinkled, whitish worm was surgically removed. The parasite was histopathologically identified as Spirometra mansoni. CONCLUSION: Sparganosis is rare and physicians have little experience, so if suspected, should be included among the list of differential diagnosis and special serological test should be recommended before surgery.

First report of sparganosis manifested by pleuritis and decreased peripheral blood eosinophils in Jiangsu province, China.

Sparganosis is a parasitic infection caused by the metacestode stage of Spirometra mansoni and some other related diphyllobothriidean cestodes. Although various internal organs were involved in sparganum infection, pulmonary and pleural involvement is rarely reported. We herein report an uncommon form of sparganosis manifested by pleuritis and decreased peripheral blood eosinophils. Sparganum worms were found in the pleural effusion accidentally and confirmed by pathological diagnosis. After being treated with praziquantel for 10 days, the patient's symptoms, laboratory examinations, and imaging findings were improved gradually.

Prevalence of Spirometra mansoni in dogs, cats, and frogs and its medical relevance in Guangzhou, China.

BACKGROUND: Sparganosis is an important parasitic disease in Guangzhou and is mainly acquired through the consumption of frog meat or contact with fresh frogs infected by larval stages (spargana) of the tapeworm species Spirometra mansoni. METHODS: In this study, the prevalence of intestinal S. mansoni infections (with adult parasites) in dogs and cats and of extraintestinal S. mansoni infections (with spargana) in frogs was assessed. In addition, a questionnaire survey was carried out among residents in Guangzhou City in order to evaluate their awareness about the medical and epidemiological relevance of Spirometra and sparganosis. RESULTS: In total, the feces of 229 dogs and 116 cats were examined for eggs, and 1949 frogs were examined for spargana. Sixty-three dogs (27.5%) and 47 cats (40.5%) had eggs in their feces. Two hundred and sixteen out of 416 wild Rana tigrina rugulosa Wiegmann frogs examined were sparganum-positive, with an infection rate of 51.9%, while the infection rate in Rana limnocharis Boie was 35.1% (13/37). None of the tested farmed frogs (including R. tigrina rugulosa and Rana catesbeiana) was positive (0/1382). Analysis of the questionnaire revealed the following results: (1) about 41.0% of residents in Guangzhou had some knowledge of sparganosis or sparganum infection, and information in TV programs was the most important way that residents learned about sparganosis. (2) About 59.9% of the residents ate frog meat. Eating the meat, viscera, or blood of animals, e.g., frogs, snakes, pigs, chicken, mice, and birds, in an improper way might be the main means by which residents acquire the infection. (3) The risk of sparganum infection was higher in males than in females. CONCLUSIONS: A high sparganum infection rate was observed in the wild frogs sold in agricultural product markets in Guangzhou. The infection was also serious in cats and dogs in Guangdong Province. With lifestyles and eating habits resulting in sparganum infection, it is necessary to focus on market management and community education in order to prevent the transmission of this disease in Guangzhou.

Eosinophilic pleural effusion due to Spirometra mansoni spargana: a case report and review of the literature.

A 36-year-old female presented with an eosinophilic pleural effusion. The eosinophilic pleural effusion was considered to have been caused by a parasitic infection. Spirometra mansoni spargana was confirmed by semi-rigid thoracoscopy. About 2 months after treatment with praziquantel for 3 days, the pleural effusion had disappeared on the chest roentgenogram.