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Schistosoma

A genus of trematodes, Schistosoma, commonly known as blood-flukes, are parasitic flatworms which are responsible for a highly significant group of infections in humans termed schistosomiasis. Schistosomiasis is considered by the World Health Organization as the second most socioeconomically devastating parasitic disease, (after malaria), with hundreds of millions infected worldwide.[1][2]

Adult flatworms parasitize mesenteric blood vessels. They are unique among trematodes and any other flatworms in that they are dioecious with distinct sexual dimorphism between male and female. Thousands of eggs are released and reach either the bladder or the intestine (according to the infecting species), and these are then excreted in urine or feces to fresh water. Larvae must then pass through an intermediate snail host, before the next larval stage of the parasite emerges that can infect a new mammalian host by directly penetrating the skin.

History[edit]

The eggs of these parasites were first seen by Theodor Maximilian Bilharz, a German pathologist working in Egypt in 1851 who found the eggs of Schistosoma haematobium during the course of a post mortem. He wrote two letters to his former teacher von Siebold in May and August 1851 describing his findings. Von Siebold wrote a paper (published in 1852) summarizing Bilharz's findings. Bilharz wrote a paper in 1856 describing the worms more fully and he named them Distoma haematobium. Their unusual morphology meant that they could not be comfortably included in Distoma. So in 1856 Meckel von Helmsback created the genus Bilharzia for them. In 1858 Weinland proposed the name Schistosoma (Greek: 'split body') after the male worms' morphology. Despite Bilharzia having precedence the genus name Schistosoma was officially adopted by the International Commission on Zoological Nomenclature. The term Bilharzia to describe infection with these parasites is still in use in medical circles.

Bilharz also described Schistosoma mansoni but this species was redescribed by Louis Westenra Sambon in 1907 at the London School of Tropical Medicine who named it after his teacher Patrick Manson.

In 1898, all the then known species were placed in a subfamily by Stiles and Hassel. This was then elevated to family status by Looss in 1899. Poche in 1907 corrected a grammatical error in the family name. The life cycle was determined by da Silva in 1908.

In 2009, the genomes of Schistosoma mansoni and Schistosoma japonicum were decoded [3][4] opening the way for new targeted treatments. In particular, the study discovered that the genome of S. mansoni contained 11,809 genes including many which produce enzymes for breaking down proteins which enable the parasite to bore through tissue. Also, S. mansoni does not have an enzyme to make certain fats so that it must rely on its host to produce these.[5]

Evolution[edit]

Electron micrograph of an adult male Schistosoma parasite worm. The bar (bottom left) represents a length of 500 μm.

The origins of this genus remain unclear. For many years it was believed that this genus had an African origin but DNA sequencing suggests that the species (S. edwardiense and S. hippopotami) that infect the hippo (Hippopotamus amphibius) could be basal. Since hippos were present in both Africa and Asia during the Cenozoic era the genus might have originated as parasites of hippos.[6] The original hosts for the South East Asian species were probably rodents.

Based on the phylogenetics of the host snails it seems likely that the genus evolved in Gondwana between 70 million years ago and 120 million years ago.[7]

The sister group to Schistosoma is a genus of elephant-infecting schistosomes — Bivitellobilharzia. The cattle, sheep, goat and cashmere goat parasite Orientobilharzia turkestanicum appears to be related to the African schistosomes.[8][9] This latter species has since been transferred to the genus Schistosoma.[10]

Within the haematobium group S. bovis and S. curassoni appear to be closely related as do S. leiperi and S. mattheei.

S. mansoni appears to have evolved in East Africa 0.43–0.30 million years ago.

S. incognitum and S. nasale are more closely related to the African species rather than the japonicum group.

S. sinensium appears to have radiated during the Pliocene.

S. mekongi appears to have invaded South East Asia in the mid-Pleistocene.

Estimated speciation dates for the japonicum group: ~3.8 million years ago for S. japonicum/South East Asian schistosoma and ~2.5 million years ago for S. malayensis/S. mekongi.

Schistosoma turkestanicum is found infecting red deer in Hungary. These strains appear to have diverged from those found in China and Iran.[11] The date of divergence appears to be 270,000 years before present.

Taxonomy[edit]

The genus Schistosoma as currently defined is paraphyletic so revisions are likely. Currently over twenty species are recognised within this genus.

The genus has been divided into four groups — indicum, japonicum, haematobium and mansoni. The affinities of the remaining species are still being clarified.

Thirteen species are found in Africa. Twelve of these are divided into two groups — those with a lateral spine on the egg (mansoni group) and those with a terminal spine (haematobium group).

The four mansoni group species are: S. edwardiense, S. hippotami, S. mansoni and S. rodhaini.

The nine haematobium group species are: S. bovis, S. curassoni, S. intercalatum, S. guineensis, S. haematobium, S. kisumuensis, S. leiperi, S. margrebowiei and S. matthei.

S. leiperi and S. matthei appear to be related.[12] S. margrebowiei is basal in this group.[13] S. guineensis is the sister species to the S. bovis and S. curassoni grouping. S. intercalatum may actually be a species complex of at least two species.[14][15]

S. spindale is widely distributed in Asia but is also found in Africa.

The other species occur in Asia and India.

The indicum group has three species: S. indicum, S. nasale and S. spindale. This group appears to have evolved during the Pleistocene. All use pulmonate snails as hosts.

S. indicum is found in India and Thailand.

This group appears to be the sister clade to the African species.[16]

The japonicum group has three species: S. japonicum, S. malayensis and S. mekongi.

S. sinensium is a sister clade to the S. japonicum group and is found in China.

S. ovuncatum forms a clade with S. sinensium and is found in northern Thailand. The definitive host is the rat (Rattus rattus) and the intermediate host is the snail Tricula bollingi. This species is known to use snails of the family Pomatiopsidae as hosts.

S. incognitum appears to be basal in this genus. It may be more closely related to the African/Indian species than to the South East Asian group. This species uses pulmonate snails as hosts.

New species[edit]

Four additional species have been transferred to this genus.[10] These were previously classified as species in the genus Orientobilharzia. Orientobilharzia differs from Schistosoma morphologically only on the basis of the number of testes. A review of the morphological and molecular data has shown that the differences between these genera are too small to justify their separation. The four species that have been transferred to this genus are

Examination of the mitochondria suggests that Schistosoma incognitum may be a species complex.[17]

Cladogram[edit]

A cladogram based on 18S ribosomal RNA, 28S ribosomal RNA, and partial cytochrome-c oxidase I (COI) genes shows phylogenic relations of species in the genus Schistosoma:[18]













Schistosoma curassoni



Schistosoma intercalatum




Schistosoma bovis





Schistosoma leiperi



Schistosoma mattheei





Schistosoma haematobium




Schistosoma margrebowiei






Schistosoma spindale



Schistosoma indicum




Schistosoma nasale






Schistosoma mansoni



Schistosoma rodhaini





Schistosoma incognitum




Schistosoma turkestanicum





Schistosoma edwardiense



Schistosoma sp. from Ceratophallus natalensis








Schistosoma mekongi



Schistosoma malayensis




Schistosoma japonicum





Schistosoma sinensium



Schistosoma ovuncatum





Comparison of eggs[edit]

Schistosomiasis[edit]

The parasitic flatworms of Schistosoma cause a group of chronic infections called schistosomiasis known also as bilharziasis.[19] An anti-schistosome drug is a schistosomicide.

Species infecting humans[edit]

Parasitism of humans by Schistosoma appears to have evolved at least three occasions in both Asia and Africa.

  • S. haematobium, commonly referred to as the bladder fluke, originally found in Africa, the Near East, and the Mediterranean basin, was introduced into India during World War II. Freshwater snails of the Bulinus genus are an important intermediate host for this parasite. Among final hosts humans are most important. Other final hosts are rarely baboons and monkeys.[20]
  • S. intercalatum. The usual final hosts are humans. Other animals can be infected experimentally.[20]
  • S. japonicum whose common name is simply blood fluke is found widely spread in Eastern Asia and the southwestern Pacific region. In Taiwan this species only affects animals, not humans. Freshwater snails of the Oncomelania genus are an important intermediate host for S. japonicum. Final hosts are humans and other mammals including cats, dogs, goats, horses, pigs, rats and water buffalo.[20]
  • S. mekongi is related to S. japonicum and affects both the superior and inferior mesenteric veins. S. mekongi differs in that it has smaller eggs, a different intermediate host (Neotricula aperta) and longer prepatent period in the mammalian host. Final hosts are humans and dogs.[20] The snail Tricula aperta can also be experimentally infected with this species.
Human Schistosomes
Scientific NameFirst Intermediate HostEndemic Area
Schistosoma guineensisBulinus forskaliiWest Africa
Schistosoma intercalatumBulinus sppAfrica
Schistosoma haematobiumBulinus spp.Africa, Middle East
Schistosoma japonicumOncomelania spp.China, East Asia, Philippines
Schistosoma malayensisNot knownSouth East Asia
Schistosoma mansoniBiomphalaria spp.Africa, South America, Caribbean, Middle East
Schistosoma mekongiNeotricula apertaSouth East Asia

Species infecting animals other than humans[edit]

Schistosoma indicum, Schistosoma nasale, Schistosoma spindale,Schistosoma leiperi are all parasites of ruminants.

Schistosoma edwardiense and Schistosoma hippopotami are parasites of the hippo.

Schistosoma ovuncatum and Schistosoma sinensium are parasites of rodents.

Morphology[edit]

Adult schistosomes share all the fundamental features of the digenea. They have a basic bilateral symmetry, oral and ventral suckers, a body covering of a syncytial tegument, a blind-ending digestive system consisting of mouth, oesophagus and bifurcated caeca; the area between the tegument and alimentary canal filled with a loose network of mesoderm cells, and an excretory or osmoregulatory system based on flame cells. Adult worms tend to be 10–20 mm (0.4–0.8 in) long and use globins from their hosts' hemoglobin for their own circulatory system.

Reproduction[edit]

Unlike other trematodes, the schistosomes are dioecious — i.e., the sexes are separate. The two sexes display a strong degree of sexual dimorphism, and the male is considerably larger than the female. The male surrounds the female and encloses her within his gynacophoric canal for the entire adult lives of the worms, where they reproduce sexually.

Genome[edit]

The genomes of Schistosoma haematobium, S. japonicum and S. mansoni have been reported.[3][4][21][22]

References[edit]

  1. ^ "Schistosomiasis Fact Sheet". World Health Organization. Retrieved 10 August 2011. 
  2. ^ "Schistosomiasis". Centers for Disease Control and Prevention. Retrieved 10 August 2011. 
  3. ^ a b Zhou, Y.; Zheng, H.; Chen, Y.; Zhang, L.; Wang, K.; Guo, J.; Huang, Z.; Zhang, B.; Huang, W.; Jin, K.; Dou, T.; Hasegawa, M.; Wang, L.; Zhang, Y.; Zhou, J.; Tao, L.; Cao, Z.; Li, Y.; Vinar, T.; Brejova, B.; Brown, D.; Li, M.; Miller, D. J.; Blair, D.; Zhong, Y.; Chen, Z.; Liu, F.; Hu, W.; Wang, Z. Q.; Zhang, Q. H. (2009). "The Schistosoma japonicum genome reveals features of host–parasite interplay". Nature 460 (7253): 345–351. doi:10.1038/nature08140. PMC 3747554. PMID 19606140.  edit
  4. ^ a b Berriman, M.; Haas, B. J.; Loverde, P. T.; Wilson, R. A.; Dillon, G. P.; Cerqueira, G. C.; Mashiyama, S. T.; Al-Lazikani, B.; Andrade, L. F.; Ashton, P. D.; Aslett, M. A.; Bartholomeu, D. C.; Blandin, G.; Caffrey, C. R.; Coghlan, A.; Coulson, R.; Day, T. A.; Delcher, A.; Demarco, R.; Djikeng, A.; Eyre, T.; Gamble, J. A.; Ghedin, E.; Gu, Y.; Hertz-Fowler, C.; Hirai, H.; Hirai, Y.; Houston, R.; Ivens, A.; Johnston, D. A. (2009). "The genome of the blood fluke Schistosoma mansoni". Nature 460 (7253): 352–358. doi:10.1038/nature08160. PMC 2756445. PMID 19606141.  edit
  5. ^ "Killer parasites' genes decoded". BBC News. July 16, 2009. Retrieved 2009-07-16. 
  6. ^ Morgan JA, DeJong RJ, Kazibwe F, Mkoji GM, Loker ES (August 2003). "A newly-identified lineage of Schistosoma". Int. J. Parasitol. 33 (9): 977–85. doi:10.1016/S0020-7519(03)00132-2. PMID 12906881. 
  7. ^ Beer SA, Voronin MV, Zazornova OP, Khrisanfova GG, Semenova SK (2010) Phylogenetic relationships among schistosomatidae. Med Parazitol (Mosk) 2010 (2):53-59
  8. ^ Wang CR, Li L, Ni HB, et al. (February 2009). "Orientobilharzia turkestanicum is a member of Schistosoma genus based on phylogenetic analysis using ribosomal DNA sequences". Exp. Parasitol. 121 (2): 193–7. doi:10.1016/j.exppara.2008.10.012. PMID 19014940. 
  9. ^ Wang Y, Wang CR, Zhao GH, Gao JF, Li MW, Zhu XQ (December 2011). "The complete mitochondrial genome of Orientobilharzia turkestanicum supports its affinity with African Schistosoma spp". Infect. Genet. Evol. 11 (8): 1964–70. doi:10.1016/j.meegid.2011.08.030. PMID 21930247. 
  10. ^ a b Aldhoun JA, Littlewood DT (2012) Orientobilharzia Dutt & Srivastava, 1955 (Trematoda: Schistosomatidae), a junior synonym of Schistosoma Weinland, 1858. Syst Parasitol 82(2):81-8. doi: 10.1007/s11230-012-9349-8
  11. ^ Lawton SP, Majoros G (2013) A foreign invader or a reclusive native? DNA bar coding reveals a distinct European lineage of the zoonotic parasite Schistosoma turkestanicum (syn. Orientobilharzia turkestanicum). Infect Genet Evol 14:186-93. doi: 10.1016/j.meegid.2012.11.013
  12. ^ Kaukas A, Dias Neto E, Simpson AJ, Southgate VR, Rollinson D (1994) A phylogenetic analysis of Schistosoma haematobium group species based on randomly amplified polymorphic DNA. Int J Parasitol 24(2):285-290
  13. ^ Webster BL, Southgate VR, Littlewood DT (2006) A revision of the interrelationships of Schistosoma including the recently described Schistosoma guineensis. Int J Parasitol 36(8):947-955
  14. ^ Kane RA, Southgate VR, Rollinson D, Littlewood DT, Lockyer AE, Pagès JR, Tchuem Tchuentè LA, Jourdane J (2003) A phylogeny based on three mitochondrial genes supports the division of Schistosoma intercalatum into two separate species. Parasitology 127(Pt 2):131-137
  15. ^ Pagès JR, Durand P, Southgate VR, Tchuem Tchuenté LA, Jourdane J (2001) Molecular arguments for splitting of Schistosoma intercalatum, into two distinct species. Parasitol Res 87(1):57-62
  16. ^ Agatsuma T, Iwagami M, Liu CX, Rajapakse RP, Mondal MM, Kitikoon V, Ambu S, Agatsuma Y, Blair D, Higuchi T (2002) Affinities between Asian non-human Schistosoma species, the S. indicum group, and the African human schistosomes. J Helminthol 76(1):7-19
  17. ^ Webster BL, Littlewood DT (2012) Mitochondrial gene order change in Schistosoma (Platyhelminthes: Digenea: Schistosomatidae). Int J Parasitol 42(3):313-321
  18. ^ Brant, S. V.; Morgan, J. A. T.; Mkoji, G. M.; Snyder, S. D.; Rajapakse, R. P. V. J.; Loker, E. S. (2006). "An Approach to Revealing Blood Fluke Life Cycles, Taxonomy, and Diversity: Provision of Key Reference Data Including Dna Sequence from Single Life Cycle Stages". Journal of Parasitology 92 (1): 77–88. doi:10.1645/GE-3515.1. PMC 2519025. PMID 16629320.  edit
  19. ^ Britannica Concise Encyclopedia 2007
  20. ^ a b c d e Manson-Bahr, P.E.C.; Bell, D.R., eds. (1987). Manson's Tropical Diseases. London: Bailliere Tindall. ISBN 0-7020-1187-8. 
  21. ^ Young, N. D.; Jex, A. R.; Li, B.; Liu, S.; Yang, L.; Xiong, Z.; Li, Y.; Cantacessi, C.; Hall, R. S.; Xu, X.; Chen, F.; Wu, X.; Zerlotini, A.; Oliveira, G.; Hofmann, A.; Zhang, G.; Fang, X.; Kang, Y.; Campbell, B. E.; Loukas, A.; Ranganathan, S.; Rollinson, D.; Rinaldi, G.; Brindley, P. J.; Yang, H.; Wang, J.; Wang, J.; Gasser, R. B. (2012). "Whole-genome sequence of Schistosoma haematobium". Nature Genetics 44 (2): 221–225. doi:10.1038/ng.1065. PMID 22246508.  edit
  22. ^ Protasio, A. V.; Tsai, I. J.; Babbage, A.; Nichol, S.; Hunt, M.; Aslett, M. A.; De Silva, N.; Velarde, G. S.; Anderson, T. J. C.; Clark, R. C.; Davidson, C.; Dillon, G. P.; Holroyd, N. E.; Loverde, P. T.; Lloyd, C.; McQuillan, J.; Oliveira, G.; Otto, T. D.; Parker-Manuel, S. J.; Quail, M. A.; Wilson, R. A.; Zerlotini, A.; Dunne, D. W.; Berriman, M. (2012). "A Systematically Improved High Quality Genome and Transcriptome of the Human Blood Fluke Schistosoma mansoni". In Hoffmann, Karl F. PLoS Neglected Tropical Diseases 6 (1): e1455. doi:10.1371/journal.pntd.0001455. PMC 3254664. PMID 22253936.  edit

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