Natural and medical sciences

2017 Issue №4

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Hemozoin accumulation associated with Opisthorchis felineus infection and the analysis of its role in changing the bile ducts microbiota



Research works aimed at assessing the interaction in the host-parasite system, pay attention to the products of the vital activity of the parasite. Hemozoin is one of the most promising metabolites that can be used for new methods of parasite diagnostics and treatment. It is known that hemozoin is produced by parasites causing schistosomiasis and malaria. Recent research has shown that hemozoin is produced by the hepatic trematode Opisthorchis felineus, but the effects associated with the presence of hemozoin in the bile ducts of the host have not been studied yet. The authors compare the concentration of hemozoin in various organs of animals and study the ability of the O. felineus hemozoin to modify the bile ducts microbiota. The authors study the bile duct microbiota of infected and healthy animals and perform the metagenomics analysis. The microbiota is assessed by metagenomic analysis of bile duct samples of intact animals and animals with opisthorchiasis. Samples of mature forms of O. felineus are also included in the study. In accordance with the results obtained, hemozoin accumulates mainly in the liver during the invasion of O. felineus. The invasion of O. felineus leads to an increase in the alpha diversity of the bile duct microbiota in animals, and this effect is not associated with the presence of hemozoin in the bile ducts. Metagenomic analysis revealed that the most representative taxa in the mature forms of O. felineus are Sphingomonas, Prevotella, Methylobacterium.


1. Toh S. Q. et al. Heme and blood-feeding parasites: friends or foes? // Parasites & vectors. 2010. Vol. 3, № 1. P. 108.
2. Orjih A. U., Fitch C. D. Hemozoin production by Plasmodium falciparum: variation with strain and exposure to chloroquine // Biochimica et Biophysica Acta (BBA)-General Subjects. 1993. Vol. 1157, № 2. P. 270—274.
3. Chen M. M., Shi L., Sullivan D. J. Haemoproteus and Schistosoma synthesize heme polymers similar to Plasmodium hemozoin and β-hematin // Molecular and biochemical parasitology. 2001. Vol. 113, № 1. P. 1—8.
4. Oliveira M. F. et al. Structural and morphological characterization of hemozoin produced by Schistosoma mansoni and Rhodnius prolixus // Febs letters. 2005. Vol. 579, № 27. P. 6010—6016.
5. Sun J., Li C., Wang S. Organism-like formation of Schistosoma hemozoin and its function suggest a mechanism for anti-malarial action of artemisinin // Scientific reports. 2016. Vol. 6.
6. Lamikanra A. A. et al. Hemozoin (malarial pigment) directly promotes apoptosis of erythroid precursors // PloS one. 2009. Vol. 4, № 12. P. e8446. 
7. Deroost K. et al. Hemozoin induces hepatic inflammation in mice and is differentially associated with liver pathology depending on the Plasmodium strain // PloS one. 2014. Vol. 9, № 11. P. e113519.
8. Truscott M. et al. Schistosoma mansoni hemozoin modulates alternative activation of macrophages via specific suppression of Retnla expression and secretion // Infection and immunity. 2013. Vol. 81, № 1. P. 133—142.
9. Perkins D. J. et al. Severe malarial anemia: innate immunity and pathogenesis // International journal of biological sciences. 2011. Vol. 7, № 9. P. 1427. 
10. Awandare G. A. et al. Role of monocyte-acquired hemozoin in suppression of macrophage migration inhibitory factor in children with severe malarial anemia // Infection and immunity. 2007. Vol. 75, № 1. P. 201—210.
11. Pershina A. G. et al. Hemozoin “knobs” in Opisthorchis felineus infected liver // Parasites & vectors. 2015. Vol. 8, № 1. P. 459. 
12. Бычков В. Г., Крылов Г. Г., Плотников А. О. Описторхоз в Обь-Иртышском бассейне (вопросы этиологии и патогенеза) // Медицинская паразитология и паразитарные болезни. 2007. № 4. С. 1—6.
13. Ромашов Б. В. и др. Описторхоз в бассейне Верхнего Дона (Воронежская область). Воронеж, 2005.
14. Огородова Л. М. и др. Распространенность гельминтной инвазии Opisthorchis felineus у детей в Томске и Томской области // Вопросы современной педиатрии. 2011. Т. 10, № 3.
15. Fedorova O. S. et al. Opisthorchis felineus infection and cholangiocarcinoma in the Russian Federation: A review of medical statistics // Parasitology international. 2017. Vol. 66, № 4. P. 365—371.
16. Saltykova I. V. et al. Biliary Microbiota, Gallstone Disease and Infection with Opisthorchis felineus // PLoS neglected tropical diseases. 2016. Vol. 10, № 7. P. e0004809. 
17. Максимова Г. А. и др. Экспериментальная модель описторхоза на хомяках (Mesocricetus auratus) // Бюллетень сибирской медицины. 2012. Т. 11, № 6.
18. Deroost K. et al. Improved methods for haemozoin quantification in tissues yield organ-and parasite-specific information in malaria-infected mice // Malaria journal. 2012. Vol. 11, № 1. P. 166.
19. Caporaso J. G. et al. QIIME allows analysis of high-throughput community sequencing data // Nature methods. 2010. Vol. 7, № 5. P. 335—336.
20. DeSantis T. Z. et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB // Applied and environmental microbiology. 2006. Vol. 72, № 7. P. 5069—5072.
21. Paulson J. N. et al. Differential abundance analysis for microbial marker-gene surveys // Nature methods. 2013. Vol. 10, № 12. P. 1200—1202. 
22. Paulson J. N. et al. Differential abundance analysis for microbial marker-gene surveys // Nature methods. 2013. Vol. 10, № 12. P. 1200—1202. 
23. Berrilli F. et al. Interactions between parasites and microbial communities in the human gut // Frontiers in cellular and infection microbiology. 2012. Vol. 2. 
24. Gause W. C., Maizels R. M. Macrobiota—helminths as active participants and partners of the microbiota in host intestinal homeostasis // Current opinion in microbiology. 2016. Vol. 32. P. 14—18.
25. Mosca A., Leclerc M., Hugot J. P. Gut microbiota diversity and human diseases: should we reintroduce key predators in our ecosystem? // Frontiers in microbiology.2016. Vol. 7.
26. Katokhin A. V. et al. Assessment of the genetic distinctions of Opisthorchis felineus from O. viverrini and Clonorchis sinensis by ITS2 and CO1 sequences // Doklady Biochemistry and Biophysics. MAIK Nauka/Interperiodica, 2008. Vol. 421, № 1. P. 214—217.
27. Kaewpitoon N. et al. Opisthorchis viverrini: the carcinogenic human liver fluke // World journal of gastroenterology: WJG. 2008. Vol. 14, № 5. P. 666.
28. Chng K. R. et al. Tissue microbiome profiling identifies an enrichment of specific enteric bacteria in Opisthorchis viverrini associated cholangiocarcinoma // EBioMedicine. 2016. Vol. 8. P. 195—202.
29. Loke P., Lim Y. A. L. Helminths and the microbiota: parts of the hygiene hypothesis // Parasite immunology. 2015. Vol. 37, № 6. P. 314—323.