Molecular Epidemiology and Subtype Distributions of Blastocystis Sp. in Humans and Non-Human Primates

Authors

  • Longxian Zhang College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China
  • Luyang Wang College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China
  • Junqiang Li College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China

DOI:

https://doi.org/10.12974/2313-0946.2021.06.01.1

Keywords:

Blastocystis Sp, Epidemiology, Subtype, Zoonotic Potential, Humans, Non-Human Primates

Abstract

Blastocystis sp. is an intestinal protozoan that could infect human and many other non-human mammal hosts worldwide. It is estimated that there are currently more than one billion infections in humans, however the importance of public health is still remain controversy. In the recent years, various molecular epidemiological studies have been applied in the world to identify subtypes of Blastocystis sp., due to its remarkable genetic diversity. Blastocystis sp. isolates from humans and animals have been divided into 22 subtypes (STs) based on the phylogeny of small subunit rRNA genes (SSU rDNA). In this review, we investigated the molecular epidemiology and assessed the subtype distributions of Blastocystis sp. in humans and non-human primates (NHPs). These findings will update the epidemiology and subtype of Blastocystis sp., and it will help to understand the current subtypes and zoonotic potential of Blastocystis sp.

References

Nagel R, Cuttell L, Stensvold CR, Mills PC, Bielefeldt-Ohmann H, Traub RJ. Blastocystis subtypes in symptomatic and asymptomatic family members and pets and response to therapy. Intern Med J 2012; 42(11):1187-95. https://doi.org/10.1111/j.1445-5994.2011.02626.x

Bahrami F, Babaei E, Badirzadeh A, Riabi TR, Abdoli A. Blastocystis, urticaria, and skin disorders: review of the current evidences. Eur J Clin Microbiol 2020; 39(6):1027-42. https://doi.org/10.1007/s10096-019-03793-8

Stensvold CR, Tan KSW, Clark CG. Blastocystis. Trends Parasitol 2020; 36(3):315-6. https://doi.org/10.1016/j.pt.2019.12.008

Stensvold CR, van der Giezen M. Associations between Gut Microbiota and Common Luminal Intestinal Parasites. Trends Parasitol 2018; 34(5):369-77. https://doi.org/10.1016/j.pt.2018.02.004

Andersen LOB, Stensvold CR. Blastocystis in Health and Disease: Are We Moving from a Clinical to a Public Health Perspective? J Clin Microbiol 2016; 54(3):524-8. https://doi.org/10.1128/jcm.02520-15

Reh L, Muadica AS, Köster PC, Balasegaram S, Verlander NQ, Chércoles ER, et al. Substantial prevalence of enteroparasites spp., and sp. in asymptomatic schoolchildren in Madrid, Spain, November 2017 to June 2018. Euro Surveill 2019; 24(43):1900241. https://doi.org/10.2807/1560-7917.es.2019.24.43.1900241

Alexeieff A. Sur la nature des formations dites kystes de Trichomonas intestinalis. C R Soc Biol 1911; 71:296-8.

Pakandl M. Occurrence of Blastocystis sp. in pigs. Folia Parasitol (Praha) 1991; 38(4):297-301.

Pistono PG, Dusi MP, Ronchetto F, Cestonaro G, Guasco C. Blastocystis hominis in Canavese: a retrospective study of samples received for fecal parasitological examination at the Ivrea- Castellamonte Hospital over 42 months. G Batteriol Virol Immunol 1991; 84(1-12):67-76. https://doi.org/10.1007/978-3-642-85397-5_18

Rajah Salim H, Suresh Kumar G, Vellayan S, Mak JW, Khairul Anuar A, Init I, et al. Blastocystis in animal handlers. Parasitol Res 1999; 85(12):1032-3. https://doi.org/10.1007/s004360050677

Stensvold CR, Arendrup MC, Jespersgaard C, Molbak K, Nielsen HV. Detecting Blastocystis using parasitologic and DNA-based methods: a comparative study. Diagn Microbiol Infect Dis 2007; 59(3):303-7. https://doi.org/10.1016/j.diagmicrobio.2007.06.003

Stensvold CR, Traub RJ, von Samson-Himmelstjerna G, Jespersgaard C, Nielsen HV, Thompson RC. Blastocystis: subtyping isolates using pyrosequencing technology. Exp Parasitol 2007; 116(2):111-9. https://doi.org/10.1016/j.exppara.2006.12.002

Stensvold CR, Clark CG. Pre-empting Pandora's Box: Blastocystis Subtypes Revisited. Trends Parasitol 2020;36(3):229-32. https://doi.org/10.1016/j.pt.2019.12.009

Tan KS. New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 2008; 21(4):639-65. https://doi.org/10.1128/cmr.00022-08

Deng L, Wojciech L, Gascoigne NRJ, Peng G, Tan KSW. New insights into the interactions between Blastocystis, the gut microbiota, and host immunity. PLoS Pathog 2021; 17(2):e1009253. https://doi.org/10.1371/journal.ppat.1009253

Suli T, Kozoderovic G, Potkonjak A, Simin S, Simin V, Lalosevic V. Comparison of Conventional and Molecular Diagnostic Techniques for Detection of Blastocystis sp. in Pig Faeces. Iran J Parasitol 2018; 13(4):594-601.

Scicluna SM, Tawari B, Clark CG. DNA barcoding of Blastocystis. Protist 2006; 157(1):77-85. https://doi.org/10.1016/j.protis.2005.12.001

Dogruman-Al F, Yoshikawa H, Kustimur S, Balaban N. PCR-based subtyping of Blastocystis isolates from symptomatic and asymptomatic individuals in a major hospital in Ankara, Turkey. Parasitol Res 2009; 106(1):263-8. https://doi.org/10.1007/s00436-009-1658-8

Eroglu F, Koltas IS. Evaluation of the transmission mode of B. hominis by using PCR method. Parasitol Res 2010; 107(4):841-5. https://doi.org/10.1007/s00436-010-1937-4

Yoshikawa H, Iwamasa A. Human Blastocystis subtyping with subtype-specific primers developed from unique sequences of the SSU rRNA gene. Parasitol Int 2016; 65 (6):785-91. https://doi.org/10.1016/j.parint.2016.03.002

Maloney JG, da Cunha MJR, Molokin A, Cury MC, Santin M. Next-generation sequencing reveals wide genetic diversity of Blastocystis subtypes in chickens including potentially zoonotic subtypes. Parasitol Res 2021. https://doi.org/10.1007/s00436-021-07170-3.

Poirier P, Wawrzyniak I, Albert A, El Alaoui H, Delbac F, Livrelli V. Development and evaluation of a real-time PCR assay for detection and quantification of Blastocystis parasites in human stool samples: prospective study of patients with hematological malignancies. J Clin Microbiol 2011; 49(3):975-83. https://doi.org/10.1128/jcm.01392-10

Perea M, Vasquez V, Pineda V, Samudio F, Calzada JE, Saldana A. Prevalence and subtype distribution of Blastocystis sp. infecting children from a rural community in Panama. Parasite Epidemiol Control 2020; 9:e00139. https://doi.org/10.1016/j.parepi.2020.e00139

Rojas-Velazquez L, Moran P, Serrano-Vazquez A, Fernandez LD, Perez-Juarez H, Poot-Hernandez AC, et al. Genetic Diversity and Distribution of Blastocystis Subtype 3 in Human Populations, with Special Reference to a Rural Population in Central Mexico. Biomed Res Int 2018; 2018:3916263. https://doi.org/10.1155/2018/3916263

Whipps CM, Boorom K, Bermudez LE, Kent ML. Molecular characterization of Blastocystis species in Oregon identifies multiple subtypes. Parasitol Res 2010; 106(4):827-32. https://doi.org/10.1007/s00436-010-1739-8

Perez MR, Yanez CM, Hernandez AM, Sustaita JJD, Jimenez EG, Andrade MR, et al. Blastocystis infection frequency and subtype distribution in university students. Heliyon 2020; 6(12):e05729. https://doi.org/10.1016/j.heliyon.2020.e05729

Roberts T, Stark D, Harkness J, Ellis J. Subtype distribution of Blastocystis isolates identified in a Sydney population and pathogenic potential of Blastocystis. Eur J Clin Microbiol Infect Dis 2013; 32(3):335-43. https://doi.org/10.1007/s10096-012-1746-z

Roberts T, Barratt J, Harkness J, Ellis J, Stark D. Comparison of Microscopy, Culture, and Conventional Polymerase Chain Reaction for Detection of Blastocystis sp in Clinical Stool Samples. Am J Trop Med Hyg 2011; 84(2):308-12. https://doi.org/10.4269/ajtmh.2011.10-0447

Hanieh S, Mahanty S, Gurruwiwi G, Kearns T, Dhurrkay R, Gondarra V, et al. Enteric pathogen infection and consequences for child growth in young Aboriginal Australian children: a cross-sectional study. BMC Infect Dis 2021; 21(1):9. https://doi.org/10.1186/s12879-020-05685-1

Wang W, Owen H, Traub RJ, Cuttell L, Inpankaew T, Bielefeldt-Ohmann H. Molecular epidemiology of Blastocystis in pigs and their in-contact humans in Southeast Queensland, Australia, and Cambodia. Vet Parasitol 2014; 203(3-4):264-9. https://doi.org/10.1016/j.vetpar.2014.04.006

Nagel R, Cuttell L, Stensvold CR, Mills PC, Bielefeldt-Ohmann H, Traub RJ. Blastocystis subtypes in symptomatic and asymptomatic family members and pets and response to therapy. Intern Med J 2012; 42(11):1187-95. https://doi.org/10.1111/j.1445-5994.2011.02626.x

Ramirez JD, Sanchez A, Hernandez C, Florez C, Bernal MC, Giraldo JC, et al. Geographic distribution of human Blastocystis subtypes in South America. Infect Genet Evol 2016; 41:32-5. https://doi.org/10.1016/j.meegid.2016.03.017

Teng XJ, Chu HY, Zhai CC, Yu YF, Cai YC, Chen SH, et al. The epidemiological characteristics and influencing factors for Blastocystis hominis infection among human immunodeficiency virus seropositive individuals in Tengchong of Yunnan Province. Chin J Parasitol Parasit Dis 2018; 36(02):129-34.

Sulzyc-Bielicka V, Kolodziejczyk L, Adamska M, Skotarczak B, Jaczewska S, Safranow K, et al. Colorectal cancer and Blastocystis sp. infection. Parasit Vectors 2021;14(1):200. https://doi.org/10.1186/s13071-021-04681-x

Mulayim S, Aykur M, Dagci H, Dalkilic S, Aksoy A, Kaplan M. Investigation of Isolated Blastocystis Subtypes from Cancer Patients in Turkey. Acta Parasitol 2021. https://doi.org/10.1007/s11686-020-00322-y

Sanchez A, Munoz M, Gomez N, Tabares J, Segura L, Salazar A, et al. Molecular Epidemiology of Giardia, Blastocystis and Cryptosporidium among Indigenous Children from the Colombian Amazon Basin. Front Microbiol 2017; 8:248. https://doi.org/10.3389/fmicb.2017.00248

Oliveira-Arbex AP, David EB, Guimaraes S. Blastocystis genetic diversity among children of low-income daycare center in Southeastern Brazil. Infect Genet Evol 2018; 57:59-63. https://doi.org/10.1016/j.meegid.2017.11.005

Qi M, Wei Z, Zhang Y, Zhang Q, Li J, Zhang L, et al. Genetic diversity of Blastocystis in kindergarten children in southern Xinjiang, China. Parasit Vectors 2020; 13(1):15. https://doi.org/10.1186/s13071-020-3890-0

Srichaipon N, Nuchprayoon S, Charuchaibovorn S, Sukkapan P, Sanprasert V. A Simple Genotyping Method for Rapid Differentiation of Blastocystis Subtypes and Subtype Distribution of Blastocystis spp. in Thailand. Pathogens 2019; 8(1):38. https://doi.org/10.3390/pathogens8010038

Poulsen CS, Efunshile AM, Nelson JA, Stensvold CR. Epidemiological Aspects of Blastocystis Colonization in Children in Ilero, Nigeria. Am J Trop Med Hyg 2016; 95(1):175-9. https://doi.org/10.4269/ajtmh.16-0074

Ning CQ, Kang JM, Li YT, Chen HH, Chu YH, Yu YF, et al. Prevalence and risk factors of Blastocystis infections among primary school students in Jiangjin District, Chongqing City. Chin J Schi Contl 2020; 32(5):489-97. https://doi.org/10.1186/s12886-020-01410-3

Rudzinska M, Kowalewska B, Waz P, Sikorska K, Szostakowska B. Blastocystis subtypes isolated from travelers and non-travelers from the north of Poland - A single center study. Infect Genet Evol 2019; 75:103926. https://doi.org/10.1016/j.meegid.2019.103926

van Hattem JM, Arcilla MS, Schultsz C, Bootsma MC, Verhaar N, Rebers SP, et al. Carriage of Blastocystis spp. in travellers-A prospective longitudinal study. Travel Med Infect Dis 2019; 27:87-91. https://doi.org/10.1016/j.tmaid.2018.06.005

Piubelli C, Soleymanpoor H, Giorli G, Formenti F, Buonfrate D, Bisoffi Z, et al. Blastocystis prevalence and subtypes in autochthonous and immigrant patients in a referral centre for parasitic infections in Italy. PLoS One 2019; 14(1):e0210171. https://doi.org/10.1371/journal.pone.0210171

Li TC, Li Z, Zhan YL, Chen WJ, Dong XL, Yan JF, et al. Assessment of the subtypes and the zoonotic risk of Blastocystis sp. of experimental macaques in Yunnan province, southwestern China. Parasitol Res 2020; 119(2):741-8. https://doi.org/10.1007/s00436-019-06574-6

Zhao GH, Hu XF, Liu TL, Hu RS, Yu ZQ, Yang WB, et al. Molecular characterization of Blastocystis sp. in captive wild animals in Qinling Mountains. Parasitol Res 2018; 117(1):343-4. https://doi.org/10.1007/s00436-017-5692-7

Deng L, Yao J, Chen S, He T, Chai Y, Zhou Z, et al. First identification and molecular subtyping of Blastocystis sp. in zoo animals in southwestern China. Parasit Vectors 2021; 14(1):11. https://doi.org/10.1186/s13071-020-04515-2

Stensvold CR, Alfellani MA, Norskov-Lauritsen S, Prip K, Victory EL, Maddox C, et al. Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. Int J Parasitol 2009; 39(4):473-9. https://doi.org/10.1016/j.ijpara.2008.07.006

Oliveira-Arbex AP, David EB, Tenorio MD, Cicchi PJP, Patti M, Coradi ST, et al. Diversity of Blastocystis subtypes in wild mammals from a zoo and two conservation units in southeastern Brazil. Infect Genet Evol 2020; 78:10453. https://doi.org/10.1016/j.meegid.2019.104053

Helenbrook WD, Shields WM, Whipps CM. Characterization of Blastocystis species infection in humans and mantled howler monkeys, Alouatta palliata aequatorialis, living in close proximity to one another. Parasitol Res 2015; 114(7):2517-25. https://doi.org/10.1007/s00436-015-4451-x

Hublin JSY, Maloney JG, Santin M. Blastocystis in domesticated and wild mammals and birds. Res Vet Sci 2020; 135:260-82. https://doi.org/10.1016/j.rvsc.2020.09.031

Ma L, Qiao H, Wang H, Li S, Zhai P, Huang J, et al. Molecular prevalence and subtypes of Blastocystis sp. in primates in northern China. Transbound Emerg Dis 2020; 67(6):2789-96. https://doi.org/10.1111/tbed.13644

Stensvold CR. Comparison of sequencing (barcode region) and sequence-tagged-site PCR for Blastocystis subtyping. J Clin Microbiol 2013; 51(1):190-4. https://doi.org/10.1128/jcm.02541-12

Yoshikawa H, Tokoro M, Nagamoto T, Arayama S, Asih PBS, Rozi IE, et al. Molecular survey of Blastocystis sp from humans and associated animals in an Indonesian community with poor hygiene. Parasitol Int 2016; 65(6):780-4. https://doi.org/10.1016/j.parint.2016.03.010

Vielma JR. Blastocystosis: Epidemiological, clinical, pathogenic, diagnostic, and therapeutic aspects. Invest Clin 2019; 60(1):53-78. https://doi.org/10.22209/ic.v60n1a06

Skotarczak B. Genetic diversity and pathogenicity of Blastocystis. Ann Agric Environ Med 2018; 25(3):411-6. https://doi.org/10.26444/aaem/81315

Zanetti ADS, Malheiros AF, de Matos TA, Longhi FG, Moreira LM, Silva SL, et al. Prevalence of Blastocystis sp. infection in several hosts in Brazil: a systematic review and meta-analysis. Parasit Vectors 2020; 13(1):30. https://doi.org/10.1186/s13071-020-3900-2

Silberman JD, Sogin ML, Leipe DD, Clark CG. Human parasite finds taxonomic home. Nature 1996; 380(6573):398. https://doi.org/10.1038/380398a0

Clark CG, van der Giezen M, Alfellani MA, Stensvold CR. Recent developments in Blastocystis research. Adv Parasitol 2013; 82:1-32. https://doi.org/10.1016/b978-0-12-407706-5.00001-0

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Published

2022-06-15

How to Cite

Zhang, L., Wang, L., & Li, J. (2022). Molecular Epidemiology and Subtype Distributions of Blastocystis Sp. in Humans and Non-Human Primates. Global Journal Of Epidemiology and Public Health, 6, 1–37. https://doi.org/10.12974/2313-0946.2021.06.01.1

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