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Assessment of the subtypes and the zoonotic risk of Blastocystis sp. of experimental macaques in Yunnan province, southwestern China

  • Genetics, Evolution, and Phylogeny - Short Communication
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Abstract

Blastocystis is an enteral eukaryote with an omnipresent existence in animals and humans globally. Animals have been proposed to be a major reservoir for the transmission of Blastocystis to individuals due to their high prevalence and large amount of zoonotic subtypes. However, limited data on Blastocystis infection in experimental macaques in China exists. The objective of the current study was to investigate the frequency and subtypes of Blastocystis infection in macaques in southwestern China. A total of 505 fecal samples were collected from experimental macaques in Yunnan province and were analyzed by nested PCR and phylogenetic analyses on the basis of small subunit rRNA (SSU rRNA) gene fragments. A total of 235 specimens were positive for Blastocystis sp., and the prevalence of Blastocystis sp. was 46.5% (235/505). Significant differences in prevalence were also observed among the various species of macaques (P < 0.0133, df = 2, χ2 = 8.64) and the different feed types (P < 0.0093, df = 1, χ2 = 6.77). Moreover, three zoonotic subtypes, ST1, ST3, and ST5, were identified by DNA sequence analysis. There were mainly single subtype infections with some mixed subtype infections, and the predominant subtype was ST3. The results suggested a high prevalence and diversified subtypes in macaques in Yunnan province, southwestern China. Macaques are likely to be potential reservoirs capable of zoonotic transmission of Blastocystis sp. to humans. To our knowledge, this study is the first large-scale systematic analysis of Blastocystis sp. colonization in Yunnan province in the subtropics of China; these results contribute to the in-depth study of genetic characteristics and the prevention, control, and treatment of Blastocystis sp. in macaques in Yunnan province and other regions.

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References

  • Alfellani MA, Jacob AS, Perea NO, Krecek RC, Taner-Mulla D, Verweij JJ, Levecke B, Tannich E, Clark CG, Stensvold CR (2013a) Diversity and distribution of Blastocystis sp. subtypes in non-human primates. Parasitology 140:966–971

    CAS  PubMed  Google Scholar 

  • Alfellani MA, Taner-Mulla D, Jacob AS, Imeede CA, Yoshikawa H, Stensvold CR, Clark CG (2013b) Genetic diversity of Blastocystis in livestock and zoo animals. Protist 164:497–509

    Article  CAS  Google Scholar 

  • Altshuler D, Pollara VJ, Cowles CR, Van Etten WJ, Baldwin J, Linton L, Lander ES (2000) An SNP map of the human genome generated by reduced representation shotgun sequencing. Nature 407:513–516

    CAS  PubMed  Google Scholar 

  • Badparva E, Sadraee J, Kheirandish F (2015) Genetic diversity of Blastocystis isolated from cattle in Khorramabad, Iran. Jundishapur J Microbiol 8:e14810

    PubMed  PubMed Central  Google Scholar 

  • Barbosa CV, Barreto MM, Andrade RJ, Sodre F, d’Avila-Levy CM, Peralta JM, Igreja RP, de Macedo HW, HLC S (2018) Intestinal parasite infections in a rural community of Rio de Janeiro (Brazil): prevalence and genetic diversity of Blastocystis subtypes. PLoS One 13:e0193860

    PubMed  PubMed Central  Google Scholar 

  • Bednarska M, Jankowska I, Pawelas A, Piwczynska K, Bajer A, Wolska-Kusnierz B, Wielopolska M, Welc-Faleciak R (2018) Prevalence of Cryptosporidium, Blastocystis, and other opportunistic infections in patients with primary and acquired immunodeficiency. Parasitol Res 117:2869–2879

    PubMed  PubMed Central  Google Scholar 

  • Beignon AS, Le Grand R, Chapon C (2014) In vivo imaging in NHP models of malaria: challenges, progress and outlooks. Parasitol Int 63:206–215

    PubMed  Google Scholar 

  • Betts EL, Gentekaki E, Thomasz A, Breakell V, Carpenter AI, Tsaousis AD (2018) Genetic diversity of Blastocystis in non-primate animals. Parasitology 145:1228–1234

    PubMed  PubMed Central  Google Scholar 

  • Bohm-Gloning B, Knobloch J, Walderich B (1997) Five subgroups of Blastocystis hominis from symptomatic and asymptomatic patients revealed by restriction site analysis of PCR-amplified 16S-like rDNA. Trop Med Int Health 2:771–778

    CAS  PubMed  Google Scholar 

  • Casero RD, Mongi F, Sanchez A, Ramirez JD (2015) Blastocystis and urticaria: examination of subtypes and morphotypes in an unusual clinical manifestation. Acta Trop 148:156–161

    PubMed  Google Scholar 

  • Cian A, El Safadi D, Osman M, Moriniere R, Gantois N, Benamrouz-Vanneste S, Delgado-Viscogliosi P, Guyot K, Li LL, Monchy S, Noel C, Poirier P, Nourrisson C, Wawrzyniak I, Delbac F, Bosc S, Chabe M, Petit T, Certad G, Viscogliosi E (2017) Molecular epidemiology of Blastocystis sp in various animal groups from two French zoos and evaluation of potential zoonotic risk. PLoS One 12:e0169659

    PubMed  PubMed Central  Google Scholar 

  • Drakulovski P, Bertout S, Locatelli S, Butel C, Pion S, Mpoudi-Ngole E, Delaporte E, Peeters M, Mallie M (2014) Assessment of gastrointestinal parasites in wild chimpanzees (Pan troglodytes troglodytes) in southeast Cameroon. Parasitol Res 113:2541–2550

    PubMed  PubMed Central  Google Scholar 

  • Dudlova A, Jarcuska P, Jurisova S, Vasilkova Z, Krcmery V, Juris P (2018) Prevalence of non-pathogenic types of gastrointestinal protozoa in population in Slovakia and their potential importance in the aspect of public health. Acta Parasitol 63:819–825

    PubMed  Google Scholar 

  • Farah IO, Kariuki TM, King CL, Hau J (2001) An overview of animal models in experimental schistosomiasis and refinements in the use of non-human primates. Lab Anim-Uk 35:205–212

    CAS  Google Scholar 

  • Friesen J, Fuhrmann J, Kietzmann H, Tannich E, Muller M, Ignatius R (2018) Evaluation of the Roche LightMix gastro parasites multiplex PCR assay detecting Giardia duodenalis, Entamoeba histolytica, cryptosporidia, Dientamoeba fragilis, and Blastocystis hominis. Clin Microbiol Infec 24:1333–1337

    CAS  PubMed  Google Scholar 

  • Gazzonis AL, Marangi M, Zanzani SA, Villa L, Giangaspero A, Manfredi MT (2019) Molecular epidemiology of Blastocystis sp. in dogs housed in Italian rescue shelters. Parasitol Res 118:3011–3017

    PubMed  Google Scholar 

  • Greige S, El Safadi D, Becu N, Gantois N, Pereira B, Chabe M, Benamrouz-Vanneste S, Certad G, El Hage R, Chemaly M, Hamze M, Viscogliosi E (2018) Prevalence and subtype distribution of Blastocystis sp. isolates from poultry in Lebanon and evidence of zoonotic potential. Parasit Vectors 11:389

    PubMed  PubMed Central  Google Scholar 

  • Greige S, El Safadi D, Khaled S, Gantois N, Baydoun M, Chemaly M, Benamrouz-Vanneste S, Chabe M, Osman M, Certad G, Hamze M, Viscogliosi E (2019) First report on the prevalence and subtype distribution of Blastocystis sp. in dairy cattle in Lebanon and assessment of zoonotic transmission. Acta Trop 194:23–29

    PubMed  Google Scholar 

  • Hallinger MJ, Taubert A, Hermosilla C, Mutschmann F (2018) Occurrence of health-compromising protozoan and helminth infections in tortoises kept as pet animals in Germany. Parasit Vectors 11:352

  • Helenbrook WD, Shields WM, Whipps CM (2015) Characterization of Blastocystis species infection in humans and mantled howler monkeys, Alouatta palliata aequatorialis, living in close proximity to one another. Parasitol Res 114:2517–2525

    PubMed  Google Scholar 

  • Javanmard E, Niyyati M, Ghasemi E, Mirjalali H, Asadzadeh Aghdaei H, Zali MR (2018) Impacts of human development index and climate conditions on prevalence of Blastocystis: a systematic review and meta-analysis. Acta Trop 185:193–203

    PubMed  Google Scholar 

  • Katsumata M, Yoshikawa H, Tokoro M, Mizuno T, Nagamoto T, Hendarto J, Asih PBS, Rozi IE, Kimata I, Takami K, Syafruddin D (2018) Molecular phylogeny of Blastocystis isolates from wild rodents captured in Indonesia and Japan. Parasitol Res 117:2841–2846

    PubMed  Google Scholar 

  • Koltas IS, Eroglu F (2016) Subtype analysis of Blastocystis isolates using SSU rRNA-DNA sequencing in rural and urban population in southern Turkey. Exp Parasitol 170:247–251

    CAS  PubMed  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33:1870–1874

    CAS  Google Scholar 

  • Lee H, Lee SH, Seo MG, Kim HY, Kim JW, Lee YR, Kim JH, Kwon OD, Kwak D (2018) Occurrence and genetic diversity of Blastocystis in Korean cattle. Vet Parasitol 258:70–73

    CAS  PubMed  Google Scholar 

  • Legesse M, Erko B (2004) Zoonotic intestinal parasites in Papio anubis (baboon) and Cercopithecus aethiops (vervet) from four localities in Ethiopia. Acta Trop 90:231–236

    PubMed  Google Scholar 

  • Li LH, Zhang XP, Lv S, Zhang L, Yoshikawa H, Wu Z, Steinmann P, Utzinger J, Tong XM, Chen SH, Zhou XN (2007a) Cross-sectional surveys and subtype classification of human Blastocystis isolates from four epidemiological settings in China. Parasitol Res 102:83–90

    PubMed  Google Scholar 

  • Li LH, Zhou XN, Du ZW, Wang XZ, Wang LB, Jiang JY, Yoshikawa H, Steinmann P, Utzinger J, Wu Z, Chen JX, Chen SH, Zhang L (2007b) Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitol Int 56:281–286

    CAS  PubMed  Google Scholar 

  • Maloney JG, Lombard JE, Urie NJ, Shivley CB, Santin M (2019) Zoonotic and genetically diverse subtypes of Blastocystis in US pre-weaned dairy heifer calves. Parasitol Res 118:575–582

    PubMed  Google Scholar 

  • Manganelli L, Berrilli F, Di Cave D, Ercoli L, Capelli G, Otranto D, Giangaspero A (2012) Intestinal parasite infections in immigrant children in the city of Rome, related risk factors and possible impact on nutritional status. Parasit Vectors 5:265

    PubMed  PubMed Central  Google Scholar 

  • Masuda A, Sumiyoshi T, Ohtaki T, Matsumoto J (2018) Prevalence and molecular subtyping of Blastocystis from dairy cattle in Kanagawa, Japan. Parasitol Int 67:702–705

    CAS  PubMed  Google Scholar 

  • Paulos S, Koster PC, de Lucio A, Hernandez-de-Mingo M, Cardona GA, Fernandez-Crespo JC, Stensvold CR, Carmena D (2018) Occurrence and subtype distribution of Blastocystis sp in humans, dogs and cats sharing household in northern Spain and assessment of zoonotic transmission risk. Zoonoses Public Health 65:993–1002

    CAS  PubMed  Google Scholar 

  • Petrasova J, Uzlikova M, Kostka M, Petrzelkova KJ, Huffman MA, Modry D (2011) Diversity and host specificity of Blastocystis in syntopic primates on Rubondo Island, Tanzania. Int J Parasitol 41:1113–1120

    CAS  PubMed  Google Scholar 

  • Pintong AR, Sunyanusin S, Prasertbun R, Mahittikorn A, Mori H, Changbunjong T, Komalamisra C, Sukthana Y, Popruk S (2018) Blastocystis subtype 5: predominant subtype on pig farms, Thailand. Parasitol Int 67:824–828

    CAS  PubMed  Google Scholar 

  • Scanlan PD (2012) Blastocystis: past pitfalls and future perspectives. Trends Parasitol 28:327–334

    PubMed  Google Scholar 

  • Shariati A, Fallah F, Pormohammad A, Taghipour A, Safari H, Chirani AS, Sabour S, Alizadeh-Sani M, Azimi T (2019) The possible role of bacteria, viruses, and parasites in initiation and exacerbation of irritable bowel syndrome. J Cell Physiol 234:8550–8569

    CAS  PubMed  Google Scholar 

  • Skotarczak B (2018) Genetic diversity and pathogenicity of Blastocystis. Ann Agric Environ Med 25:411–416

    PubMed  Google Scholar 

  • Song JK, Yin YL, Yuan YJ, Tang H, Ren GJ, Zhang HJ, Li ZX, Zhang YM, Zhao GH (2017) First genotyping of Blastocystis sp. in dairy, meat, and cashmere goats in northwestern China. Acta Trop 176:277–282

    PubMed  Google Scholar 

  • Stensvold CR, Alfellani M, Clark CG (2012) Levels of genetic diversity vary dramatically between Blastocystis subtypes. Infect Genet Evol 12:263–273

    PubMed  Google Scholar 

  • Stensvold CR, Alfellani MA, Norskov-Lauritsen S, Prip K, Victory EL, Maddox C, Nielsen HV, Clark CG (2009) Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. Int J Parasitol 39:473–479

    CAS  Google Scholar 

  • Stensvold CR, van der Giezen M (2018) Associations between gut microbiota and common luminal intestinal parasites. Trends Parasitol 34:369–377

    CAS  Google Scholar 

  • Stenzel DJ, Boreham PF (1996) Blastocystis hominis revisited. Clin Microbiol Rev 9:563–584

    CAS  PubMed  PubMed Central  Google Scholar 

  • Teichroeb JA, Kutz SJ, Parkar U, Thompson RCA, Sicotte P (2009) Ecology of the gastrointestinal parasites of Colobus vellerosus at Boabeng-Fiema, Ghana: possible Anthropozoonotic transmission. Am J Phys Anthropol 140:498–507

    PubMed  Google Scholar 

  • Udonsom R, Prasertbun R, Mahittikorna A, Mori H, Changbunjong T, Komalamisra C, Pintong AR, Sukthana Y, Popruk S (2018) Blastocystis infection and subtype distribution in humans, cattle, goats, and pigs in Central and Western Thailand. Infect Genet Evol 65:107–111

    PubMed  Google Scholar 

  • Vaisusuk K, Saijuntha W, Sedlak S, Thanchomnang T, Pilap W, Suksavate W, Stensvold CR, Tantrawatpan C (2018) Blastocystis subtypes detected in long-tailed macaques in Thailand-further evidence of cryptic host specificity. Acta Trop 184:78–82

    PubMed  Google Scholar 

  • Villanueva-Garcia C, Gordillo-Chavez EJ, Lopez-Escamilla E, Rendon-Franco E, Munoz-Garcia CI, Gama L, Martinez-Flores WA, Gonzalez-Rodriguez N, Romero-Valdovinos M, Diaz-Lopez H, Galian J, Villalobos G, Maravilla P, Martinez-Hernandez F (2017) Clarifying the cryptic host specificity of Blastocystis spp. isolates from Alouatta palliata and A. pigra howler monkeys. PLoS One 12:e0169637

    PubMed  PubMed Central  Google Scholar 

  • Wang W, Cuttell L, Bielefeldt-Ohmann H, Inpankaew T, Owen H, Traub RJ (2013) Diversity of Blastocystis subtypes in dogs in different geographical settings. Parasit Vectors 6:215

    PubMed  PubMed Central  Google Scholar 

  • Yoshikawa H, Iwamasa A (2016) Human Blastocystis subtyping with subtype-specific primers developed from unique sequences of the SSU rRNA gene. Parasitol Int 65:785–791

    CAS  PubMed  Google Scholar 

  • Yoshikawa H, Wu Z, Pandey K, Pandey BD, Sherchand JB, Yanagi T, Kanbara H (2009) Molecular characterization of Blastocystis isolates from children and rhesus monkeys in Kathmandu, Nepal. Vet Parasitol 160:295–300

    CAS  Google Scholar 

  • Zanzani SA, Gazzonis AL, Epis S, Manfredi MT (2016) Study of the gastrointestinal parasitic fauna of captive non-human primates (Macaca fascicularis). Parasitol Res 115:307–312

    PubMed  Google Scholar 

  • Zhao GH, Hu XF, Liu TL, Hu RS, Yu ZQ, Yang WB, Wu YL, Yu SK, Song JK (2017) Molecular characterization of Blastocystis sp. in captive wild animals in Qinling Mountains. Parasitol Res 116:2327–2333

    CAS  Google Scholar 

  • Zierdt CH (1991) Blastocystis hominis - past and future. Clin Microbiol Rev 4:61–79

    CAS  PubMed  PubMed Central  Google Scholar 

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Funding

Project support was provided by the Open Funds of the State Key Laboratory of Veterinary Etiological Biology (Grant No. SKLVEB2017KFKT008) and the Promotion Project of ESI Discipline of Yunnan Agricultural University (Grant No. 2019YNAUESIMS03).

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Correspondence to Feng-Cai Zou.

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The study protocol was approved by the Kunming Primate Research Center of the Chinese Academy of Sciences as well as the Research Ethics Committee of Yunnan Agricultural University, before the study. Fecal samples were collected from macaques in accordance with the Animal Ethics Procedures and Guidelines of the People’s Republic of China.

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The authors declare that they have no competing interests.

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Section Editor: Yaoyu Feng

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Li, TC., Li, Z., Zhang, YL. et al. Assessment of the subtypes and the zoonotic risk of Blastocystis sp. of experimental macaques in Yunnan province, southwestern China. Parasitol Res 119, 741–748 (2020). https://doi.org/10.1007/s00436-019-06574-6

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  • DOI: https://doi.org/10.1007/s00436-019-06574-6

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