Abstract
Blastocystis sp. is the most common eukaryotic parasite in the intestinal tract of humans. Due to its potential impact in public health, we determined the Blastocystis sp. subtypes (STs) and their relative frequency in symptomatic patients living in or in the vicinity of two Italian cities (Rome and Sassari). A total of 34 Blastocystis sp. isolates corresponding to 26 single and 4 mixed infections were subtyped using partial small subunit ribosomal RNA gene sequencing. From this molecular approach, the ST distribution in the present Italian population was as follows: ST3 (47.1%), ST2 (20.6%), ST4 (17.7%), ST1 (8.8%), and ST7, and ST8 (2.9%). As in almost all countries worldwide, ST3 was the most common ST reinforcing the hypothesis of its human origin. Together with a previous preliminary report, a total of seven STs (with the addition of ST5) have been found in Italian symptomatic patients. The wide range of STs identified in the Italian population suggest that Blastocystis sp. infection is not associated with specific STs even if some STs (ST1–ST4) are predominant as reported in all other countries. Since most of the STs identified in Italian patients are zoonotic, our data raise crucial questions concerning the identification of animal reservoirs for Blastocystis sp. and the potential risks of transmission to humans.
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References
Abe N (2004) Molecular and phylogenetic analysis of Blastocystis isolates from various hosts. Vet Parasitol 120:235–242
Abe N, Nagoshi M, Takami K, Sawano Y, Yoshikawa H (2002) A survey of Blastocystis sp. in livestock, pets, and zoo animals in Japan. Vet Parasitol 106:203–212
Amin OM (2002) Seasonal prevalence of intestinal parasites in the United States during 2000. Am J Trop Med Hyg 66:799–803
Arisue N, Hashimoto T, Yoshikawa H, Nakamura Y, Nakamura G, Nakamura F, Yano TA, Hasegawa M (2002) Phylogenetic position of Blastocystis hominis and of stramenopiles inferred from multiple molecular sequence data. J Eukaryot Microbiol 49:42–53
Arisue N, Hashimoto T, Yoshikawa H (2003) Sequence heterogeneity of the small subunit ribosomal RNA genes among Blastocystis isolates. Parasitology 126:1–9
Böhm-Gloning B, Knobloch J, Walderich B (1997) Five subgroups of Blastocystis hominis isolates from symptomatic and asymptomatic patients revealed by restriction site analysis of PCR-amplified 16S-like rDNA. Trop Med Int Health 2:117–118
Boorom KF, Smith H, Nimri L, Viscogliosi E, Spanakos G, Parkar U, Li LH, Zhou XN, Ok UZ, Leelayoova S, Jones MS (2008) Oh my aching gut: irritable bowel syndrome, Blastocystis, and asymptomatic infection. BMC Parasit Vectors 1:40
Chen XQ, Singh M, Howe J, Ho LC, Tan SW, Yap EH (1999) In vitro encystation and excystation of Blastocystis ratti. Parasitology 118:151–160
Dogruman-Al F, Dragci H, Yoshikawa H, Kurt Ö, Demirel M (2008) A possible link between subtype 2 and asymptomatic infections of Blastocystis hominis. Parasitol Res 103:685–689
Dogruman-Al F, Kustimur S, Yoshikawa H, Tuncer C, Simsek Z, Tanyuksel M, Araz E, Boorom K (2009) Blastocystis subtypes in irritable bowel syndrome and inflammatory bowel disease in Ankara, Turkey. Mem Inst Oswaldo Cruz 104:724–727
Dogruman-Al F, Simsek Z, Boorom K, Ekici E, Sahin M, Tuncer C, Kustimur S, Altinbas A (2010) Comparison of methods for detection of Blastocystis infection in routinely submitted stool samples, and also in IBS/IBD Patients in Ankara, Turkey. PLoS ONE 5:e15484
Dominguez-Marquez MV, Guna R, Munoz C, Gomez-Munoz MT, Borras R (2009) High prevalence of subtype 4 among isolates of Blastocystis hominis from symptomatic patients of a health district of Valencia (Spain). Parasitol Res 105:949–955
Elwakil HS, Hewedi HI (2010) Pathogenic potential of Blastocystis hominis in laboratory mice. Parasitol Res 107:685–689
Eroglu F, Genc A, Elgun G, Koltas IS (2009) Identification of Blastocystis hominis isolates from asymptomatic and symptomatic patients by PCR. Parasitol Res 105:1589–1592
Hameed DM, Hassanin OM, Zuel-Fakkar NM (2010) Association of Blastocystis hominis genetic subtypes with urticaria. Parasitol Res. doi:10.1007/s00436-010-2097-2
Hussein EM, Hussein AM, Eida MM, Atwa MM (2008) Pathophysiological variability of different genotypes of human Blastocystis hominis egyptian isolates in experimentally infected rats. Parasitol Res 102:853–860
Jones MS, Whipps CM, Ganac RD, Hudson NR, Boroom K (2009) Association of Blastocystis subtype 3 and 1 with patients from an Oregon community presenting with chronic gastrointestinal illness. Parasitol Res 104:341–345
Katsarou-Katsari A, Vassalos CM, Tzanetou K, Spanakos G, Papadopoulou C, Vakalis N (2008) Acute urticaria associated with amoeboid forms of Blastocystis sp. subtype 3. Acta Derm Venereol 88:80–81
Leelayoova S, Siripattanapipong S, Thathaisong U, Naaglor T, Taamasri P, Piyaraj P, Mungthin M (2008) Drinking water: a possible source of Blastocystis spp. subtype 1 infection in schoolchildren of a rural community in central Thailand. Am J Trop Med Hyg 79:401–406
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 (2007) Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitol Int 56:281–286
Mattiucci S, De Rosa A, Gabrielli S, Iori A, Cancrini G (2010) Molecular identification of Blastocystis sp. subtypes from humans in Italy: preliminary results. Parassitologia 52:207
Moe KT, Singh M, Howe J, Ho LC, Tan SW, Chen XQ, Ng GC, Yap EH (1997) Experimental Blastocystis hominis infection in laboratory mice. Parasitol Res 83:319–325
Noël C, Dufernez F, Gerbod D, Edgcomb VP, Delgado-Viscogliosi P, Ho LC, Singh M, Wintjens R, Sogin ML, Capron M, Pierce R, Zenner L, Viscogliosi E (2005) Molecular phylogenies of Blastocystis isolates from different hosts: implications for genetic diversity, identification of species, and zoonosis. J Clin Microbiol 43:348–355
Östan I, Kilimcioglu AA, Girginkardesler N, Özyurt BC, Limoncu ME, Ok UZ (2007) Health inequities: lower socio-economic conditions and higher incidences of intestinal parasites. BMC Public Health 7:342
Özyurt M, Kurt O, Molbak K, Nielsen HV, Haznedaroglu T, Stensvold CR (2008) Molecular epidemiology of Blastocystis infections in Turkey. Parasitol Int 57:300–306
Parkar U, Traub RJ, Kumar S, Mungthin M, Vitali S, Leelayoova S, Morris K, Thompson RCA (2007) Direct characterization of Blastocystis from faeces by PCR and evidence of zoonotic potential. Parasitology 134:359–367
Parkar U, Traub RJ, Vitali S, Elliot A, Levecke B, Robertson I, Geurden T, Steele J, Drake B, Thompson RC (2010) Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Vet Parasitol 169:8–17
Puthia MK, Vaithilingam A, Lu J, Tan KS (2005) Degradation of human secretory immunoglobulin A by Blastocystis. Parasitol Res 97:386–389
Puthia MK, Sio SW, Lu J, Tan KS (2006) Blastocystis ratti induces contact-independent apoptosis, F-actin rearrangement, and barrier function disruption in IEC-6 cells. Infect Immun 74:4114–4223
Puthia MK, Lu J, Tan KS (2008) Blastocystis ratti contains cysteine proteases that mediate interleukin-8 response from human intestinal epithelial cells in an NF-kappaB-dependent manner. Eukaryot Cell 7:435–443
Santin M, Gomez-Munoz MT, Solano-Aguilar G, Fayer R (2011) Development of a new PCR protocol to detect and subtype Blastocystis spp. from humans and animals. Parasitol Res. doi:10.1007/s00436-010-2097-2
Scicluna SM, Tawari B, Clark CG (2006) DNA barcoding of Blastocystis. Protist 157:77–85
Silberman JD, Sogin ML, Leipe DD, Clark CG (1996) Human parasite finds taxonomic home. Nature 380:398
Souppart L, Sanciu G, Cian A, Wawrzyniak I, Delbac F, Capron M, Dei-Cas E, Boorom K, Delhaes L, Viscogliosi E (2009) Molecular epidemiology of human Blastocystis isolates in France. Parasitol Res 105:413–421
Souppart L, Moussa H, Cian A, Sanciu G, Poirier P, El Alaoui H, Delbac F, Boorom K, Delhaes L, Dei-Cas E, Viscogliosi E (2010) Subtype analysis of Blastocystis isolates from symptomatic patients in Egypt. Parasitol Res 106:505–511
Stensvold CR, Suresh GK, Tan KSW, Thompson RCA, Traub RJ, Viscogliosi E, Yoshikawa H, Clark CG (2007) Terminology for Blastocystis subtypes—a consensus. Trends Parasitol 23:93–96
Stensvold CR, Alfellani MA, Nørskov-Lauritsen S, Prip K, Victory EL, Maddox C, Nielsen HV, Clark CG (2009a) Subtype distribution of Blastocystis isolates from synanthropic and zoo animals and identification of a new subtype. Int J Parasitol 39:473–479
Stensvold CR, Nielsen HV, Mølbak K, Smith HV (2009b) Pursuing the clinical significance of Blastocystis—diagnostic limitations. Trends Parasitol 25:23–29
Stensvold CR, Lewis HC, Hammerum AM, Porsbo LJ, Nielsen SS, Olsen KE, Arendrup MC, Nielsen HV, Molbak K (2009c) Blastocystis: unravelling potential risk factors and clinical significance of a common but neglected parasite. Epidemiol Infect 137:1655–1663
Stenzel DJ, Boreham PFL (1996) Blastocystis hominis revisited. Clin Microbiol Rev 9:563–584
Su F-H, Chu F-Y, Li C-Y, Tang H-F, Lin Y-S, Peng Y-J, Su Y-M, Lee S-D (2009) Blastocystis hominis infection in long-term care facilities in Taiwan: prevalence and associated clinical factors. Parasitol Res 105:1007–1013
Suresh K, Ng GC, Ramachandran NP, Ho LC, Yap EH, Singh M (1993) In vitro encystment and experimental infections of Blastocystis hominis. Parasitol Res 79:456–460
Tai WP, Hu PJ, Wu J, Lin XC (2010) Six ulcerative colitis patients with refractory symptoms co-infective with Blastocystis hominis in China. Parasitol Res. doi:10.1007/s00436-010-2164-8
Tan KSW (2004) Blastocystis in humans and animals: new insights using modern methodologies. Vet Parasitol 126:121–144
Tan KSW (2008) New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 21:639–665
Tan TC, Suresh KG, Smith HV (2008) Phenotypic and genotypic characterization of Blastocystis hominis isolates implicates subtype 3 as a subtype with pathogenic potential. Parasitol Res 104:85–93
Tan TC, Ong SC, Suresh KG (2009) Genetic variability of Blastocystis sp. isolates obtained from cancer and HIV/AIDS patients. Parasitol Res 105:1283–1286
Thathaisong U, Worapong J, Mungthin M, Tan-Ariya P, Viputtigul K, Sudatis A, Noonai A, Leelayoova S (2003) Blastocystis isolates from a pig and a horse are closely related to Blastocystis hominis. J Clin Microbiol 41:967–975
Vogelberg C, Stensvold CR, Monecke S, Ditzen A, Stopsack K, Heinrich-Grafe U, Pohlmann C (2010) Blastocystis sp. subtype 2 detection during recurrence of gastrointestinal and urticarial symptoms. Parasitol Int 59:469–471
Whipps CM, Boorom K, Bermudez LE, Kent ML (2010) Molecular characterization of Blastocystis species in Oregon identifies multiple subtypes. Parasitol Res 106:827–832
Wong KHS, Ng GC, Lin RTP, Yoshikawa H, Taylor MB, Tan KSW (2008) Predominance of subtype 3 among Blastocystis isolates from a major hospital in Singapore. Parasitol Res 102:663–670
Yakoob J, Jafri W, Jafir N, Khan R, Islam M, AsimBeg M, Zaman V (2004) Irritable bowel syndrome: in search of an etiology: role of Blastocystis hominis. Am J Trop Med Hyg 70:383–385
Yakoob J, Jafri W, Beg MA, Abbas Z, Naz S, Islam M, Khan R (2010a) Irritable bowel syndrome: is it associated with genotypes of Blastocystis hominis. Parasitol Res 106:1033–1038
Yakoob J, Jafri W, Beg MA, Abbas Z, Naz S, Islam M, Khan R (2010b) Blastocystis hominis and Dientamoeba fragilis in patients fulfilling irritable bowel syndrome criteria. Parasitol Res 107:679–684
Yamamoto-Furusho JK, Torijano-Carrera E (2010) Intestinal protozoa infections among patients with ulcerative colitis: prevalence and impact on clinical disease course. Digestion 82:18–23
Yan Y, Su S, Ye J, Lai X, Lai R, Liao H, Chen G, Zhang R, Hou Z, Luo X (2007) Blastocystis sp. subtype 5: a possibly zoonotic genotype. Parasitol Res 101:1527–1532
Yoshikawa H, Abe N, Iwasawa M, Kitano S, Nagano I, Wu Z, Takahashi Y (2000) Genomic analysis of Blastocystis hominis strains isolated from two long-term health care facilities. J Clin Microbiol 38:1324–1330
Yoshikawa H, Yoshida K, Nakajima A, Yamanari K, Iwatani S, Kimata I (2004a) Fecal–oral transmission of the cyst form of Blastocystis hominis in rats. Parasitol Res 94:391–396
Yoshikawa H, Wu Z, Kimata I, Iseki M, Ali IKMD, Hossain MB, Zaman V, Haque R, Takahashi Y (2004b) Polymerase chain reaction-based genotype classification among human Blastocystis hominis populations isolated from different countries. Parasitol Res 92:22–29
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
Acknowledgments
This work was developed in the framework of the Center for Infection and Immunity of Lille and supported by the Institut Pasteur de Lille, the Institut National de la Santé et de la Recherche Médicale, the Centre National de la Recherche Scientifique, and the Université Lille Nord de France. DM and GS were supported by grants from the ERASMUS Program and Regione Autonoma della Sardegna.
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Meloni, D., Sanciu, G., Poirier, P. et al. Molecular subtyping of Blastocystis sp. isolates from symptomatic patients in Italy. Parasitol Res 109, 613–619 (2011). https://doi.org/10.1007/s00436-011-2294-7
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DOI: https://doi.org/10.1007/s00436-011-2294-7