ISSN: 2008-2258
Vol 15, No 2 (2022): Spring
High occurrence of Blastocystis subtype 3 in individuals referred to medical laboratories in Kermanshah, West of Iran
Gastroenterology and Hepatology from Bed to Bench,
,
https://doi.org/10.22037/ghfbb.vi.2403
Abstract
Aim: The purpose of this study was to investigate the prevalence and identification of different subtypes of Blastocystis in individuals referred to medical laboratories in Kermanshah, West of Iran.
Background: Blastocystis is a common intestinal anaerobic unicellular eukaryote parasite that was found in human and a wide range of animals. Nowadays, it has been suggested that some Blastocystis subtypes are involved in the development of gastrointestinal disorders.
Methods: A total 950 stool samples were surveyed by using standard formalin-ether concentration technique. All specimens were cultured in Robinson xenic medium. Then, DNA extraction and PCR amplification of subtype specific sequence-tagged site (STS) was conducted.
Results: Of the 950 samples tested by microscopic survey, 86 (9.05%) samples were infected with Blastocystis. 33 samples (38%) of microscopic positive cases were grown in culture medium and all of them were confirmed by conventional PCR. In this regard, six subtypes of Blastocystis consisted (ST1, ST2, ST3, ST5, ST6 and ST7) were identified. Among them, Blastocystis ST3 (45.0%) was the predominant subtype, followed by ST1 (15.15%) and ST2 (12%).
Conclusion: The present study indicated ST3 subtype was the most prevalent subtype among the positive samples. Finally, the identification of subtype distribution can help to improve understanding of the risk factors.
Keywords:
- Blastocystis, Prevalence, Subtype, Kermanshah, West of Iran.
References
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9. Udkow MP, Markell EK. Blastocystis hominis: prevalence in asymptomatic versus symptomatic hosts. J Infect Dis 1993;168(1):242-4.
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27. 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.
28. Stensvold CR. Laboratory diagnosis of Blastocystis spp. Trop Parasitol 2015;5(1):3.
29. Verweij JJ, Stensvold CR. Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clin microbiol Rev 2014;27(2):371-418.
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32. Riabi TR, Mirjalali H, Haghighi A, Nejad MR, Pourhoseingholi MA, Poirier P, et al. Genetic diversity analysis of Blastocystis subtypes from both symptomatic and asymptomatic subjects using a barcoding region from the 18S rRNA gene. Infect Genet Evol 2018;61:119-26.
33. Shahbazi A, Fallah E, Heydarian P, Ghazanchaei A, Khanmohammadi M, Mirsamdi N. PCR-based subtyping of blastocystis isolates from symptomatic and asymptomatic patients in North-West of Iran. J Pure Appl Microbiol 2013;7(4):2957-63.
34. Badparva E, Sadraee J, Kheirandish F, Frouzandeh M. Genetic diversity of human blastocystis isolates in khorramabad, central iran. Iran J Parasitol 2014;9(1):44.
35. 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.
36. Popruk S, Udonsom R, Koompapong K, Mahittikorn A, Kusolsuk T, Ruangsittichai J, et al. Subtype distribution of Blastocystis in Thai-Myanmar border, Thailand. Korean J Parasitol 2015;53(1):13.
37. Zulfa F, Sari IP, Kurniawan A, editors. Association of Blastocystis subtypes with diarrhea in children. J Physics: Conference Series; 2017; IOP Publishing Ltd.
38. Meloni D, Sanciu G, Poirier P, El Alaoui H, Chabé M, Delhaes L, et al. Molecular subtyping of Blastocystis sp. isolates from symptomatic patients in Italy. Parasitol Res 2011;109(3):613-9.
39. Li L-H, Zhou X-N, Du Z-W, Wang X-Z, Wang L-B, Jiang J-Y, et al. Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitol Int 2007;56(4):281-6.
40. 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.
41. Souppart L, Moussa H, Cian A, Sanciu G, Poirier P, El Alaoui H, et al. Subtype analysis of Blastocystis isolates from symptomatic patients in Egypt. Parasitol Res 2010;106(2):505-11.
42. Santín M, Gómez-Muñoz MT, Solano-Aguilar G, Fayer R. Development of a new PCR protocol to detect and subtype Blastocystis spp. from humans and animals. Parasitol Res 2011;109(1):205-12.
43. Alfellani MA, Jacob AS, Perea NO, Krecek RC, Taner-Mulla D, Verweij JJ, et al. Diversity and distribution of Blastocystis sp. subtypes in non-human primates. Parasitol 2013;140(8):966-71.
44. Jantermtor S, Pinlaor P, Sawadpanich K, Pinlaor S, Sangka A, Wilailuckana C, et al. Subtype identification of Blastocystis spp. isolated from patients in a major hospital in northeastern Thailand. Parasitol Res. 2013;112(4):1781-6.
45. Khademvatan S, Masjedizadeh R, Rahim F, Mahbodfar H, Salehi R, Yousefi-Razin E, et al. Blastocystis and irritable bowel syndrome: Frequency and subtypes from Iranian patients. Parasitol Int 2017;66(2):142-5.
46. Özyurt M, Kurt Ö, Mølbak K, Nielsen HV, Haznedaroglu T, Stensvold CR. Molecular epidemiology of Blastocystis infections in Turkey. Parasitol Int 2008;57(3):300-6.
47. El Safadi D, Gaayeb L, Meloni D, Cian A, Poirier P, Wawrzyniak I, et al. Children of Senegal River Basin show the highest prevalence of Blastocystissp. ever observed worldwide. BMC Infect Dis 2014;14(1):164.
48. Ramírez JD, Sánchez LV, Bautista DC, Corredor AF, Flórez AC, Stensvold CR. Blastocystis subtypes detected in humans and animals from Colombia. Infect Genet Evol 2014;22:223-8.
49. Rivera WL. Phylogenetic analysis of Blastocystis isolates from animal and human hosts in the Philippines. Vet Parasitol 2008;156(3-4):178-82.
50. Clark CG, van der Giezen M, Alfellani MA, Stensvold CR. Recent developments in Blastocystis research. Advances in parasitology. 82: Elsevier; 2013. p. 1-32.
51. Stensvold CR, Clark CG. Current status of Blastocystis: a personal view. Parasitol Int 2016;65(6):763-71.
52. Oliveira-Arbex AP, David ÉB, Guimarães S. Blastocystis genetic diversity among children of low-income daycare center in Southeastern Brazil. Infect Genet Evol 2018;57:59-63.
53. Jalallou N, Iravani S, Rezaeian M, Alinaghizade A, Mirjalali H. Subtypes distribution and frequency of Blastocystis sp. isolated from diarrheic and non-diarrheic patients. Iran J Parasitol 2017;12(1):63.
54. Alinaghizade A, Mirjalali H, Mohebali M, Stensvold CR, Rezaeian M. Inter-and intra-subtype variation of Blastocystis subtypes isolated from diarrheic and non-diarrheic patients in Iran. Infect Genet Evol 2017;50:77-82.
55. Ramírez JD, Sánchez A, Hernández C, Flórez C, Bernal MC, Giraldo JC, et al. Geographic distribution of human Blastocystis subtypes in South America. Infect Genet Evol 2016;41:32-5.
56. Yıldız S, Doğan İ, Doğruman Al F, Nalbantoğlu U, Üstek D, Sarzhanov F, et al. Association of enteric protist Blastocystis spp. and gut microbiota with hepatic encephalopathy. 2016.
57. Muadica AS, Köster PC, Dashti A, Bailo B, Hernández-de-Mingo M, Reh L, et al. Molecular diversity of Giardia duodenalis, Cryptosporidium spp. and Blastocystis sp. in asymptomatic school children in Leganés, Madrid (Spain). Microorganisms 2020;8(4):466.
58. Sharifi Y, Abbasi F, Shahabi S, Zaraei A, Mikaeili F, Sarkari B. Comparative genotyping of Blastocystis infecting cattle and human in the south of Iran. Comp Immunol Microbiol Infect Dis 2020;72:101529.
59. Khoshnood S, Rafiei A, Saki J, Alizadeh K. Prevalence and genotype characterization of Blastocystis hominis among the baghmalek people in southwestern Iran in 2013-2014. Jundishapur j Microbiol 2015;8(10).
60. Piranshahi AR, Tavalla M, Khademvatan S. Genomic analysis of Blastocystis hominis isolates in patients with HIV-positive using locus SSU-rDNA. J Parasit Dis 2018;42(1):28-33.
61. Koltas IS, Eroglu F. Subtype analysis of Blastocystis isolates using SSU rRNA-DNA sequencing in rural and urban population in southern Turkey. Exp Parasitol 2016;170:247-51.
62. Sanpool O, Laymanivong S, Thanchomnang T, Rodpai R, Sadaow L, Phosuk I, et al. Subtype identification of human Blastocystis spp. isolated from Lao People’s Democratic Republic. Acta trop 2017;168:37-40.
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2. Yoshikawa H, Tokoro M, Nagamoto T, Arayama S, Asih PB, 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.
3. Fathy FM. A study on Blastocystis hominis in food-handlers: diagnosis and potential pathogenicity. J Egypt Soc Parasitol 2011;41(2):433-53.
4. Yoshikawa H, Wu Z, Pandey K, Pandey BD, Sherchand JB, Yanagi T, et al. Molecular characterization of Blastocystis isolates from children and rhesus monkeys in Kathmandu, Nepal. Vet Parasitol 2009;160(3-4):295-300.
5. Tan KS. New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev 2008;21(4):639-65.
6. Alfellani MA, Stensvold CR, Vidal-Lapiedra A, Onuoha ESU, Fagbenro-Beyioku AF, Clark CG. Variable geographic distribution of Blastocystis subtypes and its potential implications. Acta Trop 2013;126(1):11-8.
7. Tan KS, Mirza H, Teo JD, Wu B, MacAry PA. Current views on the clinical relevance of Blastocystis spp. Curr Infect Dis Rep 2010;12(1):28-35.
8. Sun T, Katz S, Tanenbaum B, Schenone C. Questionable clinical significance of Blastocystis hominis infection. Am J Gastroenterol 1989;84(12).
9. Udkow MP, Markell EK. Blastocystis hominis: prevalence in asymptomatic versus symptomatic hosts. J Infect Dis 1993;168(1):242-4.
10. Kolkhir P, Balakirski G, Merk HF, Olisova O, Maurer M. Chronic spontaneous urticaria and internal parasites–a systematic review. Allergy 2016;71(3):308-22.
11. El Deeb HK, Salah-Eldin H, Khodeer S. Blastocystis hominis as a contributing risk factor for development of iron deficiency anemia in pregnant women. Parasitol Res 2012;110(6):2167-74.
12. Jimenez-Gonzalez DE, Martinez-Flores WA, Reyes-Gordillo J, Ramirez-Miranda ME, Arroyo-Escalante S, Romero-Valdovinos M, et al. Blastocystis infection is associated with irritable bowel syndrome in a Mexican patient population. Parasitol Res 2012;110(3):1269-75.
13. Rostami A, Riahi SM, Haghighi A, Saber V, Armon B, Seyyedtabaei SJ. The role of Blastocystis sp. and Dientamoeba fragilis in irritable bowel syndrome: a systematic review and meta-analysis. Parasitol Res 2017;116(9):2361-71.
14. 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.
15. Stensvold CR, Arendrup MC, Jespersgaard C, Mølbak K, Nielsen HV. Detecting Blastocystis using parasitologic and DNA-based methods: a comparative study. Diagn Microbiol Infect Dis 2007;59(3):303-7.
16. Termmathurapoj S, Leelayoova S, Aimpun P, Thathaisong U, Nimmanon T, Taamasri P, et al. The usefulness of short-term in vitro cultivation for the detection and molecular study of Blastocystis hominis in stool specimens. Parasitol Res 2004;93(6):445-7.
17. Alfellani MA, Taner-Mulla D, Jacob AS, Imeede CA, Yoshikawa H, Stensvold CR, et al. Genetic diversity of Blastocystis in livestock and zoo animals. Protist 2013;164(4):497-509.
18. Stensvold CR, Clark CG. Molecular identification and subtype analysis of Blastocystis. Curr Protoc Microbiol 2016;43(1):20A. 2.1-A. 2.10.
19. Jiménez PA, Jaimes JE, Ramírez JD. A summary of Blastocystis subtypes in North and South America. Parasites & vectors 2019;12(1):376.
20. Scanlan PD. Blastocystis: past pitfalls and future perspectives. Trends in Parasitol 2012;28(8):327-34.
21. Moosavi A, Haghighi A, Mojarad EN, Zayeri F, Alebouyeh M, Khazan H, et al. Genetic variability of Blastocystis sp. isolated from symptomatic and asymptomatic individuals in Iran. Parasitol Res 2012;111(6):2311-5.
22. Badparva E, Sadraee J, Kheirandish F. Genetic diversity of Blastocystis isolated from cattle in Khorramabad, Iran. Jundishapur J Microbiol 2015;8(3).
23. Maleki B, SEYYED TSJ, Tahvildar F, Khorshidi A. Soil contamination of public places with Toxocara spp. egg in Kermanshah, Iran. NBM;2016.
24. Robinson G. The laboratory diagnosis of human parasitic amoebae. Trans R Soc Trop Med Hyg 1968;62(2):285-94.
25. Shargh EK, Pirestani M, Sadraei J. In vitro toxicity evaluation of short cationic antimicrobial peptide (CM11) on Blastocystis sp. Acta Trop 2020;204:105384.
26. Yoshikawa H, Wu Z, Kimata I, Iseki M, Ali IKM, Hossain MB, et al. Polymerase chain reaction-based genotype classification among human Blastocystis hominis populations isolated from different countries. Parasitol Res 2004;92(1):22-9.
27. 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.
28. Stensvold CR. Laboratory diagnosis of Blastocystis spp. Trop Parasitol 2015;5(1):3.
29. Verweij JJ, Stensvold CR. Molecular testing for clinical diagnosis and epidemiological investigations of intestinal parasitic infections. Clin microbiol Rev 2014;27(2):371-418.
30. Bahrami F, Haghighi A, Zamini G, Khademerfan M. Molecular evidence for zoonotic transmission of Blastocystis subtypes in Kurdistan province, West of Iran. Ann Parasitol 2020;66(1):19–25-19–25.
31. Salehi R, Haghighi A, Stensvold CR, Kheirandish F, Azargashb E, Raeghi S, et al. Prevalence and subtype identification of Blastocystis isolated from humans in Ahvaz, Southwestern Iran. Gastroenterol Hepatol Bed Bench 2017;10(3):235.
32. Riabi TR, Mirjalali H, Haghighi A, Nejad MR, Pourhoseingholi MA, Poirier P, et al. Genetic diversity analysis of Blastocystis subtypes from both symptomatic and asymptomatic subjects using a barcoding region from the 18S rRNA gene. Infect Genet Evol 2018;61:119-26.
33. Shahbazi A, Fallah E, Heydarian P, Ghazanchaei A, Khanmohammadi M, Mirsamdi N. PCR-based subtyping of blastocystis isolates from symptomatic and asymptomatic patients in North-West of Iran. J Pure Appl Microbiol 2013;7(4):2957-63.
34. Badparva E, Sadraee J, Kheirandish F, Frouzandeh M. Genetic diversity of human blastocystis isolates in khorramabad, central iran. Iran J Parasitol 2014;9(1):44.
35. 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.
36. Popruk S, Udonsom R, Koompapong K, Mahittikorn A, Kusolsuk T, Ruangsittichai J, et al. Subtype distribution of Blastocystis in Thai-Myanmar border, Thailand. Korean J Parasitol 2015;53(1):13.
37. Zulfa F, Sari IP, Kurniawan A, editors. Association of Blastocystis subtypes with diarrhea in children. J Physics: Conference Series; 2017; IOP Publishing Ltd.
38. Meloni D, Sanciu G, Poirier P, El Alaoui H, Chabé M, Delhaes L, et al. Molecular subtyping of Blastocystis sp. isolates from symptomatic patients in Italy. Parasitol Res 2011;109(3):613-9.
39. Li L-H, Zhou X-N, Du Z-W, Wang X-Z, Wang L-B, Jiang J-Y, et al. Molecular epidemiology of human Blastocystis in a village in Yunnan province, China. Parasitol Int 2007;56(4):281-6.
40. 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.
41. Souppart L, Moussa H, Cian A, Sanciu G, Poirier P, El Alaoui H, et al. Subtype analysis of Blastocystis isolates from symptomatic patients in Egypt. Parasitol Res 2010;106(2):505-11.
42. Santín M, Gómez-Muñoz MT, Solano-Aguilar G, Fayer R. Development of a new PCR protocol to detect and subtype Blastocystis spp. from humans and animals. Parasitol Res 2011;109(1):205-12.
43. Alfellani MA, Jacob AS, Perea NO, Krecek RC, Taner-Mulla D, Verweij JJ, et al. Diversity and distribution of Blastocystis sp. subtypes in non-human primates. Parasitol 2013;140(8):966-71.
44. Jantermtor S, Pinlaor P, Sawadpanich K, Pinlaor S, Sangka A, Wilailuckana C, et al. Subtype identification of Blastocystis spp. isolated from patients in a major hospital in northeastern Thailand. Parasitol Res. 2013;112(4):1781-6.
45. Khademvatan S, Masjedizadeh R, Rahim F, Mahbodfar H, Salehi R, Yousefi-Razin E, et al. Blastocystis and irritable bowel syndrome: Frequency and subtypes from Iranian patients. Parasitol Int 2017;66(2):142-5.
46. Özyurt M, Kurt Ö, Mølbak K, Nielsen HV, Haznedaroglu T, Stensvold CR. Molecular epidemiology of Blastocystis infections in Turkey. Parasitol Int 2008;57(3):300-6.
47. El Safadi D, Gaayeb L, Meloni D, Cian A, Poirier P, Wawrzyniak I, et al. Children of Senegal River Basin show the highest prevalence of Blastocystissp. ever observed worldwide. BMC Infect Dis 2014;14(1):164.
48. Ramírez JD, Sánchez LV, Bautista DC, Corredor AF, Flórez AC, Stensvold CR. Blastocystis subtypes detected in humans and animals from Colombia. Infect Genet Evol 2014;22:223-8.
49. Rivera WL. Phylogenetic analysis of Blastocystis isolates from animal and human hosts in the Philippines. Vet Parasitol 2008;156(3-4):178-82.
50. Clark CG, van der Giezen M, Alfellani MA, Stensvold CR. Recent developments in Blastocystis research. Advances in parasitology. 82: Elsevier; 2013. p. 1-32.
51. Stensvold CR, Clark CG. Current status of Blastocystis: a personal view. Parasitol Int 2016;65(6):763-71.
52. Oliveira-Arbex AP, David ÉB, Guimarães S. Blastocystis genetic diversity among children of low-income daycare center in Southeastern Brazil. Infect Genet Evol 2018;57:59-63.
53. Jalallou N, Iravani S, Rezaeian M, Alinaghizade A, Mirjalali H. Subtypes distribution and frequency of Blastocystis sp. isolated from diarrheic and non-diarrheic patients. Iran J Parasitol 2017;12(1):63.
54. Alinaghizade A, Mirjalali H, Mohebali M, Stensvold CR, Rezaeian M. Inter-and intra-subtype variation of Blastocystis subtypes isolated from diarrheic and non-diarrheic patients in Iran. Infect Genet Evol 2017;50:77-82.
55. Ramírez JD, Sánchez A, Hernández C, Flórez C, Bernal MC, Giraldo JC, et al. Geographic distribution of human Blastocystis subtypes in South America. Infect Genet Evol 2016;41:32-5.
56. Yıldız S, Doğan İ, Doğruman Al F, Nalbantoğlu U, Üstek D, Sarzhanov F, et al. Association of enteric protist Blastocystis spp. and gut microbiota with hepatic encephalopathy. 2016.
57. Muadica AS, Köster PC, Dashti A, Bailo B, Hernández-de-Mingo M, Reh L, et al. Molecular diversity of Giardia duodenalis, Cryptosporidium spp. and Blastocystis sp. in asymptomatic school children in Leganés, Madrid (Spain). Microorganisms 2020;8(4):466.
58. Sharifi Y, Abbasi F, Shahabi S, Zaraei A, Mikaeili F, Sarkari B. Comparative genotyping of Blastocystis infecting cattle and human in the south of Iran. Comp Immunol Microbiol Infect Dis 2020;72:101529.
59. Khoshnood S, Rafiei A, Saki J, Alizadeh K. Prevalence and genotype characterization of Blastocystis hominis among the baghmalek people in southwestern Iran in 2013-2014. Jundishapur j Microbiol 2015;8(10).
60. Piranshahi AR, Tavalla M, Khademvatan S. Genomic analysis of Blastocystis hominis isolates in patients with HIV-positive using locus SSU-rDNA. J Parasit Dis 2018;42(1):28-33.
61. Koltas IS, Eroglu F. Subtype analysis of Blastocystis isolates using SSU rRNA-DNA sequencing in rural and urban population in southern Turkey. Exp Parasitol 2016;170:247-51.
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