Investigation of Blastocystis Prevalence in Rural Areas: A Field Study Example

Abstract

Blastocystis is a zoonotic protist that is commonly found in humans and other mammals, as well as birds, reptiles, fish and insects. More epidemiological studies are needed to identify risk factors for Blastocystis transmission and to shape control programs. The aim of this study was to investigate the prevalence of Blastocystis among the people living in Kırıklı village in Karaisali district of Adana province. Stool samples of 115 participants were examined for the presence of Blastocystis by direct microscopy (DM) and culture method. DM positivity was 40% (46/115) and culture positivity was 70.4% (81/115), and this difference was statistically significant (p= 0.006). It was determined that the use of culture method in the diagnosis was advantageous in the detection of Blastocystis. While no statistically significant correlation was found between Blastocystis positivity and sociodemographic factors like age, gender, and body mass index (BMI), it is crucial to highlight the elevated prevalence of Blastocystis in areas where livestock farming is prevalent and the zoonotic cycle in the transmission of the parasite.

Keywords

• Blastocystis
• Culture
• Field Study
• Prevalence

Project Number

123S965

Ethical Statement

This research was approved by The Ethics Committee of the Faculty of Medicine, Çukurova University (Ref No: 135/49, Tarih: 14/07/2023)

Kırsal Alanda Blastocystis Prevalansının Araştırılması: Saha Çalışma Örneği

Abstract

Blastocystis, insanlar ile diğer memelilerin yanı sıra kuş, sürüngen, balık, böcek gibi pek çok canlıda yaygın olarak bulunan zoonotik bir protisttir. Blastocystis bulaşındaki risk faktörlerini belirlemek ve kontrol programlarını şekillendirmek için daha fazla epidemiyolojik çalışmaya ihtiyaç duyulmaktadır. Çalışmamızda Adana ilinin Karaisali ilçesine bağlı Kırıklı köyünde yaşayanlarda Blastocystis prevalansının araştırılması amaçlanmıştır. Çalışmaya dahil edilen 115 katılımcının dışkı örneği direkt mikroskobi (DM) ve kültür yöntemiyle Blastocystis varlığı açısından incelenmiştir. Yöntemlerden DM pozitifliği %40 (46/115), kültür pozitifliği ise %70,4 (81/115) olarak tespit edilmiş, bu fark istatistiksel olarak anlamlılık göstermiştir (p = 0,006). Tanıda kültür yönteminin kullanılmasının Blastocystis belirlenmesinde avantaj sağladığı tespit edilmiştir. Blastocystis varlığına ilişkin yaş, cinsiyet, vücut kitle indeksi (VKİ) gibi sosyodemografik faktörler ile Blastocystis pozitifliği arasında istatistiksel olarak anlamlı bir ilişki görülmemiş olsa da hayvancılık yapılan bölgelerde Blastocystis pozitifliğinin yüksek olduğunun gösterilmesi ve parazitin bulaşında zoonotik döngünün üzerinde durulması gerektiğine vurgu açısından önemli bulunmuştur.

Keywords

• Blastocystis
• Kültür
• Prevalans
• Saha Çalışması

Project Number

123S965

Ethical Statement

Bu araştırma Çukurova Üniversitesi Tıp Fakültesi Etik Kurulu tarafından onaylanmıştır (Ref No: 135/49, Tarih: 14/07/2023)

References

1. Abdo, S. M., El-Adawy, H., Farag, H. F., El-Taweel, H. A., Elhadad, H., & El-Badry, A. A. (2021). Detection and molecular identification of Blastocystis isolates from humans and cattle in northern Egypt. Journal of parasitic diseases : official organ of the Indian Society for Parasitology, 45(3), 738–745. https://doi.org/10.1007/s12639-021-01354-5
2. Abdulsalam, A. M., Ithoi, I., Al-Mekhlafi, H. M., Khan, A. H., Ahmed, A., Surin, J., & Mak, J. W. (2013). Prevalence, predictors and clinical significance of Blastocystis sp. in Sebha, Libya. Parasites & vectors, 6, 86. https://doi.org/10.1186/1756-3305-6-86
3. Aykur, M., Calıskan Kurt, C., Dirim Erdogan, D., Biray Avcı, C., Vardar, R., Aydemir, S., Girginkardesler, N., Gunduz, C., & Dagci, H. (2023). Distribution and Phylogenetic Analysis of Subtypes and Alleles of Blastocystis sp. in the Stool Samples Collected from Patients with Gastrointestinal Complaints in İzmir, Turkey. Acta parasitologica, 68(2), 304–316. https://doi.org/10.1007/s11686-023-00665-2
4. Aykur, M., Camyar, A., Türk, B. G., Sin, A. Z., & Dagci, H. (2022). Evaluation of association with subtypes and alleles of Blastocystis with chronic spontaneous urticaria. Acta tropica, 231, 106455. https://doi.org/10.1016/j.actatropica.2022.106455
5. Bahrami, F., Babaei, E., Badirzadeh, A., Riabi, T. R., & Abdoli, A. (2020). Blastocystis, urticaria, and skin disorders: review of the current evidences. European journal of clinical microbiology & infectious diseases : official publication of the European Society of Clinical Microbiology, 39(6), 1027–1042. https://doi.org/10.1007/s10096-019-03793-8
6. Beyhan, Y. E., Güven, İ., & Aydın, M. (2023). Detection of Blastocystis sp. in ulcerative colitis, Crohn's and chronic diarrheal patients by microscopy, culture and real-time polymerase chain reaction. Microbial pathogenesis, 177, 106039. https://doi.org/10.1016/j.micpath.2023.106039
7. Boutahar, M., Belaouni, M., Ibrahimi, A., Eljaoudi, R., Aanniz, T., & Er-Rami, M. (2023). Prevalence of Blastocystis sp. in Morocco: Comparative assessment of three diagnostic methods and characterization of parasite forms in Jones' culture medium. Parasite (Paris, France), 30, 64. https://doi.org/10.1051/parasite/2023065 Boutahar, M., Er-Rami, M., & Belaouni, M. (2023). Prevalence of Blastocystis sp. among cooks in the region of Fez-Meknes (Morocco). Helminthologia, 60(1), 36–43. https://doi.org/10.2478/helm-2023-0002
8. Centers for Disease Control and Prevention. ‘’ Blastocystis spp. infection’’. https://www.cdc.gov/parasites/blastocystis/index.html . Son erişim tarihi: 06 Mayıs 2024

9. Celik, T., Daldal, N., Karaman, U., Aycan, O. M., & Atambay, M. (2006). Malatya ili merkezinde üç ilköğretim okulu çocuklarinda bağirsak parazitlerinin dağilimi. Turkiye Parazitoloii Dergisi, 30(1), 35–38.
10. Dagci, H., Kurt, O., Demirel, M., Ostan, I., Azizi, N. R., Mandiracioglu, A., Yurdagül, C., Tanyüksel, M., Eroglu, E., & Ak, M. (2008). The prevalence of intestinal parasites in the province of Izmir, Turkey. Parasitology research, 103(4), 839–845. https://doi.org/10.1007/s00436-008-1065-6
11. Dogruman-Al, F., Yoshikawa, H., Kustimur, S., & Balaban, N. (2009). PCR-based subtyping of Blastocystis isolates from symptomatic and asymptomatic individuals in a major hospital in Ankara, Turkey. Parasitology research, 106(1), 263–268. https://doi.org/10.1007/s00436-009-1658-8
12. Eida M., & Eida A. (2008). Identification of Blastocystis hominis in patients with irritable bowel syndrome using microscopy and culture compared to PCR, Parasitol. United J. 1 (2) 87–89.
13. El Safadi, D., Gaayeb, L., Meloni, D., Cian, A., Poirier, P., Wawrzyniak, I., Delbac, F., Dabboussi, F., Delhaes, L., Seck, M., Hamze, M., Riveau, G., & Viscogliosi, E. (2014). Children of Senegal River Basin show the highest prevalence of Blastocystis sp. ever observed worldwide. BMC infectious diseases, 14, 164. https://doi.org/10.1186/1471-2334-14-164
14. El Safadi, D., Meloni, D., Poirier, P., Osman, M., Cian, A., Gaayeb, L., Wawrzyniak, I., Delbac, F., El Alaoui, H., Delhaes, L., Dei-Cas, E., Mallat, H., Dabboussi, F., Hamze, M., & Viscogliosi, E. (2013). Molecular epidemiology of Blastocystis in Lebanon and correlation between subtype 1 and gastrointestinal symptoms. The American journal of tropical medicine and hygiene, 88(6), 1203–1206. https://doi.org/10.4269/ajtmh.12-0777
15. Elghareeb, A. S., Younis, M. S., El Fakahany, A. F., Nagaty, I. M., & Nagib, M. M. (2015). Laboratory diagnosis of Blastocystis spp. in diarrheic patients. Tropical parasitology, 5(1), 36–41. https://doi.org/10.4103/2229-5070.149919
16. Ergüden Gürbüz, C., Gülmez, A., Özkoç, S., İnceboz, T., Miman, Ö., Aksoy, Ü., & Bayram Delibaş, S. (2020). Distribution of Intestinal Parasites Detected between September 2011-2018 at Dokuz Eylül University Medical Faculty Hospital. Turkiye parazitolojii dergisi, 44(2), 83–87. https://doi.org/10.4274/tpd.galenos.2020.6662
17. Gureser, A. S., Karasartova, D., Sarzhanov, F., Kosar, N., Taylan-Ozkan, A., & Dogruman-Al, F. (2023). Prevalence of Blastocystis and Dientamoeba fragilis in diarrheal patients in Corum, Türkiye. Parasitology research, 122(12), 2977–2987. https://doi.org/10.1007/s00436-023-07987-0
18. Güler, E., & Süer, K. (2021). Epidemiology of Intestinal Parasites in a University Hospital in Northern Cyprus: A 4-year Retrospective Experience. Kuzey Kıbrıs’ta Bir Üniversite Hastanesinde İntestinal Parazitlerin Epidemiyolojisi: Dört Yıllık Retrospektif Deneyim. Turkiye parazitolojii dergisi, 45(2), 128–132. https://doi.org/10.4274/tpd.galenos.2021.6847
19. Hajare, S. T., Gobena, R. K., Chauhan, N. M., & Erniso, F. (2021). Prevalence of Intestinal Parasite Infections and Their Associated Factors among Food Handlers Working in Selected Catering Establishments from Bule Hora, Ethiopia. BioMed research international, 2021, 6669742. https://doi.org/10.1155/2021/6669742
20. Hamdy, D. A., Abd El Wahab, W. M., Senosy, S. A., & Mabrouk, A. G. (2020). Blastocystis spp. and Giardia intestinalis co-infection profile in children suffering from acute diarrhea. Journal of parasitic diseases : official organ of the Indian Society for Parasitology, 44(1), 88–98. https://doi.org/10.1007/s12639-019-01165-9
21. Hublin, J. S. Y., Maloney, J. G., & Santin, M. (2021). Blastocystis in domesticated and wild mammals and birds. Research in veterinary science, 135, 260–282. https://doi.org/10.1016/j.rvsc.2020.09.031
22. Idowu, O. A., & Rowland, S. A. (2006). Oral fecal parasites and personal hygiene of food handlers in Abeokuta, Nigeria. African health sciences, 6(3), 160–164. https://doi.org/10.5555/afhs.2006.6.3.160
23. Khorshidvand, Z., Khazaei, S., Amiri, M., Taherkhani, H., & Mirzaei, A. (2021). Worldwide prevalence of emerging parasite Blastocystis in immunocompromised patients: A systematic review and meta-analysis. Microbial pathogenesis, 152, 104615.
24. Kurt, Ö., Doğruman Al, F., & Tanyüksel, M. (2016). Eradication of Blastocystis in humans: Really necessary for all?. Parasitology international, 65(6 Pt B), 797–801. https://doi.org/10.1016/j.parint.2016.01.010
25. Li, L. H., Zhang, X. P., Lv, S., Zhang, L., Yoshikawa, H., Wu, Z., Steinmann, P., Utzinger, J., Tong, X. M., Chen, S. H., & Zhou, X. N. (2007). Cross-sectional surveys and subtype classification of human Blastocystis isolates from four epidemiological settings in China. Parasitology research, 102(1), 83–90. https://doi.org/10.1007/s00436-007-0727-0
26. Maçin S, Musayeva L. (2019). Gastroenterit Tanısı İle Hastanemize Başvuran Pediatrik Hastalarda Blastocystis spp. Varlığının Araştırılması. Pediatr Pract Res. 7(Ek):497-500.
27. Menu, E., Mary, C., Toga, I., Raoult, D., Ranque, S., & Bittar, F. (2019). A hospital qPCR-based survey of 10 gastrointestinal parasites in routine diagnostic screening, Marseille, France. Epidemiology and infection, 147, e100. https://doi.org/10.1017/S0950268819000165
28. Mohemmi N, Moradi M, Khalilian A vd. (2015). The relationship between Blastocystis hominis infection and Irritable Bowel Syndrome (IBS) and comparing direct wet mount, stool culture, FormalinEther and trichrome staining procedures for identifying organisms. Hormozgan Medical Journal, Vol 19, No.2, June-July
29. Nguyen, L. D. N., Gantois, N., Hoang, T. T., Do, B. T., Desramaut, J., Naguib, D., Tran, T. N., Truong, A. D., Even, G., Certad, G., Chabé, M., & Viscogliosi, E. (2023). First Epidemiological Survey on the Prevalence and Subtypes Distribution of the Enteric Parasite Blastocystis sp. in Vietnam. Microorganisms, 11(3), 731. https://doi.org/10.3390/microorganisms11030731
30. Osman, M., El Safadi, D., Cian, A., Benamrouz, S., Nourrisson, C., Poirier, P., Pereira, B., Razakandrainibe, R., Pinon, A., Lambert, C., Wawrzyniak, I., Dabboussi, F., Delbac, F., Favennec, L., Hamze, M., Viscogliosi, E., & Certad, G. (2016). Prevalence and Risk Factors for Intestinal Protozoan Infections with Cryptosporidium, Giardia, Blastocystis and Dientamoeba among Schoolchildren in Tripoli, Lebanon. PLoS neglected tropical diseases, 10(3), e0004496. https://doi.org/10.1371/journal.pntd.0004496
31. Öncel K. (2018). Distribution of Intestinal Parasites Detected in Şanlıurfa Mehmet Akif Inan Education and Research Hospital Between October 2015 and October 2016. Turkiye parazitolojii dergisi, 42(1), 20–27. https://doi.org/10.5152/tpd.2018.5718
32. Peruzzi, S., Gorrini, C., Piccolo, G., Calderaro, A., Dettori, G., & Chezzi, C. (2006). Prevalence of intestinal parasites in the area of Parma during the year 2005. Acta bio-medica : Atenei Parmensis, 77(3), 147–151.
33. Piubelli, C., Soleymanpoor, H., Giorli, G., Formenti, F., Buonfrate, D., Bisoffi, Z., & Perandin, F. (2019). Blastocystis prevalence and subtypes in autochthonous and immigrant patients in a referral centre for parasitic infections in Italy. PloS one, 14(1), e0210171. https://doi.org/10.1371/journal.pone.0210171
34. Polat E, Özdemir S, Sirekbasan S. (2020). İstanbul’da Bir Üniversite Hastanesine Başvuran Hastalarda Bağırsak Parazitlerinin Dağılımı: Yedi Yıllık Retrospektif Analiz. Turkiye Parazitoloji Dergisi ;44(3):139-42.
35. Rebolla, M. F., Silva, E. M., Gomes, J. F., Falcão, A. X., Rebolla, M. V., & Franco, R. M. (2016). High Prevalence of Blastocystis Spp. Infection In Children and Staff Members Attending Public Urban Schools in São Paulo State, Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo, 58, 31. https://doi.org/10.1590/S1678-9946201658031
36. Roberts, T., Barratt, J., Harkness, J., Ellis, J., & Stark, D. (2011). Comparison of microscopy, culture, and conventional polymerase chain reaction for detection of blastocystis sp. in clinical stool samples. The American journal of tropical medicine and hygiene, 84(2), 308–312. https://doi.org/10.4269/ajtmh.2011.10-0447 Ruang-Areerate, T., Piyaraj, P., Suwannahitatorn, P., Ruang-Areerate, P., Thita, T., Naaglor, T., Witee, U., Sakboonyarat, B., Leelayoova, S., & Mungthin, M. (2021). Zoonotic Transmission of Blastocystis Subtype 1 among People in Eastern Communities of Thailand: Organic Fertilizer from Pig Feces as a Potential Source. Microbiology spectrum, 9(2), e0036221. https://doi.org/10.1128/Spectrum.00362-21
37. Salehi, R., Rostami, A., Mirjalali, H., Stensvold, C. R., & Haghighi, A. (2022). Genetic characterization of Blastocystis from poultry, livestock animals and humans in the southwest region of Iran-Zoonotic implications. Transboundary and emerging diseases, 69(3), 1178–1185. https://doi.org/10.1111/tbed.14078
38. Santos, H. J., & Rivera, W. L. (2013). Comparison of direct fecal smear microscopy, culture, and polymerase chain reaction for the detection of Blastocystis sp. in human stool samples. Asian Pacific journal of tropical medicine, 6(10), 780–784. https://doi.org/10.1016/S1995-7645(13)60138-8
39. Sarzhanov, F., Dogruman-Al, F., Santin, M., Maloney, J. G., Gureser, A. S., Karasartova, D., & Taylan-Ozkan, A. (2021). Investigation of neglected protists Blastocystis sp. and Dientamoeba fragilis in immunocompetent and immunodeficient diarrheal patients using both conventional and molecular methods. PLoS neglected tropical diseases, 15(10), e0009779. https://doi.org/10.1371/journal.pntd.0009779
40. Seyer, A., Karasartova, D., Ruh, E., Güreser, A. S., Turgal, E., Imir, T., & Taylan-Ozkan, A. (2017). Epidemiology and Prevalence of Blastocystis spp. in North Cyprus. The American journal of tropical medicine and hygiene, 96(5), 1164–1170. https://doi.org/10.4269/ajtmh.16-0706
41. Shaker D, Fakhar M, Ziaei H, et al. (2017). Prevalence of Blastocystis hominis in Individuals Attending Sari Health Centers, 2014. J Mazandaran Univ Med Sci. ;27(148):143-7
42. 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. Parasitology research, 105(2), 413–421. https://doi.org/10.1007/s00436-009-1398-9
43. Şahin, M., Ödemiş, N., Yılmaz, H., & Beyhan, Y. E. (2023). Investigation of Parasites in Food Handlers in Turkey. Foodborne pathogens and disease, 20(9), 381–387. https://doi.org/10.1089/fpd.2023.0016
44. Takizawa, M.d, Falavigna, D. L., & Gomes, M. L. (2009). Enteroparasitosis and their ethnographic relationship to food handlers in a tourist and economic center in Paraná, Southern Brazil. Revista do Instituto de Medicina Tropical de Sao Paulo, 51(1), 31–35. https://doi.org/10.1590/s0036-46652009000100006 Tan K. S. (2008). New insights on classification, identification, and clinical relevance of Blastocystis spp. Clinical microbiology reviews, 21(4), 639–665. https://doi.org/10.1128/CMR.00022-08
45. Tanrıverdi Çaycı, Y., Hacıeminoğlu, K., Birinci A. (2017). Ondokuz Mayıs Üniversitesi Hastanesi Tıbbi Parazitoloji Laboratuvarında 2014-2016 Yılları Arasında Saptanan Bağırsak Parazitlerinin Dağılımı. Kocaeli Üniversitesi Sağlık Bilimleri Dergisi, 3(3),.6-8.
46. Tavur A. Önder Z. (2022): Molecular Prevalence and Phylogenetic Characterization of Blastocystis in Cattle in Kayseri Province, Turkey. Kocatepe Vet Journal, 15(1):1-6.
47. Termmathurapoj, S., Leelayoova, S., Aimpun, P., Thathaisong, U., Nimmanon, T., Taamasri, P., & Mungthin, M. (2004). The usefulness of short-term in vitro cultivation for the detection and molecular study of Blastocystis hominis in stool specimens. Parasitology research, 93(6), 445–447. https://doi.org/10.1007/s00436-004-1157-x
48. Viesy, S., Rezaei, Z., Pouladi, I., Mirzaei, A., & Abdi, J. (2022). The Prevalence of Blastocystis sp. and Its Relationship with Gastrointestinal Disorders and Risk factors. Iranian journal of parasitology, 17(1), 90–95. https://doi.org/10.18502/ijpa.v17i1.9029
49. World Health Organization (2011) ‘’ Guidelines for Drinking-water Quality’’. https://www.who.int/publications/m/item/guidelines-for-drinking-water-quality-4th-ed.-incorporating-the-1st-addendum-(chapters) Son erişim tarihi: 7 Mayıs 2023.
50. Xu, N., Jiang, Z., Liu, H., Jiang, Y., Wang, Z., Zhou, D., Shen, Y., & Cao, J. (2021). Prevalence and genetic characteristics of Blastocystis hominis and Cystoisospora belli in HIV/AIDS patients in Guangxi Zhuang Autonomous Region, China. Scientific reports, 11(1), 15904. https://doi.org/10.1038/s41598-021-94962-3
51. Yakoob, J., Jafri, W., Beg, M. A., Abbas, Z., Naz, S., Islam, M., & Khan, R. (2010). Blastocystis hominis and Dientamoeba fragilis in patients fulfilling irritable bowel syndrome criteria. Parasitology research, 107(3), 679–684. https://doi.org/10.1007/s00436-010-1918-7
52. Zamani, R., Khademvatan, S., Tappeh, K. H., Diba, K., & Abasi, E. (2021). Comparison of diagnostic methods (wet mount, trichrome staining, formol-ether, PCR, and xenic in vitro culture) for the detection of Blastocystis in stool samples in Urmia educational hospitals, the Northwest of Iran. Annals of parasitology, 67(4), 795–803. https://doi.org/10.17420/ap6704.398