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Open Access 01-12-2016 | Research article

Prevalence, risk factors for infection and subtype distribution of the intestinal parasite Blastocystis sp. from a large-scale multi-center study in France

Published in: BMC Infectious Diseases | Issue 1/2016

Abstract

Background

Blastocystis sp. is the most common intestinal parasite of humans. Despite its potential public health impact, epidemiological data regarding the prevalence and molecular subtype distribution of Blastocystis sp. in Europe are rarely reported. Therefore, the first multi-center epidemiological survey performed in Europe was conducted in France to diagnose and subtype Blastocystis sp. and to identify risk factors for infection.

Methods

Stool samples from 788 patients were collected either in summer or winter in 11 hospitals throughout France together with patient data. All stool samples were tested for the presence of Blastocystis sp. by quantitative PCR targeting the SSU rDNA gene. Positive samples were sequenced to determine the distribution of the subtypes in our cohort. Statistical analyses were performed to identify potential risk factors for infection.

Results

Using quantitative PCR, the overall prevalence of Blastocystis sp. was shown to reach 18.1 %. The prevalence was significantly higher in summer (23.2 %) than in winter (13.7 %). Travellers or subjects infected with other enteric parasites were significantly more infected by Blastocystis sp. than non-travellers or subjects free of other enteric parasites, respectively. Different age-related epidemiological patterns were also highlighted from our data. The prevalence of Blastocystis sp. was not significantly higher in patients with digestive symptoms or diagnosed with chronic bowel diseases. Among symptomatic patients, Blastocystis sp. infection was significantly associated with abdominal pain. Gender, socioeconomic status, and immune status were not identified as potential risk factors associated with infection. Among a total of 141 subtyped isolates, subtype 3 was predominant (43.3 %), followed by subtype 1 and subtype 4 (20 %), subtype 2 (12.8 %), subtype 6 and subtype 7 (2.1 %). No association between ST and clinical symptoms was statistically evidenced.

Conclusions

A high prevalence of Blastocystis sp. infection was found in our French patient population. Seasonal impact on the prevalence of Blastocystis sp. was highlighted and recent travels and age were identified as main risk factors for infection. Most cases were caused by subtypes 1 to 4, with a predominance of subtype 3. Large variations in both prevalence and ST distribution between hospitals were also observed, suggesting distinct reservoirs and transmission sources of the parasite.

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Tan KS. New insights on classification, identification, and clinical relevance of Blastocystis spp. Clin Microbiol Rev. 2008;21:639–65.CrossRefPubMedPubMedCentral

Clark CG, van der Giezen M, Alfellani MA, Stensvold CR. Recent developments in Blastocystis research. Adv Parasitol. 2013;82:1–32.CrossRefPubMed

Wawrzyniak I, Poirier P, Viscogliosi E, Meloni D, Texier C, Delbac F, El Alaoui H. Blastocystis, an unrecognized parasite: an overview of pathogenesis and diagnosis. Ther Adv Infect Dis. 2013;1:167–78.CrossRefPubMedPubMedCentral

Alfellani MA, Stensvold CR, Vidal-Lapiedra A, Onuoha ES, Fagbenro-Beyioku AF, Clark CG. Variable geographic distribution of Blastocystis subtypes and its potential implications. Acta Trop. 2013;126:11–8.CrossRefPubMed

Bart A, Wentink-Bonnema EMS, Gilis H, Verhaar N, Wassenaar CJA, van Vugt M, Goorhuis A, van Gool T. Diagnosis and subtype analysis of Blastocystis sp. in 442 patients in a hospital setting in the Netherlands. BMC Infect Dis. 2013;13:389.CrossRefPubMedPubMedCentral

Ramirez JD, Sanchez LV, Bautista DC, Corredor AF, Florez AC, Stensvold CR. Blastocystis subtypes detected in humans and animals from Colombia. Infect Genet Evol. 2014;22:223–8.CrossRefPubMed

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. Children of Senegal River Basin show the highest prevalence of Blastocystis sp. ever observed worldwide. BMC Infect Dis. 2014;14:164.CrossRefPubMedPubMedCentral

Suresh K, Smith H, Tan T. Viable Blastocystis cysts in Scottish and Malaysian sewage samples. Appl Environ Microbiol. 2005;71:5619–20.CrossRefPubMedPubMedCentral

Poirier P, Wawrzyniak I, Albert A, El AH, 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;49:975–83.CrossRefPubMedPubMedCentral

10.

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

11.

Parkar U, Traub RJ, Vitali S, Elliot A, Levecke B, Robertson I, Geurden T, Steele J, Drake B, Thompson RCA. Molecular characterization of Blastocystis isolates from zoo animals and their animal-keepers. Vet Parasitol. 2010;169:8–17.CrossRefPubMed

12.

Denoeud F, Roussel M, Noël B, Wawrzyniak I, Da Silva C, Diogon M, Viscogliosi E, Brochier-Armamet C, Couloux A, Poulain J, Segurans B, Anthouard V, Texier C, Blot N, Poirier P, Ng GC, Tan KSW, Antiguenave F, Jaillon O, Aury J, Delbac F, Wincker P, Vivarès CP, El Alaoui H. Genome sequence of the stramenopile Blastocystis, a human anaerobic parasite. Genome Biol. 2011;12:R29.CrossRefPubMedPubMedCentral

13.

Mirza H, Wu Z, Teo JDW, Tan KSW. Statin pleiotropy prevents rho kinase-mediated intestinal epithelial barrier compromise induced by Blastocystis cysteine proteases. Cell Microbiol. 2012;14:1474–84.CrossRefPubMed

14.

Ajjampur SSR, Tan KSW. Pathogenic mechanisms in Blastocystis spp. – Interpreting results from in vitro and in vivo studies. Parasitol Int. 2016, http://dx.doi.org/10.1016/j.parint.2016.05.007.

15.

Wu Z, Mirza H, Tan KSW. Intra-subtype variation in enteroadhesion accounts for differences in epithelial barrier disruption and is associated with metronidazole resistance in Blastocystis subtype-7. PLoS Negl Trop Dis. 2014;8:e2885.CrossRefPubMedPubMedCentral

16.

Poirier P, Wawrzyniak I, Vivares CP, Delbac F, El Alaoui H. New insights into Blastocystis spp.: a potential link with irritable bowel syndrome. PLoS Pathog. 2012;8:e1002545.CrossRefPubMedPubMedCentral

17.

Nourrisson C, Scanzi J, Pereira B, NkoudMango C, Wawrzyniak I, Cian A, Viscogliosi E, Livrelli V, Delbac F, Dapoigny M, Poirier P. Blastocystis is associated with decrease of fecal microbiota protective bacteria: comparative analysis between patients with irritable bowel syndrome and control subjects. PLoS One. 2014;9:e111868.CrossRefPubMedPubMedCentral

18.

Longstreth GF, Thompson WG, Chey WD, Houghton LA, Mearin F, Spiller RC. Functional bowel disorders. Gastroenterology. 2006;130:1480–91.CrossRefPubMed

19.

Pinel C, Réjasse C, Picot S, Brenier-Pinchart MP, Grillot R, Ambroise-Thomas P. Blastocystis hominis: réfléxions épidémiologiques et cliniques à propos de plus de 3500 examens coprologiques. Ann Biol Clin (Paris). 1999;57:601–4.

20.

Bourée P. Blastocystis: commensal ou pathogène? Etude de 590 cas et revue de la littérature. Antibiotiques. 2007;9:20–4.CrossRef

21.

Souppart L, Sanciu G, Cian A, Wawrzyniak I, Delbac F, Capron M, Dei-Cas E, Boorom K, Delhaes L, Viscogliosi E. Molecular epidemiology of human Blastocystis isolates in France. Parasitol Res. 2009;105:413–21.CrossRefPubMed

22.

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;59:303–7.CrossRefPubMed

23.

Masucci L, Graffeo R, Bani S, Bugli F, Boccia S, Nicolotti N, Fiori B, Fadda G, Spanu T. Intestinal parasites isolated in a large teaching hospital, Italy, 1 May 2006 to 31 December 2008. Euro Surveill. 2011;16:24.

24.

Gonzalez-Moreno O, Domingo L, Teixidor J, Gracenea M. Prevalence and associated factors of intestinal parasitisation: a cross-sectional study among outpatients with gastrointestinal symptoms in Catalonia, Spain. Parasitol Res. 2011;108:87–93.CrossRefPubMed

25.

Windsor JJ, Macfarlane L, Hughes-Thapa G, Jones SK, Whiteside TM. Incidence of Blastocystis hominis in faecal samples submitted for routine microbiological analysis. Br J Biomed Sci. 2002;59:154–7.CrossRefPubMed

26.

Suresh K, Smith H. Comparison of methods for detecting Blastocystis hominis. Eur J Clin Microbiol Infect Dis. 2004;23:509–11.CrossRefPubMed

27.

Haider SS, Baqai R, Qureshi FM, Boorom K. Blastocystis spp., Cryptosporidium spp., and Entamoeba histolytica exhibit similar symptomatic and epidemiological patterns in healthcare-seeking patients in Karachi. Parasitol Res. 2012;111:1357–68.CrossRefPubMed

28.

Amin OM. The epidemiology of Blastocystis hominis in the United States. Res J Parasitol. 2006;1:1–10.CrossRef

29.

Ithoi I, Jali A, Mak JW, Sulaiman WYW, Mahmud R. Occurrence of Blastocystis in water of two rivers from recreational areas in Malaysia. J Parasitol Res. 2011;2011:123916.CrossRefPubMedPubMedCentral

30.

Nimri LF. Evidence of an epidemic of Blastocystis hominis infections in preschool children in northern Jordan. J Clin Microbiol. 1993;31:2706–8.PubMedPubMedCentral

31.

Dagci H, Kurt Ö, Demirel M, Östan I, Azizi NR, Mandiracioglu A, Yurdagül C, Tanyüksel M, Eroglu C, Ak M. The prevalence of intestinal parasites in the province of Izmir, Turkey. Parasitol Res. 2008;103:839–45.CrossRefPubMed

32.

Pipatsatitpong D, Rangsin R, Leelayoova S, Naaglor T, Mungthin M. Incidence and risk factors of Blastocystis infection in an orphanage in Bangkok, Thailand. Parasit Vectors. 2012;5:37.CrossRefPubMedPubMedCentral

33.

Cirioni O, Giacometti A, Drenaggi D, Ancarani F, Scalise G. Prevalence and clinical relevance of Blastocystis hominis in diverse patient cohorts. Eur J Epidemiol. 1999;15:389–93.CrossRefPubMed

34.

Hailemariam G, Kassu A, Abebe G, Abate E, Damte D, Mekonnen E, Ota F. Intestinal parasitic infections in HIV/AIDS and HIV seronegative individuals in a teaching hospital, Ethiopia. Jpn J Infect Dis. 2004;57:41–3.PubMed

35.

Alemu A, Shiferaw Y, Getnet G, Yalew A, Addis Z. Opportunistic and other intestinal parasites among HIV/AIDS patients attending Gambi higher clinic in Bahir Dar city, North West Ethiopia. Asian Pac J Trop Dis. 2011;4:661–5.CrossRef

36.

Kurniawan A, Karyadi T, Dwintasari SW, Sari IP, Yunihastuti E, Djauzi S, Smith HV. Intestinal parasitic infections in HIV/AIDS patients presenting with diarrhoea in Jakarta, Indonesia. Trans R Soc Trop Med Hyg. 2009;103:892–8.CrossRefPubMed

37.

Stensvold CR, Nielsen SD, Badsberg J-H, Engberg J, Friis-Møller N, Nielsen SS, Nielsen HV, Friis-Moller A. The prevalence and clinical significance of intestinal parasites in HIV-infected patients in Denmark. Scand J Infect Dis. 2011;43:129–35.CrossRefPubMed

38.

Adamu H, Wegayehu T, Petros B. High prevalence of diarrhoegenic intestinal parasite infections among non-ART HIV patients in Fitche Hospital, Ethiopia. PLoS One. 2013;8:e72634.CrossRefPubMedPubMedCentral

39.

Tasova Y, Sahin B, Koltas S, Paydas S. Clinical significance and frequency of Blastocystis hominis in Turkish patients with hematological malignancy. Acta Med Okayama. 2000;54:133–6.PubMed

40.

Cekin AH, Cekin Y, Adakan Y, Tasdemir E, Koclar FG, Yolcular BO. Blastocystosis in patients with gastrointestinal symptoms: a case-control study. BMC Gastroenterol. 2012;12:122.CrossRefPubMedPubMedCentral

41.

Petersen AM, Stensvold CR, Mirsepasi H, Engberg J, Friis-Møller A, Porsbo LJ, Hammerum AM, Nordgaard-Lassen I, Nielsen HV, Krogfelt KA. Active ulcerative colitis associated with low prevalence of Blastocystis and Dientamoeba fragilis infection. Scand J Gastroenterol. 2013;48:638–9.CrossRefPubMed

42.

Mattiucci S, Crisafi B, Gabrielli S, Paoletti M, Cancrini G. Molecular epidemiology and genetic diversity of Blastocystis infection in humans in Italy. Epidemiol Infect. 2016;144:635–46.CrossRefPubMed

Title: Prevalence, risk factors for infection and subtype distribution of the intestinal parasite Blastocystis sp. from a large-scale multi-center study in France
Publication date: 01-12-2016
Published in: BMC Infectious Diseases / Issue 1/2016
Electronic ISSN: 1471-2334
DOI: https://doi.org/10.1186/s12879-016-1776-8

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Results

Conclusions

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