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Open Access 01-12-2019 | Candida Balanitis | Research

The influence of probiotic bacteria and human gut microorganisms causing opportunistic infections on Blastocystis ST3

Authors: M. Lepczyńska, E. Dzika

Published in: Gut Pathogens | Issue 1/2019

Abstract

Background

Blastocystis subtype 3 is an intestinal protist present in humans throughout the world with a controversial pathogenic potential. It has been suggested that probiotic bacteria inhibit the multiplication of gut protozoans, while others are beneficial for their development. This study aimed to evaluate the efficacy of the lactic acid bacteria Lactobacillus rhamnosus, Lactococcus lactis and Enterococcus faecium in Blastocystis ST3 eradication and the relevance of the intestinal microorganisms Escherichia coli, Candida albicans and Candida glabrata in protozoan proliferation. Blastocystis xenic and axenic culture was co-incubated with the above-mentioned microorganisms and their cell free supernatants at different concentrations in vitro. The number of protozoan cells was counted every day.

Results

Both experiments, with xenic and axenic cultures, showed Blastocystis inhibition by L. rhamnosus and L. lactis and their supernatants from the 2nd day of co-incubation. Furthermore, co-incubation with both E. faecium and E. coli showed a beneficial influence on Blastocystis during the first 2 days. Only after 3 days did the above-mentioned bacteria start to inhibit Blastocystis growth in both cultures. The supernatant containing the metabolites of E. coli was effective to a lesser degree. Compared to the control samples, co-incubation with both C. albicans and C. glabrata showed a faster decrease in Blastocystis proliferation, but this was not statistically significant.

Conclusions

This study has shown the potential of using L. rhamnosus and L. lactis, as well as E. faecium as a prophylactic treatment against Blastocystis colonization or as an additional treatment regimen in combination with standard drugs.

Tan KS. New insights on classification, identification and clinical relevance of Blastocystis spp. Clin Microbiol Rev. 2008;21(4):639–65.PubMedPubMedCentralCrossRef

Scanlan PD, Stensvold CR, Rajilić-Stojanović M, Heilig HG, De Vos WM, O’Toole PW, Cotter PD. The microbial eukaryote Blastocystis is a prevalent and diverse member of the healthy human gut microbiota. FEMS Microbiol Ecol. 2014;90(1):326–30.PubMedCrossRef

Basak S, Rajurkar MN, Mallick SK. Detection of Blastocystis hominis: a controversial human pathogen. Parasitol Res. 2014;113(1):261–5.PubMedCrossRef

Lukes J, Stensvold CR, Jirků-Pomajbíková K, Parfrey LW. Are human intestinal eukaryotes beneficial or commensals? PLoS Pathog. 2015;11(8):e1005039.PubMedPubMedCentralCrossRef

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. Molecular phylogenies of Blastocystis isolates from different hosts: implications for genetic diversity, identification of species and zoonosis. J Clin Microbiol. 2005;43(1):348–55.PubMedPubMedCentralCrossRef

El Safadi D, Gaayeb L, Meloni D, Cian A, Poirier P, Wawrzyniak I, Delbak 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;14:164–74.PubMedPubMedCentralCrossRef

Albrecht H, Stellbrink HJ, Koperski K, Greten H. Blastocystis hominis in human immunodeficiency virus—related diarrhea. Scand J Gastroenterol. 1995;30(9):909–14.PubMedCrossRef

Sanchez-Aguillon F, Lopez-Escamilla E, Velez-Perez F, Martinez-Flores WA, Rodriguez-Zulueta P, Martinez-Ocaña J, Martinez-Hernandez F, Romero-Valdovinos M, Maravilla P. Parasitic infections in a Mexican HIV/AIDS cohort. J Infect Dev Ctries. 2013;7(10):763–6.PubMedCrossRef

Lu CTL, Sung YJ. Epidemiology of Blastocystis hominis and other intestinal parasites among the immigrant population in northeastern by routine physical examination for resistance approval. J Microbiol Immunol Infect. 2009;42(6):505–9.PubMed

10.

Zaglool DAM, Khodari YAW, Farooq MU. Blastocystis hominis and allergic skin diseases; a single centre experience. J H Sci. 2012;2(1):66–9.

11.

Abdel-Hameed DM, Hassanin OM. Protease activity of Blastocystis hominis subtype 3 in symptomatic and asymptomatic patients. Parasitol Res. 2011;109(2):321–7.PubMedCrossRef

12.

Teow WL, Ho LC, Ng GC, Chan YC, Yap EH, Chan PP, Howe J, Zaman V, Singh M. Virus—like particles in a Blastocystis species from the sea snake Lapemi hardwickii. Int J Parasitol. 1992;22(7):1029–32.CrossRef

13.

Berrilli F, Di Cave D, Cavallero S, D’Amelio S. Interactions between parasites and microbial communities in the human gut. Front Cell Infect Microbiol. 2012;2:141.PubMedPubMedCentralCrossRef

14.

Nourrisson C, Wawrzyniak I, Cian A, Livrelli V, Viscogliosi E, Delbac F, Poirier P. On Blastocystis secreted cysteine proteases: a legumain-activated cathepsin B increases paracellular permeability of intestinal Caco-2 cell monolayers. Parasitology. 2016;146(13):1713–22.CrossRef

15.

Nagel R, Traub RJ, Allcock RJN, Kwan MMS, Bielefeldt-Ohmann H. Comparison of faecal microbiota in Blastocystis-positive and Blastocystis-negative irritable bowel syndrome patients. Microbiome. 2016;4(1):47.PubMedPubMedCentralCrossRef

16.

Audebert C, Even G, Cian A, The Blastocystis Investigation Group, Loywick A, Merlin S, Viscogliosi E, Chabé M. Colonization with the enteric protozoa Blastocystis is associated with increased diversity of human gut bacterial microbiota. Nat Sci Rep. 2016; Article number 25255. https://doi.org/10.1038/srep25255.

17.

Iebba V, Santangelo F, Totino V, Pantanella F, Monsia A, Di Cristanziano V, Di Cave D, Schippa S, Berrilli F, D’Alfonso R. Gut microbiota related to Giardia duodenalis, Entamoeba spp. and Blastocystis hominis infections in humans from Côte d’Ivoire. J Infect Dev Ctries. 2016;10(9):1035–41.PubMedCrossRef

18.

Molan AL. Bacteria versus parasites: effect of Lactobacillu rhamnosus cell-free supernatant on the sporulation of coccidian oocysts in vitro and in vivo. IOSR J Dental Med Sci. 2014;13(6):86–92.CrossRef

19.

Goyal N, Tiwari RP, Shukla G. Lactobacillus rhamnosus GG as an effective probiotic for murine giardiasis. Interdiscip Perspect Infect Dis. 2011;2011:795219.PubMedPubMedCentralCrossRef

20.

Pérez PF, Minnaard J, Rouvet M, Knabenhans C, Brassart D, De Antoni GL, Schiffrin EJ. Inhibition of Giardia intestinalis by extracellular factors from Lactobacilli: an in vitro study. Appl Environ Microbiol. 2011;67(11):5037–42.CrossRef

21.

Tierney J, Gowing H, Van Sinderen D, Flynn S, Stanley L, McHardy N, Hallahan S, Mulcahy G. In vitro inhibition of Eimeria tenella invasion by indigenous chicken Lactobacillus species. Vet Parasitology. 2004;122(3):171–82.CrossRef

22.

Sarjapuram N, Mekala N, Singh M, Tatu U. The potential of Lactobacillus casei and Enterococcus faecium combination as a preventive probiotic against Entamoeba. Probiotics Antimicrob Proteins. 2016;9(2):142–9.CrossRef

23.

Simpson KW, Rishniw M, Bellosa M, Liotta J, Lucio A, Baumgart M, Czarnecki-Maulden G, Benyacoub J, Bowman D. Influence of Enterococcus faecium SF68 probiotic on giardiasis in dogs. J Vet Intern Med. 2009;23(3):476–81.PubMedCrossRef

24.

Dinleyici EC, Eren M, Dogan N, Reyhanioglu S, Yargic ZA, Vandenplas Y. Clinical efficacy of Saccharomyces boulardii or metronidazole in symptomatic children with Blastocystis hominis infection. Parasitol Res. 2011;108(3):541–5.PubMedCrossRef

25.

Hill C, Guarner F, Reid G, Gibson GR, Merenstein DJ, Pot B, Morelli L, Canani RB, Flint HJ, Salminen S, Calder PC, Sanders ME. Expert consensus document. The International Scientific Association for Probiotics and Prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–14.PubMedCrossRef

26.

Jones WR. The experimental infection of rats with Entamoeba histolytica; with a method for evaluating the anti-amoebic properties of new compounds. Ann Trop Med Parasitol. 1946;40:130–40.PubMedCrossRef

27.

Leelayoova S, Taamasri P, Rangsin R, Naaglor T, Thathaisong U, Mungthin M. In-vitro cultivation: a sensitive method for detecting Blastocystis hominis. Ann Trop Med Parasitol. 2002;96(8):803–7.PubMedCrossRef

28.

El Deeb HK, Al Khadrawy FM, Abd El-Hameid A. Inhibitory effect of Ferula asafetida L. (Umbelliferae) on Blastocystis sp. subtype 3 growth in vitro. Parasitol Res. 2012;111(3):1213–21.PubMedCrossRef

29.

Sawangjaroen N, Sawangjaroen K. The effects of extracts from anti-diarrheic Thai medicinal plants on the in vitro growth of the intestinal protozoa parasite: blastocystis hominis. J Ethnopharmacol. 2005;98(1–2):67–72.PubMedCrossRef

30.

Haresh K, Suresh K, Khairul Anus A, Saminathan S. Isolate resistance of Blastocystis hominis to metronidazole. Trop Med Int Health. 1999;4(4):274–7.PubMedCrossRef

31.

Dunn LA, Tan KS, Vanelle P, Juspin T, Crozet MD, Terme T, Upcroft P, Upcroft JA. Development of metronidazole-resistant lines of Blastocystis sp. Parasitol Res. 2012;111(1):441–50.PubMedCrossRef

32.

Batista L, Pérez Jove J, Rosinach M, Gonzalo V, Sainz E, Loras C, Forné M, Esteve M, Fernández-Bañares F. Low efficacy of metronidazole in the eradication of Blastocystis hominis in symptomatic patients: case series and systematic literature review. Gastroenterol Hepatol. 2017;40(6):381–7.PubMedCrossRef

33.

Rajamanikam A, Govind SK. Amoebic forms of Blastocystis spp.—evidence for a pathogenic role. Parasites Vectors. 2013;6(1):295.PubMedPubMedCentralCrossRef

34.

Thergarajan G, Govind SK, Bhassu S. In vitro and in vivo thermal stress induces proliferation of Blastocystis sp. Parasitol Res. 2018;117(1):177–87.PubMedCrossRef

35.

Zhang X, Qiao J, Wu X, Da R, Zhao L, Wei Z. In vitro culture of Blastocystis hominis in three liquid media and its usefulness in the diagnosis of blastocystosis. Int J Infect Dis. 2012;16(1):e23–8.PubMedCrossRef

36.

Scanlan PD, Shanahan F, O’Mahony C, Marchesi JR. Culture-independent analyses of temporal variation of the dominant fecal microbiota and targeted bacterial subgroups in Crohn’s disease. J Clin Microbiol. 2006;44(11):3980–8.PubMedPubMedCentralCrossRef

37.

Tannock GW, Munro K, Harmsen HJ, Welling GW, Smart J, Gopal PK. Analysis of the fecal microflora of human subjects consuming a probiotic product containing Lactobacillus rhamnosus DR20. Appl Environ Microbiol. 2000;66(6):2578–88.PubMedPubMedCentralCrossRef

38.

Vanhoutte T, Huys G, Brandt E, Swings J. Temporal stability analysis of the microbiota in human feces by denaturing gradient gel electrophoresis using universal and group-specific 16S rRNA gene primers. FEMS Microbiol Ecol. 2004;48(3):437–46.PubMedCrossRef

39.

Zoetendal EG, Akkermans AD, De Vos WM. Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol. 1998;64(10):3854–9.PubMedPubMedCentral

40.

Walter J, Hertel C, Tannock GW, Lis CM, Munro K, Hammes WP. Detection of Lactobacillus, Pediococcus, Leuconostoc, and Weissella species in human feces by using group-specific PCR primers and denaturing gradient gel electrophoresis. Appl Environ Microbiol. 2001;67(6):2578–85.PubMedPubMedCentralCrossRef

41.

Seto CT, Jeraldo P, Orenstein R, Chia N, DiBaise JK. Prolonged use of a proton pump inhibitor reduces microbial diversity: implications for Clostridium difficile susceptibility. Microbiome. 2014;2:42.PubMedPubMedCentralCrossRef

42.

Tsuda A, Suda W, Morita H, Takanashi K, Takagi A, Koga Y, Hattori M. Influence of proton-pump inhibitors on the luminal microbiota in the gastrointestinal tract. Clin Transl Gastroenterol. 2015;6:e89.PubMedPubMedCentralCrossRef

43.

Dodd HM, Gasson MJ. Bacteriocins of lactic acid bacteria. In: Gasson MJ, de Vos WM, editors. Genetics and biotechnology of lactic acid bacteria. London: Blackie Academic and Professional; 1994. p. 211–55.CrossRef

44.

Langhendries JP, Detry J, Van Hees J, Lamboray JM, Darimont J, Mozin MJ, Secretin MC, Senterre J. Effect of a fermented infant formula containing viable Bifidobacteria on the faecal flora composition and pH of healthy full-term infants. J Pediatr Gastroenterol Nutr. 1995;21(2):177–81.CrossRefPubMed

45.

Kailasapathy K, Chin J. Survival and therapeutic potential of probiotic organisms with reference to Lactobacillus acidophilus and Bifidobacterium spp. Immunol Cell Biol. 2000;78(1):80–8.PubMedCrossRef

46.

Rolfe RD. The role of probiotic cultures in the control of gastrointestinal health. J Nutr. 2000;130(2):396S–402S.PubMedCrossRef

47.

Beasley SB, Saris PEJ. Nisin-producing Lactococcus lactis strains isolated from human milk. Appl Environ Microbiol. 2004;70(8):5051–3.PubMedPubMedCentralCrossRef

48.

Siegumfeldt H, Björn Rechinger K, Jakobsen M. Dynamic changes of intracellular pH in individual lactic acid bacterium cells in response to a rapid drop in extracellular pH. Appl Environ Microbiol. 2000;66(6):2330–5.PubMedPubMedCentralCrossRef

49.

Zheng W, Zhang Y, Lu HM, Li DT, Zhang ZL, Tang ZX, Shi LE. Antimicrobial activity and safety evaluation of Enterococcus faecium KQ 2.6 isolated from peacock feces. BMC Biotechnology. 2015;15:30.PubMedPubMedCentralCrossRef

50.

Buydens P, Debeuckelaere S. Efficacy of SF 68 in the treatment of acute diarrhea. A placebo-controlled trial. Scand J Gastroenterol. 1996;31(9):887–91.PubMedCrossRef

51.

Wunderlich PF, Braun L, Fumagalli I, D’Apuzzo V, Heim F, Karly M, Lodi R, Politta G, Vonbank F, Zeltner L. Double-blind report on the efficacy of lactic acid-producing Enterococcus SF68 in the prevention of antibiotic-associated diarrhea and in the treatment of acute diarrhea. J Int Med Res. 1989;17(4):333–8.PubMedCrossRef

52.

Starke IC, Zentek J, Vahjen W. Effects of the probiotic Enterococcus faecium NCIMB 10415 on selected lactic acid bacteria and enterobacteria in co-culture. Benef Microbes. 2015;6(3):345–52.PubMedCrossRef

53.

Klingspor S, Bondzio A, Martens H, Aschenbach JR, Bratz K, Tedin K, Einspanier R, Lodemann U. Enterococcus faecium NCIMB 10415 modulates epithelial integrity, heat shock protein, and proinflammatory cytokine response in intestinal cells. Mediators Inflamm. 2015. https://doi.org/10.1155/2015/304149 (Epub 2015 Apr 8).PubMedPubMedCentralCrossRef

54.

Bednorz C, Guenther S, Oelgeschläger K, Kinnemann B, Pieper R, Hartmann S, Tedin K, Semmler T, Neumann K, Schierack P, Bethe A, Wieler LH. Feeding the probiotic Enterococcus faecium strain NCIMB 10415 to piglets specifically reduces the number of Escherichia coli pathotypes that adhere to the Gut Mucosa. Appl Environ Microbiol. 2013;79(24):7896–904.PubMedPubMedCentralCrossRef

55.

Russo TA, Johnson JR. Proposal for a new inclusive designation for extraintestinal pathogenic isolates of Escherichia coli: ExPEC. J Infect Dis. 2000;181(5):1753–4.PubMedCrossRef

56.

Kaper JB, Nataro JP, Mobley HL. Pathogenic Escherichia coli. Nat Rev Microbiol. 2004;2(2):123–40.PubMedCrossRef

57.

Ganas P, Liebhart D, Glösmann M, Hess C, Hess M. Escherichia coli strongly supports the growth of Histomonas meleagridis, in a monoxenic culture, without influence on its pathogenicity. Int J Parasitol. 2012;42(10):893–901.PubMedCrossRef

58.

Dunn LA, Boreham PF, Stenzel DJ. Ultrastructural variation of Blastocystis hominis stocks in culture. Int J Parasitol. 1989;19(1):43–56.PubMedCrossRef

59.

Rezania S, Amirmozaffari N, Tabarraei B, Jeddi-Tehrani M, Zarei O, Alizadeh R, Masjedian F, Zarnani AH. Extraction, purification and characterization of lipopolysaccharide from Escherichia coli and Salmonella typhi. Avicenna J Med Biotechnol. 2011;3(1):3–9.PubMedPubMedCentral

60.

Hager CL, Ghannoum MA. The mycobiome: role in health and disease, and as a potential probiotic target in gastrointestinal disease. Dig Liver Dis. 2017;49(11):1171–6.PubMedCrossRef

61.

Moyes DL, Wilson D, Richardson JP, Mogavero S, Tang SX, Wernecke J, Höfs S, Gratacap RL, Robbins J, Runglall M, Murciano C, Blagojevic M, Thavaraj S, Förster TM, Hebecker B, Kasper L, Vizcay G, Iancu SI, Kichik N, Häder A, Kurzai O, Luo T, Krüger T, Kniemeyer O, Cota E, Bader O, Wheeler RT, Gutsmann T, Hube B, Naglik JR. Candidalysin is a fungal peptide toxin critical for mucosal infection. Nature. 2016;532(7597):64–8.PubMedPubMedCentralCrossRef

62.

Konno N, Ishii M, Nagai A, Watanabe T, Ogasawara A, Mikami T, Matsumoto T. Mechanism of Candida albicans transformation in response to changes of pH. Biol Pharm Bull. 2006;29(5):923–6.PubMedCrossRef

63.

Sherrington SL, Sorsby E, Mahtey N, Kumwenda P, Lenardon MD, Brown I, Ballou ER, MacCallum DM, Hall RA. Adaptation of Candida albicans to environmental pH induces cell wall remodelling and enhances innate immune recognition. PLoS Pathog. 2017;13(5):e1006403.PubMedPubMedCentralCrossRef

64.

Morales DK, Hogan DA. Candida albicans interactions with bacteria in the context of human health and disease. PLoS Pathog. 2010;6(4):e1000886.PubMedPubMedCentralCrossRef

Title: The influence of probiotic bacteria and human gut microorganisms causing opportunistic infections on Blastocystis ST3
Authors: M. Lepczyńska
E. Dzika
Publication date: 01-12-2019
Publisher: BioMed Central
Keywords: Candida Balanitis
Candida Albicans
Probiotics
Respiratory Microbiota
Protozoa
Published in: Gut Pathogens / Issue 1/2019
Electronic ISSN: 1757-4749
DOI: https://doi.org/10.1186/s13099-019-0287-8

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The influence of probiotic bacteria and human gut microorganisms causing opportunistic infections on Blastocystis ST3

Abstract

Background

Results

Conclusions

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Abstract

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