Skip to main content
Top
Published in: European Journal of Clinical Microbiology & Infectious Diseases 9/2016

01-09-2016 | Original Article

Associations between common intestinal parasites and bacteria in humans as revealed by qPCR

Authors: L. O’Brien Andersen, A. B. Karim, H. M. Roager, L. K. Vigsnæs, K. A. Krogfelt, T. R. Licht, C. R. Stensvold

Published in: European Journal of Clinical Microbiology & Infectious Diseases | Issue 9/2016

Login to get access

Abstract

Several studies have shown associations between groups of intestinal bacterial or specific ratios between bacterial groups and various disease traits. Meanwhile, little is known about interactions and associations between eukaryotic and prokaryotic microorganisms in the human gut. In this work, we set out to investigate potential associations between common single-celled parasites such as Blastocystis spp. and Dientamoeba fragilis and intestinal bacteria. Stool DNA from patients with intestinal symptoms were selected based on being Blastocystis spp.-positive (B+)/negative (B−) and D. fragilis-positive (D+)/negative (D−), and split into four groups of 21 samples (B+ D+, B+ D−, B− D+, and B− D−). Quantitative PCR targeting the six bacterial taxa Bacteroides, Prevotella, the butyrate-producing clostridial clusters IV and XIVa, the mucin-degrading Akkermansia muciniphila, and the indigenous group of Bifidobacterium was subsequently performed, and the relative abundance of these bacteria across the four groups was compared. The relative abundance of Bacteroides in B– D– samples was significantly higher compared with B+ D− and B+ D+ samples (P < 0.05 and P < 0.01, respectively), and this association was even more significant when comparing all parasite-positive samples with parasite-negative samples (P < 0.001). Additionally, our data revealed that a low abundance of Prevotella and a higher abundance of Clostridial cluster XIVa was associated with parasite-negative samples (P < 0.05 and P < 0.01, respectively). Our data support the theory that Blastocystis alone or combined with D. fragilis is associated with gut microbiota characterized by low relative abundances of Bacteroides and Clostridial cluster XIVa and high levels of Prevotella.
Literature
1.
go back to reference Zoetendal EG, Akkermans AD, De Vos WM (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64:3854–3859PubMedPubMedCentral Zoetendal EG, Akkermans AD, De Vos WM (1998) Temperature gradient gel electrophoresis analysis of 16S rRNA from human fecal samples reveals stable and host-specific communities of active bacteria. Appl Environ Microbiol 64:3854–3859PubMedPubMedCentral
3.
go back to reference Jiménez E, Fernández L, Marín ML, Martín R, Odriozola JM, Nueno-Palop C, Narbad A, Olivares M, Xaus J, Rodríguez JM (2005) Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 51:270–274CrossRefPubMed Jiménez E, Fernández L, Marín ML, Martín R, Odriozola JM, Nueno-Palop C, Narbad A, Olivares M, Xaus J, Rodríguez JM (2005) Isolation of commensal bacteria from umbilical cord blood of healthy neonates born by cesarean section. Curr Microbiol 51:270–274CrossRefPubMed
4.
5.
go back to reference Aziz Q, Doré J, Emmanuel A, Guarner F, Quigley EM (2013) Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol Motil 25:4–15CrossRefPubMed Aziz Q, Doré J, Emmanuel A, Guarner F, Quigley EM (2013) Gut microbiota and gastrointestinal health: current concepts and future directions. Neurogastroenterol Motil 25:4–15CrossRefPubMed
6.
7.
10.
go back to reference Lukeš J, Stensvold CR, Jirků-Pomajbíková K, Wegener Parfrey L (2015) Are human intestinal eukaryotes beneficial or commensals? PLoS Pathog 11:e1005039CrossRefPubMedPubMedCentral Lukeš J, Stensvold CR, Jirků-Pomajbíková K, Wegener Parfrey L (2015) Are human intestinal eukaryotes beneficial or commensals? PLoS Pathog 11:e1005039CrossRefPubMedPubMedCentral
11.
go back to reference Krogsgaard LR, Engsbro AL, Stensvold CR, Nielsen HV, Bytzer P (2015) The prevalence of intestinal parasites is not greater among individuals with irritable bowel syndrome: a population-based case–control study. Clin Gastroenterol Hepatol 13:507.e502–513.e502CrossRef Krogsgaard LR, Engsbro AL, Stensvold CR, Nielsen HV, Bytzer P (2015) The prevalence of intestinal parasites is not greater among individuals with irritable bowel syndrome: a population-based case–control study. Clin Gastroenterol Hepatol 13:507.e502–513.e502CrossRef
12.
go back to reference Rossen NG, Bart A, Verhaar N, van Nood E, Kootte R, de Groot PF, D’Haens GR, Ponsioen CY, van Gool T (2015) Low prevalence of Blastocystis sp. in active ulcerative colitis patients. Eur J Clin Microbiol Infect Dis 34:1039–1044CrossRefPubMedPubMedCentral Rossen NG, Bart A, Verhaar N, van Nood E, Kootte R, de Groot PF, D’Haens GR, Ponsioen CY, van Gool T (2015) Low prevalence of Blastocystis sp. in active ulcerative colitis patients. Eur J Clin Microbiol Infect Dis 34:1039–1044CrossRefPubMedPubMedCentral
13.
go back to reference Petersen AM, Stensvold CR, Mirsepasi H, Engberg J, Friis-Møller A, Porsbo LJ, Hammerum AM, Nordgaard-Lassen I, Nielsen HV, Krogfelt KA (2013) Active ulcerative colitis associated with low prevalence of Blastocystis and Dientamoeba fragilis infection. Scand J Gastroenterol 48:638–639CrossRefPubMed Petersen AM, Stensvold CR, Mirsepasi H, Engberg J, Friis-Møller A, Porsbo LJ, Hammerum AM, Nordgaard-Lassen I, Nielsen HV, Krogfelt KA (2013) Active ulcerative colitis associated with low prevalence of Blastocystis and Dientamoeba fragilis infection. Scand J Gastroenterol 48:638–639CrossRefPubMed
14.
go back to reference Clemente JC, Ursell LK, Parfrey LW, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270CrossRefPubMed Clemente JC, Ursell LK, Parfrey LW, Knight R (2012) The impact of the gut microbiota on human health: an integrative view. Cell 148:1258–1270CrossRefPubMed
15.
go back to reference Andersen LO, Bonde I, Nielsen HB, Stensvold CR (2015) A retrospective metagenomics approach to studying Blastocystis. FEMS Microbiol Ecol 91. doi:10.1093/femsec/fiv072 Andersen LO, Bonde I, Nielsen HB, Stensvold CR (2015) A retrospective metagenomics approach to studying Blastocystis. FEMS Microbiol Ecol 91. doi:10.​1093/​femsec/​fiv072
16.
go back to reference Stensvold CR, Ahmed UN, Andersen LO, Nielsen HV (2012) Development and evaluation of a genus-specific, probe-based, internal-process-controlled real-time PCR assay for sensitive and specific detection of Blastocystis spp. J Clin Microbiol 50:1847–1851CrossRefPubMedPubMedCentral Stensvold CR, Ahmed UN, Andersen LO, Nielsen HV (2012) Development and evaluation of a genus-specific, probe-based, internal-process-controlled real-time PCR assay for sensitive and specific detection of Blastocystis spp. J Clin Microbiol 50:1847–1851CrossRefPubMedPubMedCentral
17.
go back to reference Verweij JJ, Mulder B, Poell B, van Middelkoop D, Brienen EA, van Lieshout L (2007) Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Mol Cell Probes 21:400–404CrossRefPubMed Verweij JJ, Mulder B, Poell B, van Middelkoop D, Brienen EA, van Lieshout L (2007) Real-time PCR for the detection of Dientamoeba fragilis in fecal samples. Mol Cell Probes 21:400–404CrossRefPubMed
18.
go back to reference Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035S–1045SPubMed Mackie RI, Sghir A, Gaskins HR (1999) Developmental microbial ecology of the neonatal gastrointestinal tract. Am J Clin Nutr 69:1035S–1045SPubMed
19.
go back to reference Tannock GW, Tilsala-Timisjarvi A, Rodtong S, Ng J, Munro K, Alatossava T (1999) Identification of Lactobacillus isolates from the gastrointestinal tract, silage, and yoghurt by 16S-23S rRNA gene intergenic spacer region sequence comparisons. Appl Environ Microbiol 65:4264–4267PubMedPubMedCentral Tannock GW, Tilsala-Timisjarvi A, Rodtong S, Ng J, Munro K, Alatossava T (1999) Identification of Lactobacillus isolates from the gastrointestinal tract, silage, and yoghurt by 16S-23S rRNA gene intergenic spacer region sequence comparisons. Appl Environ Microbiol 65:4264–4267PubMedPubMedCentral
20.
go back to reference Bergström A, Licht TR, Wilcks A, Andersen JB, Schmidt LR, Grønlund HA, Vigsnaes LK, Michaelsen KF, Bahl MI (2012) Introducing GUt low-density array (GULDA): a validated approach for qPCR-based intestinal microbial community analysis. FEMS Microbiol Lett 337:38–47CrossRefPubMed Bergström A, Licht TR, Wilcks A, Andersen JB, Schmidt LR, Grønlund HA, Vigsnaes LK, Michaelsen KF, Bahl MI (2012) Introducing GUt low-density array (GULDA): a validated approach for qPCR-based intestinal microbial community analysis. FEMS Microbiol Lett 337:38–47CrossRefPubMed
21.
22.
go back to reference Blair RC, Higgins JJ (1980) A comparison of the power of Wilcoxon’s rank-sum statistic to that of Student’s t statistic under various nonnormal distributions. J Educ Stat 5:24CrossRef Blair RC, Higgins JJ (1980) A comparison of the power of Wilcoxon’s rank-sum statistic to that of Student’s t statistic under various nonnormal distributions. J Educ Stat 5:24CrossRef
23.
go back to reference Claesson MJ, Cusack S, O’Sullivan O et al (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 108(Suppl 1):4586–4591CrossRefPubMed Claesson MJ, Cusack S, O’Sullivan O et al (2011) Composition, variability, and temporal stability of the intestinal microbiota of the elderly. Proc Natl Acad Sci USA 108(Suppl 1):4586–4591CrossRefPubMed
24.
go back to reference Roager HM, Licht TR, Poulsen SK, Larsen TM, Bahl MI (2014) Microbial enterotypes, inferred by the prevotella-to-bacteroides ratio, remained stable during a 6-month randomized controlled diet intervention with the new nordic diet. Appl Environ Microbiol 80:1142–1149CrossRefPubMedPubMedCentral Roager HM, Licht TR, Poulsen SK, Larsen TM, Bahl MI (2014) Microbial enterotypes, inferred by the prevotella-to-bacteroides ratio, remained stable during a 6-month randomized controlled diet intervention with the new nordic diet. Appl Environ Microbiol 80:1142–1149CrossRefPubMedPubMedCentral
25.
go back to reference Bergström A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, Mølgaard C, Michaelsen KF, Licht TR (2014) Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 80:2889–2900CrossRefPubMedPubMedCentral Bergström A, Skov TH, Bahl MI, Roager HM, Christensen LB, Ejlerskov KT, Mølgaard C, Michaelsen KF, Licht TR (2014) Establishment of intestinal microbiota during early life: a longitudinal, explorative study of a large cohort of Danish infants. Appl Environ Microbiol 80:2889–2900CrossRefPubMedPubMedCentral
26.
go back to reference Stensvold CR, Smith HV, Nagel R, Olsen KE, Traub RJ (2010) Eradication of Blastocystis carriage with antimicrobials: reality or delusion? J Clin Gastroenterol 44:85–90CrossRefPubMed Stensvold CR, Smith HV, Nagel R, Olsen KE, Traub RJ (2010) Eradication of Blastocystis carriage with antimicrobials: reality or delusion? J Clin Gastroenterol 44:85–90CrossRefPubMed
Metadata
Title
Associations between common intestinal parasites and bacteria in humans as revealed by qPCR
Authors
L. O’Brien Andersen
A. B. Karim
H. M. Roager
L. K. Vigsnæs
K. A. Krogfelt
T. R. Licht
C. R. Stensvold
Publication date
01-09-2016
Publisher
Springer Berlin Heidelberg
Published in
European Journal of Clinical Microbiology & Infectious Diseases / Issue 9/2016
Print ISSN: 0934-9723
Electronic ISSN: 1435-4373
DOI
https://doi.org/10.1007/s10096-016-2680-2

Other articles of this Issue 9/2016

European Journal of Clinical Microbiology & Infectious Diseases 9/2016 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.