Annemarie Boleij

Radboud University Nijmegen

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Bas E. Dutilh

Utrecht University

Harold Tjalsma

Radboud University Nijmegen

Daniel Garza

Université Paris-Saclay

Martijn A. Huynen

Radboud University Nijmegen

Irıs D. Nagtegaal

Radboud University Nijmegen

Rahwa Taddese

Radboud University Nijmegen

Rian Roelofs

Radboud University Medical Center

Carlijn E. Bruggeling

Radboud University Medical Center

Ikuko Kato

Wayne State University

Dorine W. Swinkels

Radboud University Medical Center

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Radboud University Nijmegen

175

Radboud University Medical Center

135

University Medical Center

Radboud Institute for Molecular Life Sciences

Johns Hopkins University

Utrecht University

Johns Hopkins Medicine

Instituto de Salud Carlos III

Centro de Investigación Biomédica en Red de Epidemiología y Salud Pública

University Medical Center Utrecht

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Clinical Importance of Streptococcus gallolyticus Infection Among Colorectal Cancer Patients: Systematic Review and Meta-analysis

Clinical Infectious Diseases (2011)

Annemarie Boleij Marleen M. H. J. van Gelder Dorine W. Swinkels Harold Tjalsma

Streptococcus bovis has long been associated with colorectal cancer (CRC). However, not all genospecies are as closely related to CRC. With this systematic review, we aim to increase the awareness of the association between S. bovis biotype I (Streptococcus gallolyticus) and CRC and urge for uniform molecular microbiological classification.In January 2011, the PubMed database was searched for all studies that investigated the association between S. bovis, infective endocarditis (IE), and CRC. A total of 191 studies were screened for eligibility and yielded 52 case reports and 31 case series, of which 11 were used for meta-analysis on the association between S. bovis biotype, IE, and adenomas/carcinomas (CRC).Among the S. bovis-infected patients who underwent colonic evaluation, the median percentage of patients who had concomitant adenomas/carcinomas was 60% (interquartile range, 22%), which largely exceeds the disease rate reported in the general asymptomatic population. Meta-analysis showed that patients with S. bovis biotype I infection had a strongly increased risk of having CRC (pooled odds ratio [OR], 7.26; 95% confidence interval [CI], 3.94-13.36) and IE (pooled OR, 16.61; 95% CI, 8.85-31.16), compared with S. bovis biotype II-infected patients. Notably, CRC occurred more often among patients with S. bovis IE than among patients with S. bovis infection at other sites (pooled OR, 3.72; 95% CI, 2.03-6.81).Our meta-analysis clearly indicates that S. bovis should no longer be regarded as a single species in clinical practice, because S. gallolyticus (S. bovis biotype I) infection, in particular, has an unambiguous association with CRC.

Streptococcus bovis

10.1093/cid/cir609

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Citations (351)

Towards the human colorectal cancer microbiome

F1000Research (2012)

Bas E. Dutilh Julian R. Marchesi Annemarie Boleij Harold Tjalsma

Open peer review

Gut microbiome

10.7490/f1000research.1092048.1

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Citations (3)

Association of Streptococcus gallolyticus subspecies gallolyticus with colorectal cancer: Serological evidence

International Journal of Cancer (2015)

Julia Butt Beatriz Romero‐Hernández Beatriz Pérez‐Gómez Martina Willhauck‐Fleckenstein Dana Holzinger

The colonic opportunist Streptococcus gallolyticus subspecies gallolyticus (SGG) is potentially associated with colorectal cancer (CRC). Large‐scale seroepidemiological data for SGG antibodies and their possible association with CRC is currently missing. Associations between CRC and antibody responses to SGG were examined in 576 CRC cases and 576 controls matched by sex, age and province from a population‐based multicase–control project (MCC‐Spain). MCC‐Spain was conducted between 2008 and 2013 in 12 Spanish provinces. Antibody responses to recombinant affinity‐purified SGG pilus proteins Gallo1569, 2039, 2178 and 2179 were analysed by multiplex serology. Polyomavirus (PyV) JC VP1 and PyV 6 VP1 proteins served as disease‐specificity controls. In the control population, antibody responses to pilus proteins were mostly weak. Antibody responses to individual pilus proteins Gallo2039 (OR: 1.58, 95% CI: 1.09–2.28), Gallo2178 (OR: 1.58, 95% CI: 1.09–2.30) and Gallo2179 (OR: 1.45, 95% CI: 1.00–2.11) were significantly associated with CRC risk. The association was stronger for positivity to two or more pilus proteins of Gallo1569, Gallo2178 and Gallo2179 (OR:1.93, 95% CI: 1.04–3.56) and for double‐positivity to Gallo2178 and Gallo2179 (OR: 3.54, 95% CI: 1.49–8.44). The association between SGG infection and CRC risk was stronger among individuals younger than 65 years. For the first time we demonstrated a statistically significant association of exposure to SGG antigens and CRC in a large seroepidemiological study. These results should stimulate further studies on the role of SGG in CRC pathogenesis.

Multiplex

10.1002/ijc.29914

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Citations (46)

The itinerary of Streptococcus gallolyticus infection in patients with colonic malignant disease

The Lancet Infectious Diseases (2013)

Annemarie Boleij Harold Tjalsma

Streptococcus bovis

Dysbiosis

Flora

10.1016/s1473-3099(13)70107-5

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Citations (140)

Optimized bacterial DNA isolation method for microbiome analysis of human tissues

Zenodo (CERN European Organization for Nuclear Research) (2021)

Carlijn E. Bruggeling Daniel Garza Soumia Achiouti Wouter Mes Bas E. Dutilh

Supplementary Data S1: Data of 508 bacterial metagenomes isolated from human colon biopsies (shotgun metagenomic sequencing) Supplementary Data S2: Data of 15 bacterial metagenomes isolated from human colon biopsies (16S rRNA versus shotgun metagenomic sequencing)

Isolation

10.5281/zenodo.4678215

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Citations (0)

Additional file 9 of Nutrition or nature: using elementary flux modes to disentangle the complex forces shaping prokaryote pan-genomes

Figshare (2022)

Daniel Garza F. A. Bastiaan von Meijenfeldt Bram van Dijk Annemarie Boleij Martijn A. Huynen

Additional file 9: Table S4. Environment-driven reaction scores (EDS) for all 46 prokaryote families.

Prokaryote

10.6084/m9.figshare.20499832

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Maag-, darm- en leverziekten

Bohn Stafleu van Loghum eBooks (2022)

Tanya Bisseling Sander van der Marel Annemarie Boleij Carlijn Bruggeling Menso Westerouen van Meeteren

10.1007/978-90-368-2761-4_7

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Citations (1)

Association between Streptococcus bovis and Colon Cancer

Journal of Clinical Microbiology (2009)

Annemarie Boleij Renée M. J. Schaeps Harold Tjalsma

We read with great interest the article by Marcella Beck and colleagues (1). We fully support their recommendation that proper distinction between the “Streptococcus bovis” strains belonging to Streptococcus gallolyticus and Streptococcus infantarius (previously biotypes I and II/2, respectively) should be made in future studies to obtain a clear picture of the disease associations of these opportunistic pathogens; above all, because proper bacterial classification and subsequent recognition of their association with colon cancer can be a life-saving event for S. bovis-infected individuals with undiagnosed colon cancer (4, 5, 8). We were therefore somewhat puzzled by the authors’ conclusion that the association between S. bovis bacteremia and colon cancer (7%) may not be as strong as previously thought. Beck and colleagues based their conclusion on the finding that 3 out of 46 individuals with S. bovis bacteremia presented with a coincidental colon carcinoma. The authors recognize, however, that only 15 of these 46 patients underwent full bowel examination and that in the other patients asymptomatic colon tumors could be missed. In two cited papers, Ruoff et al. (6) and Corredoira et al. (2) report respective associations of 100% and 57% for the association of S. bovis biotype I and colon cancer in patients that underwent colonoscopy. Importantly, these associations also took into account the presence of premalignant adenomas that are generally regarded as (earlystage) precursors of carcinomas. In fact, Corredoira et al. (3)

Streptococcus bovis

Bacteremia

10.1128/jcm.01755-08

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Citations (71)

Navigating beyond associations: Opportunities to establish causal relationships between the gut microbiome and colorectal carcinogenesis

Cell Host & Microbe (2024)

Floor S Baas Nele Brusselaers Irıs D. Nagtegaal Lars Engstrand Annemarie Boleij

Gut microbiome

10.1016/j.chom.2024.07.008

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Abstract PR01: Right-sided colonic biofilms are associated with adenoma formation in patients with Lynch syndrome

Cancer Research (2020)

Carlijn E. Bruggeling Vera Witjes Daniel Garza Milou Fransen Joyce Krekels

Abstract Colonic bacterial biofilms are an emerging manifestation in colorectal cancer (CRC); they exhibit carcinogenic properties and are frequently present on right-sided cancerous lesions. Whether bacterial biofilms propose a risk factor for early carcinogenesis in humans is yet unresolved. Therefore, we studied bacterial biofilms in tandem with adenoma formation in patients with Lynch syndrome (LS). LS patients carry a pathogenic germline variant in one of the DNA mismatch repair (MMR) genes, resulting in a variable predisposition to develop colonic cancerous lesions. A total of 100 LS patients were included in our study, consisting of 23 MLH1, 24 MSH2, 36 MSH6, and 17 PMS2 MMR variants. During regular screening colonoscopies, normal-appearing forceps biopsies were taken from colon ascendens (right colon) and descendens (left colon). Biopsies were screened for bacterial biofilms using fluorescent in situ hybridization by targeting bacterial 16s rRNA. The frequency of colorectal adenomas (tubular adenomas and [tubulo]villous adenomas) before and during colonoscopy was registered. Overall, 60% of patients presented with a biofilm, of which most were right-sided (right-sided: 25%, both sides: 21%, left-sided: 14%). Interestingly, adenomas were more frequently present in patients with a right-sided biofilm (right-sided: 64%, both sides: 58%) than in patients with a left-sided biofilm (29%) or no biofilm (38%). The occurrence of bacterial biofilms was not correlated with age, BMI, or MMR-variant. Statistical analysis revealed that right-sided bacterial biofilms correlated with right-sided adenomas (Pearson: 0.272, p=0.007) and left-sided adenomas (Pearson: 0.227, p=0.026), while left-sided biofilms were not correlated with left- or right-sided adenomas (Pearson: 0.037, p=0.718 and -.127, p=.213). To model the probability of right-sided adenoma formation, we performed a binary logistic regression analysis and found that age (odds ratio: 1.065 [CI: 1.024; 1.108, p=0.002]) and right-sided biofilms (odds ratio: 3.020 [CI: 1.151; 7.926, p=0.025]) significantly contributed. Our data suggest that right-sided bacterial biofilms are a hallmark for high-risk LS patients and may play a role in early carcinogenesis. This abstract is also being presented as Poster A06. Citation Format: Carlijn Bruggeling, Vera Witjes, Daniel Garza, Milou Fransen, Joyce Krekels, Tanya Bisseling, Mariëtte van Kouwen, Nicoline Hoogerbrugge, Sebastian Lücker, Bas Dutilh, Iris Nagtegaal, Annemarie Boleij. Right-sided colonic biofilms are associated with adenoma formation in patients with Lynch syndrome [abstract]. In: Proceedings of the AACR Special Conference on the Microbiome, Viruses, and Cancer; 2020 Feb 21-24; Orlando, FL. Philadelphia (PA): AACR; Cancer Res 2020;80(8 Suppl):Abstract nr PR01.

Tubular adenoma

Lynch Syndrome

Villous adenoma

MLH1

MSH6

MSH2

PMS2

10.1158/1538-7445.mvc2020-pr01

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