Potential contribution of the uterine microbiome in the development of endometrial cancer View Full Text


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Article Info

DATE

2016-11-25

AUTHORS

Marina R. S. Walther-António, Jun Chen, Francesco Multinu, Alexis Hokenstad, Tammy J. Distad, E. Heidi Cheek, Gary L. Keeney, Douglas J. Creedon, Heidi Nelson, Andrea Mariani, Nicholas Chia

ABSTRACT

BackgroundEndometrial cancer studies have led to a number of well-defined but mechanistically unconnected genetic and environmental risk factors. One of the emerging modulators between environmental triggers and genetic expression is the microbiome. We set out to inquire about the composition of the uterine microbiome and its putative role in endometrial cancer.MethodsWe undertook a study of the microbiome in samples taken from different locations along the female reproductive tract in patients with endometrial cancer (n = 17), patients with endometrial hyperplasia (endometrial cancer precursor, n = 4), and patients afflicted with benign uterine conditions (n = 10). Vaginal, cervical, Fallopian, ovarian, peritoneal, and urine samples were collected aseptically both in the operating room and the pathology laboratory. DNA extraction was followed by amplification and high-throughput next generation sequencing (MiSeq) of the 16S rDNA V3-V5 region to identify the microbiota present. Microbiota data were summarized using both α-diversity to reflect species richness and evenness within bacterial populations and β-diversity to reflect the shared diversity between bacterial populations. Statistical significance was determined through the use of multiple testing, including the generalized mixed-effects model.ResultsThe microbiome sequencing (16S rDNA V3-V5 region) revealed that the microbiomes of all organs (vagina, cervix, Fallopian tubes, and ovaries) are significantly correlated (p < 0.001) and that there is a structural microbiome shift in the cancer and hyperplasia cases, distinguishable from the benign cases (p = 0.01). Several taxa were found to be significantly enriched in samples belonging to the endometrial cancer cohort: Firmicutes (Anaerostipes, ph2, Dialister, Peptoniphilus, 1–68, Ruminococcus, and Anaerotruncus), Spirochaetes (Treponema), Actinobacteria (Atopobium), Bacteroidetes (Bacteroides and Porphyromonas), and Proteobacteria (Arthrospira). Of particular relevance, the simultaneous presence of Atopobium vaginae and an uncultured representative of the Porphyromonas sp. (99 % match to P. somerae) were found to be associated with disease status, especially if combined with a high vaginal pH (>4.5).ConclusionsOur results suggest that the detection of A. vaginae and the identified Porphyromonas sp. in the gynecologic tract combined with a high vaginal pH is statistically associated with the presence of endometrial cancer. Given the documented association of the identified microorganisms with other pathologies, these findings raise the possibility of a microbiome role in the manifestation, etiology, or progression of endometrial cancer that should be further investigated. More... »

PAGES

122

References to SciGraph publications

Identifiers

URI

http://scigraph.springernature.com/pub.10.1186/s13073-016-0368-y

DOI

http://dx.doi.org/10.1186/s13073-016-0368-y

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https://app.dimensions.ai/details/publication/pub.1047439451

PUBMED

https://www.ncbi.nlm.nih.gov/pubmed/27884207


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29 schema:description BackgroundEndometrial cancer studies have led to a number of well-defined but mechanistically unconnected genetic and environmental risk factors. One of the emerging modulators between environmental triggers and genetic expression is the microbiome. We set out to inquire about the composition of the uterine microbiome and its putative role in endometrial cancer.MethodsWe undertook a study of the microbiome in samples taken from different locations along the female reproductive tract in patients with endometrial cancer (n = 17), patients with endometrial hyperplasia (endometrial cancer precursor, n = 4), and patients afflicted with benign uterine conditions (n = 10). Vaginal, cervical, Fallopian, ovarian, peritoneal, and urine samples were collected aseptically both in the operating room and the pathology laboratory. DNA extraction was followed by amplification and high-throughput next generation sequencing (MiSeq) of the 16S rDNA V3-V5 region to identify the microbiota present. Microbiota data were summarized using both α-diversity to reflect species richness and evenness within bacterial populations and β-diversity to reflect the shared diversity between bacterial populations. Statistical significance was determined through the use of multiple testing, including the generalized mixed-effects model.ResultsThe microbiome sequencing (16S rDNA V3-V5 region) revealed that the microbiomes of all organs (vagina, cervix, Fallopian tubes, and ovaries) are significantly correlated (p < 0.001) and that there is a structural microbiome shift in the cancer and hyperplasia cases, distinguishable from the benign cases (p = 0.01). Several taxa were found to be significantly enriched in samples belonging to the endometrial cancer cohort: Firmicutes (Anaerostipes, ph2, Dialister, Peptoniphilus, 1–68, Ruminococcus, and Anaerotruncus), Spirochaetes (Treponema), Actinobacteria (Atopobium), Bacteroidetes (Bacteroides and Porphyromonas), and Proteobacteria (Arthrospira). Of particular relevance, the simultaneous presence of Atopobium vaginae and an uncultured representative of the Porphyromonas sp. (99 % match to P. somerae) were found to be associated with disease status, especially if combined with a high vaginal pH (>4.5).ConclusionsOur results suggest that the detection of A. vaginae and the identified Porphyromonas sp. in the gynecologic tract combined with a high vaginal pH is statistically associated with the presence of endometrial cancer. Given the documented association of the identified microorganisms with other pathologies, these findings raise the possibility of a microbiome role in the manifestation, etiology, or progression of endometrial cancer that should be further investigated.
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35 schema:keywords A. vaginae
36 Actinobacteria
37 Atopobium vaginae
38 Bacteroidetes
39 ConclusionsOur results
40 DNA extraction
41 Firmicutes
42 MethodsWe
43 Porphyromonas sp
44 Proteobacteria
45 V3-V5 region
46 amplification
47 association
48 bacterial populations
49 benign cases
50 benign uterine conditions
51 cancer
52 cancer cohort
53 cancer studies
54 cases
55 cohort
56 composition
57 conditions
58 contribution
59 data
60 detection
61 development
62 different locations
63 disease status
64 diversity
65 endometrial cancer
66 endometrial cancer cohort
67 endometrial hyperplasia
68 environmental risk factors
69 environmental triggers
70 etiology
71 evenness
72 expression
73 extraction
74 factors
75 fallopian
76 female reproductive tract
77 findings
78 generation sequencing
79 genetic expression
80 gynecologic tract
81 high vaginal pH
82 high-throughput next-generation sequencing
83 hyperplasia
84 hyperplasia cases
85 laboratory
86 location
87 manifestations
88 microbiome
89 microbiome sequencing
90 microbiome shifts
91 microbiome's role
92 microbiota data
93 microbiota present
94 microorganisms
95 mixed effects models
96 model
97 modulator
98 multiple testing
99 next-generation sequencing
100 number
101 operating room
102 organs
103 pH
104 particular relevance
105 pathology
106 pathology laboratory
107 patients
108 peritoneal
109 population
110 possibility
111 potential contribution
112 presence
113 present
114 progression
115 putative role
116 region
117 relevance
118 representatives
119 reproductive tract
120 results
121 richness
122 risk factors
123 role
124 room
125 samples
126 sequencing
127 shift
128 significance
129 simultaneous presence
130 sp
131 species richness
132 spirochaetes
133 statistical significance
134 status
135 study
136 taxa
137 testing
138 tract
139 triggers
140 uncultured representatives
141 urine samples
142 use
143 uterine conditions
144 uterine microbiome
145 vagina
146 vaginal pH
147 α-diversity
148 β-diversity
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