Characteristics of Vaginal Microbiome in Women with Pelvic Inflammatory Disease in Korea

SUKYUNG KIM; HOONHEE SEO; MD ABDUR RAHIM; HANIEH TAJDOZIAN; YUN-SOOK KIM; HO-YEON SONG

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Characteristics of Vaginal Microbiome in Women with Pelvic Inflammatory Disease in Korea

| 17 sept. 2021

Polish Journal of Microbiology

Édition 70 (2021): Edition 3 (September 2021)

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Article Category: original-paper

Publié en ligne: 17 sept. 2021

Pages: 345 - 357

Reçu: 30 avr. 2021

Accepté: 14 juil. 2021

DOI: https://doi.org/10.33073/pjm-2021-033

Mots clés
vaginal microflora, pelvic inflammatory disease, 16S rRNA amplicon sequencing, premenopausal, Korean

© 2021 Sukyung Kim et al., published by Sciendo

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Genus-level vaginal microbiome compositions in women of control group and PID patients. Data for minor orders with a relative abundance < 1% are not shown.

Boxplot of Species richness indices.A) Ace (p = 0.274), B) Chao1 (p = 0.289), C) Jackknife (p = 0.267) indices and D) The number of OTUs (p = 0.299) reflects the diversity of OTU in samples. Bars indicate the median, and the hinges represent the lower and upper quartiles. In panels (A-D), no statistically significant differences were observed between the normal control women and PID patients. The Wilcoxon rank-sum test was used to determine the species richness.

Boxplot of Species diversity indices.NP Shannon (p = 0.251), Shannon (p = 0.091), Simpson (p = 0.007), Phylogenetic diversity (p = 0.373) reflect the diversity of OTU in samples. Bars indicate the median, and the hinges represent the lower and upper quartiles. The Wilcoxon rank-sum test was used to determine the diversity index. *p < 0.05; **p < 0.01

Beta diversity of microbial communities based on Jensen-Shannon divergence, Bray-Curtis, Generalized UniFrac, and UniFrac.A) PCoA plots were produced as an ellipse in two dimensions based on a 95% confidence interval. B) PCoA plots were also presented in 3D. The blue/purple color indicates normal control women, and the light green/red color indicates PID patients, respectively. C) Permutational multivariate analysis of variance (PERMANOVA) results demonstrated the beta set-significance between the PID patient and normal control women groups. **p < 0.01.

Clustering using the Unweighted Pair Group Method with Arithmetic mean (UPGMA).

Taxonomic abundance with an LDA effect size of more than 5.

The relative level of organic acids in normal control women and PID patients. In the PID patient group, lactate was significantly decreased compared to the control group, whereas the concentrations of 4-hydroxyphenylacetate and 2-hydroxylsovalerate were significantly increased. *p < 0.05; **p < 0.01.

Distributions of bacterial community at different taxonomic levels (phylum, class, order, and family).

Phylum	Con.	PID	Class	Con.	PID	Order	Con.	PID	Family	Con.	PID
									Lactobacillaceae	63.7	35.8
						Lactobacillales	74.5	50.2	Enterococcaceae	8.1	13.4
Firmicutes	79.4	56.9	Bacilli	77.7	53.7				Streptococcaceae	2.6	0
						Bacillales	3.1	3.4	Staphylococcaceae	3.1	3.1
			Tissierellia	1.0	1.5	Tissierellales	1.0	1.5	Peptoniphilaceae	1.0	1.5
Actinobacteria	13.0	23.2	Actinobacteria	10.7	16.7	Bifidobacteriales	9.8	15.8	Bifidobacteriaceae	9.8	15.8
Actinobacteria	13.0	23.2	Coriobacteriia	2.3	6.6	Coriobacteriales	2.3	6.6	Coriobacteriaceae	2.3	6.6
			Gammaproteobacteria	4.1	11.0	Pseudomonadales	2.7	1.5	Moraxellaceae	2.4	0
Proteobacteria	4.6	12.8	Gammaproteobacteria	4.1	11.0	Enterobacterales	1.4	9.4	Enterobacteriaceae	0	9.2
			Betaproteobacteria	0	1.6	Burkholderiales	0	1.6	Oxalobacteraceae	0	1.3
Bacteroidetes	1.4	4.7	Bacteroidia	1.3	4.6	Bacteroidales	1.3	4.6	Prevotellaceae	1.2	3.7
Fusobacteria	1.2	2.4	Fusobacteria	1.2	2.4	Fusobacteriales	1.2	2.4	Leptotrichiaceae	1.2	2.2

Identification of microbes using STD multiplex PCR and culture method for PID patients.

No.	STD PCR method								Culture method
No.	MH	UP	UU	GV	CT	NG	TV	CA	Culture method
1	+	–	–	+	–	–	–	–	–
2	+	+	–	+	+	–	–	–	–
3	–	–	+	+	–	–	–	–	–
4	–	+	–	+	–	–	–	–	–
5	–	–	+	+	–	–	–	–	–
6	–	+	–	+	–	–	–	–	–
7	–	–	+	+	–	–	–	–	–
8	+	+	–	+	+	+	–	–	–
9	–	–	–	+	+	–	+	–	–
10	–	–	+	+	–	–	–	–	–
11	+	+	–	+	+	–	–	–	–
12	+	–	+	+	–	–	–	–	Staphylococcus aureus
13	–	–	–	–	–	–	–	–	Streptococcus pyogens
14	–	–	–	–	–	–	–	+	–
15	+	+	–	+	–	–	–	–	Pseudomonas koreensis
16	+	–	+	+	+	–	–	–	–
17	–	–	–	+	–	–	–	–	–
18	–	–	–	–	–	–	–	–	–
19	–	–	–	–	–	–	–	+	–
20	–	+	–	+	–	–	–	–	–
21	+	–	–	+	–	–	–	–	–
22	–	–	–	–	–	–	–	+	Candida albicans
23	–	–	–	+	–	–	–	–	Escherichia coli
24	–	–	+	+	–	–	–	–	–
25	–	+	–	+	+	–	–	–	–
26	–	–	–	+	–	–	–	–	–
27	–	–	–	+	–	–	–	–	–
28	–	–	–	–	–	–	–	+	Candida albicans
29	–	–	–	–	–	–	–	–	–
30	–	–	–	+	–	–	–	–	Pseudomonas putida
31	–	–	–	–	–	–	–	+	Candida albicans
32	–	–	+	+	–	–	–	–	–
33	+	+	–	+	–	–	–	–	–
34	–	–	–	+	–	–	–	–	Escherichia coli
35	–	–	+	+	–	–	–	–	–
36	–	–	–	+	–	–	–	–	–
37	–	–	–	+	–	–	–	–	–
38	–	–	–	+	–	–	–	–	–
39	–	+	–	+	–	–	–	–	–
40	–	–	–	+	–	–	–	–	–
41	–	–	+	+	–	–	–	–	–

The Kruskal-Wallis H tests and LEfSe analysis of the associations between normal control women and PID patients.

Taxon rank	Taxon name	p-value	LDAeffect size	Control(%)	PID patients(%)
Phylum	Firmicutes	0.04364	5.09916	79.38	56.87
Phylum	Saccharibacteria_TM7	0.02254	3.25735	0.42	0.02
Class	Bacilli	0.04089	5.12693	77.74	53.65
Class	Saccharimonas_c	0.02254	3.21094	0.42	0.02
	Lactobacillales	0.04089	5.13602	74.52	50.17
Order	Saccharimonas_o	0.02254	3.24345	0.42	0.02
	Propionibacteriales	0.00628	2.90945	0.24	0.13
	Lactobacillaceae	0.01377	5.15948	63.70	35.76
	Moraxellaceae	0.04593	4.05126	2.40	0.68
Family	Pseudomonadaceae	0.00272	3.56834	0.28	0.83
Family	Saccharimonas_f	0.02254	3.23883	0.42	0.02
	Propionibacteriaceae	0.00628	2.91443	0.24	0.12
	Yersiniaceae	0.04997	2.84709	0.06	0.16
	Lactobacillus	0.02881	5.12933	61.03	34.92
	Gardnerella	0.02706	4.54975	8.36	13.89
	Lactobacillaceae_uc	0.00128	3.98329	2.67	0.84
	Pseudomonas	0.00272	3.54428	0.28	0.83
	Parvimonas	0.00445	3.31257	0.00	0.50
Genus	Enterobacteriaceae_uc	0.01355	3.29397	0.15	0.50
	AF125206_g	0.02254	3.25111	0.42	0.02
	Megasphaera	0.03362	3.04489	0.14	0.37
	Yersinia	0.04997	2.85166	0.06	0.16
	Cutibacterium	0.01311	2.85157	0.19	0.11
	Actinotignum	0.02287	2.50200	0.06	0.00

Clinical profiles of PID patients (n = 41) and women from control group (n = 33).

Group	Age (years)(mean ± SD)	Parity(mean ± SD)	Body mass index(mean ± SD)	Symptom	Number of women	%
PID patients	35.5 ± 2.4	3.3 ± 0.2	29.5 ± 6.9	Foul odor (Fish and rotten)	25	61.0
				Itching and burning sensation	11	26.8
				Abnormal color of discharge	5	12.2
				Total	41	100
Control group	39.4 ± 3.2	3.1 ±0.2	30.1 ± 4.3	No observable abnormality	33	100
Control group	39.4 ± 3.2	3.1 ±0.2	30.1 ± 4.3	Total	33	100

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Characteristics of Vaginal Microbiome in Women with Pelvic Inflammatory Disease in Korea

Article Category: original-paper

Publié en ligne: 17 sept. 2021

Pages: 345 - 357

Reçu: 30 avr. 2021

Accepté: 14 juil. 2021

DOI: https://doi.org/10.33073/pjm-2021-033

Mots clés
vaginal microflora, pelvic inflammatory disease, 16S rRNA amplicon sequencing, premenopausal, Korean

© 2021 Sukyung Kim et al., published by Sciendo

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

Distributions of bacterial community at different taxonomic levels (phylum, class, order, and family).

Identification of microbes using STD multiplex PCR and culture method for PID patients.

The Kruskal-Wallis H tests and LEfSe analysis of the associations between normal control women and PID patients.

Clinical profiles of PID patients (n = 41) and women from control group (n = 33).

Characteristics of Vaginal Microbiome in Women with Pelvic Inflammatory Disease in Korea

Article Category: original-paper

Publié en ligne: 17 sept. 2021

Pages: 345 - 357

Reçu: 30 avr. 2021

Accepté: 14 juil. 2021

DOI: https://doi.org/10.33073/pjm-2021-033

Mots clésvaginal microflora, pelvic inflammatory disease, 16S rRNA amplicon sequencing, premenopausal, Korean

© 2021 Sukyung Kim et al., published by Sciendo

This work is licensed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License.

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

Fig. 5.

Fig. 6.

Fig. 7.

Distributions of bacterial community at different taxonomic levels (phylum, class, order, and family).

Identification of microbes using STD multiplex PCR and culture method for PID patients.

The Kruskal-Wallis H tests and LEfSe analysis of the associations between normal control women and PID patients.

Clinical profiles of PID patients (n = 41) and women from control group (n = 33).

Mots clés
vaginal microflora, pelvic inflammatory disease, 16S rRNA amplicon sequencing, premenopausal, Korean