Table 2 Oral microbial differences between pregnancy stages.

From: Oral microflora and pregnancy: a systematic review and meta-analysis

Author (year)

Country, study design

Groups (no. of subjects)

Sample source

Measurement interval

Microorganisms evaluated

Microbial detection methods

Study findings

Quality assessment

Dasanayake et al. (2005)50

USA, prospective cohort

First time pregnant women (297)

Stimulated saliva

T1: 3rd trimester

T2: Delivery

S. mutans, S. sobrinus, S. sanguinus, L. acidophilus, L. casei, A. naeslundii, Total Streptococci, Total cultivable organisms

Culturing

A. naeslundii gsp 2 level decreased with increased GA (p = 0.05)

L. casei carriage increased with increased GA (p = 0.04)

L. casei levels at the third trimester were positively associated with birth weight (β = 34.1 g; SE = 16.4; p = 0.04)

Total Streptococci and total cultivable organism levels at delivery were negatively associated with birth weight

After multivariate analysis with average bacterial levels, A. naeslundii gsp 2, L. casei, pregnancy age, and infant gender remained significantly associated with birth weight

Fair

Adriaens et al. (2009)51

Switzerland, prospective cohort

Healthy pregnant women (20)

Subgingival plaque

T1: 12 weeks GA

T2: 28 weeks GA

T3: 36 weeks GA

T4: 4–6 weeks postpartum

37 species including

S. mutans, F. nucleatum, P. intermedia, P. gingivalis, A. actinomycetemcomitans

DNA–DNA hybridization

N. mucosa increased throughout the pregnancy (p < 0.001)

Total bacterial counts

No significant differences between T1 and T2

Significant reduction from T1 to T3 (p < 0.05), and further reduction to T4 (p < 0.01)

Between T1 and T4, significant differences were found for 8 of 37 species, including S. mutans, S. aureus, polymorphum, P. micra

Between measurement intervals, no statistical differences identified for the levels of four periodontal pathogens

Fair

Molnar-Varlam et al. (2011)13

Romania, prospective cohort

Healthy pregnant women (35)

Stimulated saliva

T1: 1st trimester (11–12 weeks GA)

T2: 2nd trimester (20–22 weeks GA)

T3: 3rd trimester (34–35 weeks GA)

S. mutans, Lactobacillus

Culturing

Increase of S. mutans during the 2nd and 3rd trimester among women 25–35 years old

Increase of Lactobacilli in the 2nd trimester among women 20–24 years old and 30–35 years old

The salivary pH increased as the pregnancy progresses

Fair

Martinez-Pabon et al. (2014)52

Colombia, prospective cohort

Pregnant women (35)

Stimulated saliva

T1: Between 2nd and 3rd trimester

T2: 7 months postpartum

S. mutans, Lactobacillus spp.

Culturing

No statistically significant changes in counts of S. mutans and Lactobacillus spp., but a tendency of higher numbers during pregnancy

A statistically significant difference in the pH and the buffering capacity of saliva; both lower during pregnancy (p < 0.05)

Fair

DiGiulio et al. (2015)11

USA, case–control

Pregnant women (49)

Full term (34)

Preterm (15)

Saliva, vaginal, stool, oral swab from molar tooth surface & gum lines

Weekly from early pregnancy until delivery and monthly until 12 postpartum

Not specified;

16 s rDNA sequencing

The progression of pregnancy is not associated with a dramatic remodeling of the diversity and composition of a woman’s microbiota

Fair

Okoje-Adesomoju et al. (2015)53

Nigeria, cross-sectional

Pregnant women (395)

1st trimester (3)

2nd trimester (100)

3rd trimester (292)

Mucosal swab

One time point

Klebsiella spp., E. coli, S. albus, Proteus spp., S. aureus, Streptococcus spp., Pseudomonas spp.

Culturing, API 20A identification kits

Klebsiella species was the predominant isolate from 101 (25.6%) of the women

The pattern of microbial culture whether normal for the oral cavity or not did not vary significantly with parity (p = 0.98), trimester of pregnancy (p = 0.94) or oral hygiene status (p = 0.94)

Poor

Machado et al. (2016)54

Brazil, prospective cohort

Healthy pregnant women (31)

Supragingival & subgingival plaque

T1: 19 ± 3.3 weeks GA;

T2: 48 h postpartum;

T3: 8 weeks postpartum

T. forsythia, C. rectus, P. gingivalis, T. denticola, F. nucleatum, P. intermedia, P. nigrescens A. actinomycetemcomitans

Fluorescence in situ hybridization

Changes in the percentage of P. intermedia, F. nucleatum, P. gingivalis, T. denticola, C. rectus and an increase in A. actinomycetemcomitans was noted, but differences were not statistically significant

- A significant reduction was seen for P. nigrescens when all three time points were compared (p = 0.01, Friedman test), with a reduction from T1 to T3 (p = 0.002), and T2 to T3 (p = 0.037)

Fair

Balan et al. (2018)12

Singapore, prospective cohort

Pregnant women (30)

1st trimester (10)

2nd trimester (10)

3rd trimester (10)

Subgingival plaque, unstimulated saliva

T1: 1st trimester (< 12 weeks GA)

T2: 2nd trimester (21–24 weeks GA)

T3: 3rd trimester (32–36 weeks GA)

T4: 6 weeks postpartum

12 Phyla, 65 genera, 131 species

16s rDNA sequencing

Species richness and diversity of the subgingival plaque and saliva samples were relatively stable across the pregnancy

The abundance of Prevotella, Streptococcus and Veillonella in both subgingival plaque and saliva samples were more during pregnancy

A significant decline in the abundance of pathogenic species, e.g., Veillonella parvula, Prevotella species and Actinobaculum species, was observed from pregnancy to postpartum period

Fair

Goltsman et al. (2018)55

USA, retrospective cohort

Pregnant (10)

Term delivery (6)

Preterm (4)

Saliva, vaginal, stool, rectal swabs

Every 3 weeks over the course of gestation

1553 taxa

16 s rDNA sequencing

Alpha diversity, both inter-individual and intra-individual, remained stable across the pregnancy and postpartum

Fair

de Souza Massoni et al. (2019)56

Brazil, cross-sectional

Pregnant (52)

1st trimester (16)

2nd trimester (21)

3rd trimester (15)

Non-pregnant (15)

Subgingival plaque

One time point

A. actinomycetemcomitans, P. gingivalis, T. forsythia, S. oralis, Universal

qPCR

No significant differences in total amount of bacteria between the groups

T. forsythia showed significant differences in quantification between 1st trimester and 3rd trimester, and 1st trimester and non-pregnant (p = 0.048 and p = 0.014)

Amount of T. forsythia positively correlated with the diagnosis of gingivitis in pregnant women (p = 0.031)

Fair

Dunlop et al. (2019)57

USA, retrospective cohort

African American Pregnant women (122)

Oral samples (97)

Vaginal, oral (tongue, hard palate, gum line) and rectal swabs

T1: 8–14 weeks GA

T2: 24–30 weeks GA

Not specified

16S rDNA sequencing

No difference in Chao1 and Shannon diversity for the vaginal, oral, or gut microbiome across pregnancy for the group overall

For the oral microbiota, having a low level of education and receipt of antibiotics between study visits were associated with greater Bray–Curtis dissimilarity, with some attenuation of the effect of education when additionally controlling for prenatal antibiotics

Fair