Table 1 Oral microbial differences between pregnant and non-pregnant women.

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

Kornman and Loesche (1980)36

USA, prospective cohort

Pregnant (20)

Non-pregnant (11)

Subgingival plaque

Pregnant group

T1: < 13 weeks GA

Follow-ups: monthly after until delivery

Non-pregnant group

Monthly visit for 4 consecutive months

A. naeslundii, A. odontolyticus, A. viscosus, B. asaccharolyticus, P. intermedi), B. ochraceus, F. nucleatum, S. sanguis

Culturing

The subgingival flora evolved to a composition that has more anaerobes as pregnancy progressed

The anaerobe/aerobe ratio increased significantly at an early stage of pregnancy and remained high until the third trimester

Only B. melaninogenicus ss. intermidius (currently P. intermedia) significantly increased during pregnancy compared between trimesters

In the 2nd trimester, the anaerobe/aerobe ratio and the proportions of B. melaninogenicus ss. intermedius different significantly from the non-pregnant group

Fair

Muramatsu and Takaesu (1994)37

Japan, cross-sectional

Pregnant (19)

Non-pregnant (12)

Postpartum (8)

Supragingival plaque, saliva

Pregnant group

One time point during pregnancy

P. intermedia, Black-pigmented anaerobic rods, Actinomyces streptococcus

Culturing

Significant differences in proportions of Actinomyces were found between pregnant and non-pregnant group and between 2nd trimester pregnant and postpartum group

No statistically significant changes in proportions of P. intermedia

Fair

Yokoyama et al. (2008)38

Japan, cross-sectional

Pregnant (22)

Non-pregnant (15)

Unstimulated whole saliva

Pregnant group

27.4 ± 5.1 weeks GA

C. rectus, P. gingivalis, A. actinomycetemcomitans, F. nucleatum, P. intermedia

Real-time PCR

Positive correlations between bacteria carriage and estradiol concentrations

C. rectus (r = 0.443, p = 0.006)

P. gingivalis (r = 0.468, p = 0.028)

F. nucleatum (r = 0.452, p = 0.035)

Positive correlations between C. rectus levels and sites of 4 mm-pocket depth (r = 0.568, p = 0.006)

Fair

Gürsoy et al. (2009)16

Finland, prospective cohort

Pregnant (30)

Non-pregnant (24)

Subgingival plaque, saliva

Pregnant group

T1: 12–14 weeks GA

T2: 25–27 weeks GA

T3: 34–38 weeks GA

T4: 4–6 weeks postpartum;

T5: After lactation

Non-pregnant group

T1–T3 (once per subsequent month)

P. intermedia, P. nigrescens (former Bacteroides intermedius)

16s rDNA sequencing and culturing

Carriage of subgingival P. intermedia doubled in the 2nd trimester, comparing to the 1st trimester; continued increasing till after the delivery (p < 0.05); and decreased to the lowest point after lactation

Carriage of salivary P. intermedia remained stable during the pregnancy and decreased (p < 0.05) after lactation to the same level as the non-pregnant group

P. nigrescens is likely associated with pregnancy gingivitis

Fair

Carrillo-de-Albornoz et al. (2010)39

Spain, prospective cohort

Pregnant (48)

Non-pregnant (28)

Subgingival plaque

Pregnant group

T1: 12–14 weeks GA

T2: 23–25 weeks GA

T3: 33–36 weeks GA

T4: 3 months postpartum

Non-pregnant group

2 visits 6 months apart

C. rectus, P. gingivalis, A. actinomycetemcomitans, F. nucleatum, P. intermedia, T. forsythensis, P. micra

Culturing

No significant changes in total bacterial counts in the pregnant group either during or after pregnancy

Significant reduction in A. actinomycetemcomitans after delivery (p = 0.039)

No statistically significant differences during pregnancy for any of the pathogens evaluated; however, significant changes from the third trimester to postpartum for all the pathogens

Subjects who were positive for P. gingivalis had higher levels of gingival inflammation

Fair

Basavaraju et al. (2012)40

India, prospective cohort

Pregnant (15)

Non-pregnant (15)

Subgingival plaque

Pregnant group

T1: during pregnancy

T2: 3 weeks postpartum

Veillonella, T. forsythia, P. intermedia, P. gingivalis, Peptoscreptococcus, F. nucleatum, Propionebactierum, Mobiluncus, Candida spp.

Culturing

The organisms which were most commonly detected in both the groups were: Vielonella, T. forsythia, P. intermedia, P. gingivalis, Peptosreptococcus and F. nucleatum

P. gingivalis was present in 5 patients out of 15 in the pregnant-group as compared to 1 in the non pregnant group and the count was reduced to 3 during postpartum

Poor

Machado et al. (2012)41

Brazil, cross-sectional

Pregnant (20)

Non-pregnant (20)

Subgingival plaque

Pregnant group

14–24 weeks GA

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

Fluorescence in situ hybridization

No significant difference in mean total bacterial count between pregnant and non-pregnant group

No significant differences between groups in the numbers of all bactieral species evaluated

Fair

Emmatty et al. (2013)17

India, cross-sectional

Pregnant (30, 10 in each trimester)

Non-pregnant (10)

Subgingival plaque

Pregnant group

One time point during pregnancy

A. actinomycetemcomitans, P. gingivalis, P. intermedia, F. nucleatum, P. micra

Culturing

P. intermedia significantly increased in pregnant women who were in their second and third trimesters as compared with first trimester and non-pregnant women

Proportions of the pathogens assessed did not show any significant difference among pregnant and non-pregnant women

Fair

Borgo et al. (2014)15

Brazil, prospective cohort

Pregnant (9)

Non-pregnant (9)

Subgingival plaque

Pregnant group

T1: Second trimester (15–26 weeks GA)

T2: Third trimester (30–36 weeks GA)

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

Real-time PCR

The detection of A. actinomycetemcomitans in pregnant women at 2nd and 3rd trimester was significant higher than that in the non-pregnant women (p < 0.05)

Fair

Fujiwara et al. (2017)42

Japan, prospective cohort

Pregnant (132)

Non-pregnant (51)

Subgingival plaque, saliva

Pregnant group

T1: 7–16 weeks GA

T2: 17–28 weeks GA

T3: 29–39 weeks GA

Subgingival

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

Saliva

Above 4 + Streptococci, Staphylococci, Candida spp.

Culturing and real-time PCR

A significant difference in total cultivable microbial number between non-pregnant and each stage of pregnancy

More total bacteria counts at early stage of pregnancy (T1), comparing to the non-pregnant group (p < 0.05)

Significant higher prevalence of Candida spp. in the middle (T2) and late (T3) pregnancy, comparing to the non-pregnant group (p < 0.05)

The number of periodontal species was significantly lower in late pregnancy (T3), comparing to the early (T1) and middle (T2) pregnancy (p < 0.05)

The prevalence of P. gingivalis and A. actinomycetemcomitans was significantly higher in the early (T1) and middle (T2) stage of pregnancy, comparing to the nonpregnant women (p < 0.05)

Fair

Kamate et al. (2017)14

India, prospective cohort

Pregnant (50)

Non-pregnant (50)

Saliva

Pregnant group

T1: 6 weeks GA

T2: 18 weeks GA

T3: 30 weeks GA

T4: 6 weeks postpartum

S. mutans

Culturing

A significant increase in S. mutans during the 2nd and 3rd trimester and postpartum period of pregnancy compared to the non-pregnant group (p < 0.01)

Fair

Rio et al. (2017)43

Portugal, prospective cohort

Pregnant (30)

Non-pregnant (30)

Unstimulated saliva

Pregnant group

T1: 1st trimester

T2: 3rd trimester

Yeast

Culturing

No difference in oral yeast detection within pregnancy stages and between pregnant and non-pregnant stages (p < 0.05)

More oral yeast were found in the 3rd trimester than the 1st trimmest, but no difference comparing to the non-pregnant stage (p < 0.05)

Saliva flow rate did not change in both groups

Fair

Lin et al. (2018)44

China, prospective cohort

Pregnant (11)

Non-pregnant (7)

Supragingival plaque, saliva

Pregnant group

T1: 11–14 weeks GA

T2: 20–25 weeks GA

T3: 33–37 weeks GA

T4: 6 weeks postpartum

Non-pregnant group

4 visits (same intervals of the pregnant group)

Quantity of OUT and microbiota diversity

16s rDNA sequencing

Significant higher bacterial diversity of the supragingival microbiota in third trimester compared to the non-pregnant group

Neisseriaceae and Porphyromonadaceae and Spirochaetaceae were significantly enriched in pregnant group

Fair

Xiao et al. (2019)45

USA, cross-sectional

Low SES pregnant (48)

Low SES Non-pregnant (34)

Whole non-stimulated saliva, supragingival plaque, mucosal swabs

Pregnant group

3rd trimester (> 28 weeks GA)

C. albicans, C. glabrata, C. tropicalis, C. krusei, C. dubliniensis, S. mutans

Culturing and Colony PCR

Salivary S. mutans carriage was higher in pregnant than non-pregnant women (p < 0.05)

No difference between pregnant and non-pregnant salivary C. albicans carriage (p > 0.05)

Tonsil (57%) was the most prevalent site for C. albicans detection among pregnant women

Untreated decayed teeth is associated with higher carriage of salivary S. mutans and C. albicans detection in both pregnant and non-pregnant groups (p < 0.05)

Fair

Aikulola et al. (2020)46

Nigeria, cross-sectional

Pregnant (26)

Non-pregnant (32)

Oral swab

Pregnant group

20–28 weeks GA

S. aureus, N. catarrhalis, K. pneumonia, E. coli, P. melaninogenicus, P. propionicum, V. pervula, S. viridans, Coagulase negative Staphylococcus

Culturing

E. coli was the most common species in non-pregnant group while N. catarrhalis was the most common in the pregnant group

Poor

Huang et al. (2020)47

China, cross-sectional

Pregnant (84)

Postpartum (33)

Unstimulated saliva

Pregnant group

One time point

P. gingivalis, P. intermedia, P. nigrscens

16s rRNA PCR

P. nigrescens had higher prevalence in the pregnant group (p < 0.01)

P. nigrescens exhibited more frequently in late pregnancy than early and middle pregnancy (p < 0.05 and p < 0.01)

P. gingivalis in the postpartum group exceeds all of the pregnant stages (p < 0.01)

P. intermedia did not show any significant differences among groups

Fair

Sparvoli et al. (2020)48

Brazil, cross-sectional

Pregnant (42)

Non-pregnant (18)

Oral swab

Pregnant group

28–36 weeks GA

Quantity of OUT and microbiota diversity

16s rRNA sequencing

Significant differences in the relative abundance of oral microbiome in pregnant women

A significant dominance of Streptococcus and Gemella in pregnant women (p < 0.01 and 0 = 0.03)

Shannon diversity index were higher in the non-pregnant group, while the Simpson diversity index was higher in the pregnant group

Fair

Wagle et al. (2020)49

Norway, cross-sectional

Pregnant (38)

Non-pregnanr (50)

Saliva

Pregnant group

18–20 weeks GA

S. mutans, Lactobacillus

Culturing

S. mutans were more abundant in pregnant women (p = 0.03)

Lactobaciilus did not have the significant difference between the groups

Fair