The Association between Bacterial

Vaginosis and First Trimester

Miscarriage
By
Wael Gaber Eldamaty
Obstetrics and Gynecology Department, Faculty of Medicine, Menoufiya University

ABSTR
ACT
Background: Three-fourths of spontaneous abortion occurs before 16th week; of these,
three-fourths occur before eighth week. Causes of spontaneous abortion can be summarized to
be: chromosomal abnormalities, infection, hormonal problems, incompetent cervix,
immunological disorders, uterine abnormalities, nutritional and environmental factors. In
many cases of miscarriage no obvious cause was found. Bacterial vaginosis is a condition
characterized by alteration of the vaginal ecology in which the normal flora, dominated by
lactobacilli, is replaced by a mixed bacterial flora which includes Gardnerella vaginalis,
Mobiluncus spp and Mycoplasma hominis. In clinical practice B.V is diagnosed using the
criteria of Amsel. Gram stain of vaginal fluid is the most widely used and evaluated
microbiologic diagnostic method for bacterial vaginosis.
Objectives: To assess the association between bacterial vaginosis and first trimester
miscarriage.
Patients and methods: We recruited 192 pregnant women at the 6 th- 8th week of gestation
from the women who attended to antenatal care clinic. Samples were collected for our study.
12 samples were excluded by the laboratory because these samples were incorrectly prepared,
10 cases were missed in follow up (170 samples were collected). For each case, a full history,
general and local examinations done and we took vaginal swab to screen for bacterial
vaginosis using Nugent gram stain scoring system , and culture of the swap on chocalate agar
among these women and divided them to 2 groups: Group I: Negative for bacterial vaginosis
(120 women = 70.6%) and Group II: positive for bacterial vaginosis (50women = 29.4 %).
Results: There was statistically significant relation between bacterial vaginosis and first
trimester miscarriage when comparing pregnant women with bacterial vaginosis (30 %) with
normal flora (13.3%) regarding first trimester miscarriage. Screening of asymptomatic bacterial
vaginosis would reduce miscarriage rates, particularly in the first trimester.
Conclusion: We conclude that there was a statistically significant relation between bacterial
vaginosis and first trimester miscarriage when comparing pregnant women with bacterial
vaginosis with normal flora regarding first trimester miscarriage.

Key Words: Miscarriage, bacterial vaginosis, pregnancy outcome

INTRODUCTION pregnancy at a stage where the

Miscarriage or spontaneous embryo or fetus is incapable of
abortion is the spontaneous end of surviving, generally defined in
humans at prior to 20 weeks of
gestation or below a fetal weight of
500g(1).
Miscarriage is a common
event that causes considerable
morbidity and fetal loss for women
in the childbearing period. Some
investigators have demonstrated
that about three-fourths of
spontaneous abortion occurs before
16th week; of these, three-fourths
occur before eighth week. Almost
20% of clinically recognized
pregnancies terminate in
spontaneous abortion(2).
Data on the possible role of
cervicovaginal infection in the
causation of early pregnancy loss
are scarce. Chlamydia trachomatis
may lead to abortion through
excessive maternal immunogenic
reaction to its heat shock protein 60
antigen(3) and some authors have
found an association of spontaneous
abortion with the presence of
vaginal Ureaplasma urealyticum(4)
and with the presence of group B
streptococci and gonorrhea(5).
Causes of spontaneous
abortion can be summarized to be:
chromosomal abnormalities,
infection, hormonal problems,
incompetent cervix, immunological
disorders, uterine abnormalities,
nutritional and environmental
factors. In many cases of
miscarriage no obvious cause was
found(6).
Early diagnosis and treatment
or prevention of the causes of
miscarriage is of fundamental
importance in avoiding many
harmful maternal complications not
only fetal loss but also severe
hemorrhage, sepsis, bacterial shock,
acute renal failure and also
iatrogenic complications as
incomplete removal of the fetus and
placenta, cervical laceration and
uterine perforation during sounding
of the uterus, dilatation or
curettage(7).
Bacterial vaginosis is the most
prevalent form of vaginal infection
in women during childbearing age
the average incidence of bacterial
vaginosis varies and reported to be
20- 45% in patients visiting
gynaecological and sexually
transmitted diseases clinics and 15-
30% in patients visiting obstetric
clinics(8).
A typical clinical symptoms of
bacterial vaginosis is a thin,
homogenous, gray, malodorous
vaginal discharge, without
significant pruritis or pain However
more than 50% of all women with
bacterial vaginosis are
asymptomatic(9).
Bacterial vaginosis is
diagnosed if the patient has at least
three of the four following clinical
criteria of Amsel(10):
1. Thin homogenous gray white
vaginal discharge.
2. Clue cells on microscopy.
3. PH of vaginal fluid >4.5
4. Release of a fishy odor on
adding alkali—10% potassium
hydroxide (KOH) solution.
Vaginal infection by bacterial
vaginosis may increase the risk of
miscarriage as it is associated with
endometritis which may affect the
implantation of the embryo and
placenta so bacterial vaginosis may
have a detrimental effect on the
outcome of the first trimester(11).
Bacterial vaginosis has been
associated with many
gynaecological complications such
as cervicitis, salpingitis,
endometritis and PID also it is
associated with obstetric
complications such as a two to
seven fold increase in the risk of
mid-trimester miscarriage and
preterm birth(12), also an increased
risk of preterm rupture of
membranes, chorioamnionitis, low
birth weight and postpartum
endometritis(9).
This study is intended to
assess the association between
bacterial vaginosis and first
trimester miscarriage.
PATIENTS AND METHODS
This Prospective observational
comparative study was conducted at
antenatal care clinic. All
participants gave their verbal and
written consents to participate and
we obtained ethical approval for our
study from the local ethics
committee.
Patients:
We recruited 192 pregnant
women from attendants of antenatal
care clinic which were confirmed to
be viable by ultrasound
examination. Samples were
collected for our study. 12 samples
were excluded by the laboratory
because these samples were
incorrectly prepared and 10 cases
are missed in follow up so,170
cases were included in the study.
Inclusion criteria:
Pregnant women of age
group17–35 years, at 6 -8 weeks
with and without vaginal discharge,
confirmed fetal cardiac pulsation by
U/S and no threatened abortion.
Exclusion criteria:
1- Age > 35 years and < 17 Years.
2- Obese patient which had BMI
more than 30.
3- Patient who have History of
previous one or more abortion.
4- Multiple gestations.
5- Blighted ovum.
6- Medical conditions predisposing
to miscarriage as: Diabetes
mellitus, Chronic hypertension,
Endocrinal diseases,
autoimmune diseases, Renal
diseases and Blood diseases.
7- Patients who received
antimicrobial therapy within 4
weeks before sampling.
Methods:
1- History taking.
2- General and abdominal
examination.
3- Local examination for inspection
of abnormal vaginal discharge
and signs of vaginitis.
4- Ultrasound examination for
confirmation of pregnancy, fetal
well- being (+ve cardiac
pulsation), dating in early
pregnancy and cervical
dimension for execlusion of
cervical incompetence.
5- Follow up of the cases by serial
obstetric ultrasound once every
two weeks for assesment of fetal
well- being till the end of 13th
week gestation.
Collection of samples:
1- Explanation of the procedure to
the patients.
2- Put the patients in the lithotomy
position.
3- Insertion of a sterile speculum
into the vagina in the presence of
good illumination.
4- Take the samples by rotation of
a sterile cotton swab against the
vaginal walls and the posterior
fornix to achieve saturation and
Send the slides to the laboratory
at the same day.
5- Smear the swabs on a clean glass
slides.
6- The slides air dried then mark each
slide with the patient's study
number.
7- Fixation of the samples by heat
and prepare the slides to stain
with gram stain.
8- Culture of the swap on chocalate
agar for 24 hours incubated at 37
c.
Using Nugent gram stain
scoring system and the result of the
culture for diagnosis of bacterial
vaginosis, bacterial vaginosis was
diagnosed according to the Nugent
Score which is gram stain scoring
system and culture result. The
Nugent score is calculated by
assessing for the presence of large
gram-positive rods (Lactobacillus
morphotypes; decrease in
Lactobacillus scored as 0 to 4),
small gram-variable rods (G.
vaginalis morphotypes; scored as 0
to 4), and curved gram-variable rods
(Mobiluncus spp. morphotypes;
scored as 0 to 2) and can range from
0 to 10. A score of 7 to 10 is
consistent with bacterial vaginosis.
Gram stain of vaginal fluid is the
most widely used and evaluated
microbiologic diagnostic method
for bacterial vaginosis(13). The slides
were read by observer blinded to
outcome of pregnancy at the end of
the first trimester.
Then division of the patients
into 2 groups according to Nugent
gram stain scoring system and result
of the culture :
 Group I: patients
negative for bacterial
vaginosis.
 Group II : patient
positive for bacterial
vaginosis.
Statistical analysis:
After data collection,
verification and revision. We
analyzed tabulated data statistically
using SPSS statistical package
version (19).
Data were expressed as
number and percentage for
qualitative variables and mean +
standard deviation for quantitative
one.
Data were summarized using
the arithmetic mean, the stnadard
deviation and median.
The comparison was done
using the student "t" test and chi-
square test.
For all above-mentioned
statistical tests done, the threshold
of significance was fixed at 5%
level (P-value).
- P value of > 0.05 indicates non-
significant results.
- P value of < 0.05 indicates
significant results.
The smaller the P value
obtained, the more significant are
the results.
 In table (6), we compared
methods used in diagnosis, we
found that all the cases in group II
RESULTS (50 patients) with bacterial
Table (1) revealed no vaginosis were +ve by culture but
significant difference between both by vaginal smear there were 39
groups concerning the demographic cases ( 78.0 %) +ve and 11cases
parameters. ( 22.0 % ) were –ve which then
Table (2) showed that 60 % of appeared to be +ve by culture.
women who had Bacteial vaginosis Regarding vaginal discharge,
used IUCD before current there are asymptomatic cases of
pregnancy compared with 29.2 % in bacterial vaginosis 6 cases ( 12.0
women with normal vaginal flora %) among women +ve for bacterial
which suggest the association vaginosis (table 7).
between its incidence and IUCD.
In table (8), we classified the
In table (3), we compared miscarriage cases in the two groups
mean gestational age of diagnosis in accoding to clinical types and show
both groups which revealed no no significance regarding this
significant difference between the parameter.
two groups concerning this
parameter.
Table (4) showed that, among
the 170 women included in the
study 31 women (18.20 %)
miscarried during the first trimester
and 139 women (81.8 %) continued
their pregnancies after 13th weeks.
The results of our study showed a
statistically significant relation
between bacterial vaginosis and first
trimester miscarriage when
comparing pregnant women with
B.V (30 %) with women –ve for
B.V (13.3%) regarding first
trimester miscarriage ( P = 0.01, 2
6.85).
In table (5), by comparing
mean gestational age of abortion in
the two groups we found it was 11.8
±SD 1.1 in women with normal
vaginal flora and 10.7 ±SD 0.5 in
women with bacterial vaginosis
which reveals that miscarriage
occurred earlier in women with
bacterial vaginosis.
Table (1): Demographic characteristics of the two studied groups.

GroupI Group II
χ² P. value
(no.&%) (no.&%)
Age (years ) 28.5±12
25.5±11
mean±SD T=2.49 0.117
26.5 ± 12

17-<23 14(11.7) 8(16.0)

0.75 0.687
23 - <29 84(70.0) 32(64.0)
29 - 35 22(18.3) 10(20.0)
Parity
-Primigravida 36(30.0) 17(34.0)
0.18 0.668
- Multipara 84(70.0) 33(66.0)
Total
120(100.0) 50(100.0)

Table (2): Distribution of group I and group II according to previous

methods of contraception and occupation.

Previous methods of GroupI Group II P.

χ²
contraception (no.&%) (no.&%) value
- Non users 43(35.8) 10(20.0)
- Hormonal 37(30.8) 7(14.0)
15.73 0.001*
- IUCD 35(29.2) 30(60.0)
- Barrier 5(4.2) 3(6.0)
 Occupation
-Housewifes 67(55.8) 35(70.0) 2.95 0.085
- Workers or employees 53(44.2) 15(30.0)
Total 120(100.0) 50(100.0)

Table (3): Distribution of group I and group II according to gestational

age at diagnosis.
Mean gestational age at GroupI Group II
diagnosis N=120 N=50 χ²
P. value
(no.&%) (no.&%)
Mean ±SD
0.076
(7.14±0.8) 7.02±0.8 7.26±0.8 2.03

-7 weeks 41(34.2) 15(30.0)

2.98 0.201
-8 weeks 41(34.2) 24(48.0)

Table (4): Distribution of group I and group II according to first trimester

miscarriage

First
GroupI Group II
trimester χ² P. value
(no.&%) (no.&%)
miscarriage
-ve 104(86.7) 35(70.0)
6.85 0.01*
+ve 16(13.3) 15(30.0)
Total 120(100.0) 50(100.0)
Table (5): Relation between first trimester abortion in both groups and
mean gestational age of diagnosis and mean gestational age of abortion.
Mean gestational age at First trimester abortion χ² P. value
 diagnosis GroupI Group II
N=16 N=15
(no.&%) (no.&%)

Mean ±SD(7.1±0.8) 6.9±0.8 7.1±0.8 T=0.67

0.502
9
-6 weeks
-7 weeks 5(31.3) 4(26.7)
0.81 0.666
-8 weeks 7(43.8) 5(33.3)
4(24.9) 6(40.0)
Mean gestational age 11.8 ±
at abortion 1.1 10.7±0.5 T=2.91 0.007*
Mean ±SD(11.1 ±1)

Table (6): Distribution of bacterial vaginosis according to Methods of

diagnosis by culture and vaginal smear.

GroupI Group II
N=120 N=50 χ² P. value
(no.&%) (no.&%)
Culture
+ve 0(0.0)
50(100.0) 170 <0.001**
-ve 120(100.0)
0(0.0)
Vaginal smear
+ve 0(0.0)
39(78.0) 121.47 <0.001**
-ve 120(100.0)
11(22.0)

Table (7): Distribution of clinical suspicious of vaginal discharge for B.V in

both groups to result of the smear and culture.

Vaginal GroupI Group II

χ² P. value
discharge (no.&%) (no.&%)
-ve 111(92.5) 6(12.0)
106.59 <0.001**
+ve 9(7.5) 44(88.0)
Total 120(100.0) 50(100.0)
Table (8): Distribution of cases of abortion in both groups according to
clinical types of abortion.
 Clinical types of P.
GroupI Group II
abortion χ² valu
(no.&%) (no.&%)
e
-Missed abortion 7(43.7) 6(40.0)
-Incomplete abortion 4(25.0) 4(26.7)
0.04 0.998
- Inevitable abortion 3(18.8) 3(20.0)
-Complete abortion 2(12.5) 2(13.3)
Total 16(100.0) 15(100.0)

Figure (1): The normal vaginal epithelial cells and clue cells

Figure (2): The thin homogenous gray white vaginal discharge

Figure (3): Clue cell on Gram stain and saline wet mount of vaginal discharge(on >20%
cells G.vaginalis adhered to epithelial cells; most reliable single indicator

Figure (4): G. stained vaginal smears showing Gardnerlla vaginalis clue cell center

Figure (5): Individual squamous cells covered by a layer of bacteria that obscures the cell
membrane ( Clue cells)
 Figure (6): Unstained clue cell, in which the cell membrane being rough

Figure (7): Clue cells on saline Suspesion

Figure (8): Vaginal epithelium Clue cells coated with Gardnerlla Vaginalis
 Figure (9): G. Vaginalis growth colonies
DISCUSSION
Miscarriage is a common
event that causes considerable
morbidity and fetal loss for women
in the childbearing period(2).
Because most of the previous
studies have concentrated on
bacterial vaginosis and pregnancy
outcomes on the second trimester,
however, a firm association of
bacterial vaginosis with first trimester
miscarriage remains to be confirmed
as the diagnosis and treatment of
bacterial vaginosis are simple and
cheap if we found an association
between bacterial vaginosis and 1st
trimester miscarriage(9).
In this study the ages of
patients ranging between 17-35
years old, the mean for age was 26.5
with SD ± 12, the median age was 26
years.We divided the women
according to the parity to
primigravida 53women (31.2 %)
and multipara 117 women (68.8%)
with a range between 0-4 deliveries,
the mean for parity was 2.2 with
SD± 1.3 the median of parity was 2
previous delivery. We divided the
women according to occupation to
housewives 102 patients (60 %) and
workers or employees 68 patients
(40%). Among the 170 women
included in the study there were 4
patients (2.4 %) smokers and 166
patients (97.6 %) non smokers.
Using Nugent gram stain
scoring system and the result of the
culture we divided pregnant women
included in the study to 2 groups:
- Group I: women who are
negative for B.V (120 women
70.6% ).
- Group II: Positive for bacterial
vaginosis(50 women 29.4 % ).
Then we followed them up to
the end of first trimester. We choose
13 weeks as a end point, as our
study was designed to investigate
first trimester miscarriage. All
Women returned the questionnaire,
Then we compared the two groups
regarding the rate of first trimester
miscarriage. In the current study,
the prevalence of bacterial vaginosis
among the pregnant women
included was 29.4 %.
 In Dadhwal(14) study, the
average incidence of bacterial
vaginosis varies and is reported to
be 20- 35% in patients visiting
gynaecological clinics, 15 –30% in
patients visiting obstetric clinics and
20–45% in patients visiting services
of sexually transmitted diseases.
In our study among the 170
women included in the study 31
women (18.2 %) miscarried during
the first trimester and 139 women
(81.8 %) continued their
pregnancies after 13 week.
George(2) found that almost 20% of
clinically recognized pregnancies
terminate in spontaneous abortion.
By comparing the two groups
as regard the age, the mean for age
was 25.5 with SD ± 11 in the
women –ve for B.V, and 28.5 with
SD ± 12 in the women with
bacterial vaginosis. as regard the
parity, the mean was 2.22 with SD
± 1.31 among the women –ve for
B.V and 2.12 with SD ± 1.28
among the women with bacterial
vaginosis. There were no
statistically significant differences
between the two groups concerning
demographic baseline criteria as
Age, parity, occupation, smoking
habit and previous method of
contraception. Similarly, Darwish
et al.(15) found that there was no
statistically significant difference
regarding the demographic
characteristic between women
included in his study.
We compare methods used in
diagnosis, we found that all the
cases in group II ( 50 patients) with
bacterial vaginosis were +ve by
culture but by vaginal smear there
were 39 cases ( 78.0 %) +ve and
11cases ( 22.0 % ) were –ve which
then appeared to be +ve by culture
which provide an evidance that the
culture of the vaginal swab is the
most senstive and conclusive for
diagnosis of bacterial vaginosis.
Regarding vaginal discharge, there
are asymptomatic cases of bacterial
vaginosis 6 case ( 12.0 % ) among
women +ve for bacterial vaginosis.
The results of our study
showed a statistically significant
relation between bacterial vaginosis
and first trimester miscarriage when
comparing pregnant women with
bacterial vaginosis (30 %) to
women who are negative for
bacterial vaginosis (13%) regarding
first trimester miscarriage ( P =
0.01, 2 6.85).
By comparing mean
gestational age of abortion in the
two groups we found it was 11.8
±SD 1.1 in women with normal
vaginal flora and 10.7 ±SD 0.5 in
women with bacterial vaginosis
which reveals that miscarriage
occurred earlier in women with
bacterial vaginosis than women –ve
for B.V.
Similar study from south
London, UK screened 1214 women
at less than 10 weeks of gestation
for bacterial vaginosis. The
prevalence of bacterial vaginosis
was 32.5%. Miscarriage occurred
before 16 weeks of gestation in 282
women (23 %). There was a
significant trend for women with
bacterial vaginosis to have a
miscarriage between 10 and 12
weeks of gestation(16) and this agrees
with the results of our study.
Donders et al.(17) concluded
that bacterial vaginosis, especially
when Gardnerella vaginalis or
mycoplasmas are cultured, is
associated with a 5-fold increased
risk of spontaneous abortion. The
relative risk obtained for early
pregnancy loss among women seen
with bacterial vaginosis before 14
weeks of gestation (relative risk,
5.4), he assume that ascending
spread of the infection followed by
an inflammatory reaction is the
most likely mechanism.
So, Donders et al.(17) assumed
that inflammatory reaction after
ascending infection may therefore
be the mechanism by which
bacterial vaginosis may causes
spontaneous abortion This would
also explain why the complication
rate of bacterial vaginosis is higher
when the ascent is facilitated, such
as by the presence of an intrauterine
contraceptive device before
pregnancy, which agree with our
study,In which we found that 60 % of
women who had Bacteial vaginosis
used IUCD before current pregnancy
compared to 29.2 % in women with
normal vaginal flora which suggest
the association between its incidence
and IUCD. We classified the
patients according to method of
contraception used before the current
pregnancy to non users 53 patients
(31.2 %), 44 patients (25.9 %) used
hormonal methods, 65 patients (38.2
%) used IUCD method, 8 patients (4.7
%) used barrier method.
Also, Ralph et al.(18) have
looked at bacterial vaginosis and
miscarriage in the first trimester in
women undergoing in vitro
fertilization, with conflicting
results. They found bacterial
vaginosis was associated with a two
folds risk of miscarriage in the first
trimester in 237 women who
became pregnant after in vitro
fertilization. These women had high
overall rates of both miscarriages
(24%) and bacterial vaginosis
(25%) and most miscarriages were
preclinical, implying failure of
implantation rather than loss of an
established pregnancy. The
increased risk of preclinical
pregnancy was higher than the
overall risk of a miscarriage in the
first trimester (crude relative risk
2.69 and1.95 respectively).
Another two hospital based
studies have examined the relation
between bacterial vaginosis and
miscarriage in women who
conceived naturally. These studies
recruited women much later in
pregnancy (924 weeks' gestation)
than our study, and all were
designed to look at preterm birth as
well as miscarriage. In a prospective
study of 783 women, Hay et al.(19)
found a relative risk of 5.5 for
miscarriage at 1624 weeks'
gestation.
The 2nd study of 1260 women
mostly recruited during the second
trimester, McGregor et al.(20) found
a relative risk of 3.1 for miscarriage
before 22 weeks' gestation. In the
treatment arm (two 300-mg doses of
clindamycin) however, pregnancy
loss actually increased from 1.8% to
2.9%, which indicates that treatment
for bacterial vaginosis had not
succeeded in preventing pregnancy
losses.
The difference between our
study and results of both Hay et al.
(19)
and McGregor et al.(20) may be
due to that women included in our
study were pregnant at the 6th -8th
week of gestation and outcome
measure is miscarriage before 13
weeks, but the previously
mentioned studies were applied
during the second trimester.
From the result of our study
and the results of other similar
studies it seems that screening of
asymptomatic bacterial vaginosis
would reduce miscarriage rates,
particularly in the first trimester.
CONCLUSION
From this study, the
prevalence of bacterial vaginosis
among the pregnant women
included in the study was 29.4%.
Also, we conclude that there was a
statistically significant relation
between bacterial vaginosis and first
trimester miscarriage when
comparing pregnant women with
bacterial vaginosis with normal
flora regarding first trimester
miscarriage.
Thus it seems likely that
screening and treatment of
asymptomatic bacterial vaginosis
would reduce miscarriage rates,
particularly in the first trimester.
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