Hindawi Publishing Corporation

ISRN Infectious Diseases

Volume 2013, Article ID 980537, 4 pages
http://dx.doi.org/10.5402/2013/980537

Research Article
Bacterial Vaginosis, Educational Level of Pregnant Women,
and Preterm Birth: A Case-Control Study

Lindita Yzeiraj-Kalemaj,1 Vjollca Shpata,2 Gentian Vyshka,3 and Afërdita Manaj4

1
Fier Regional Hospital, Fier, Albania
2
Faculty of Medical and Technical Sciences, University of Medicine in Tirana, Tirana, Albania
3
Biomedical and Experimental Department, Faculty of Medicine, University of Medicine in Tirana, Tirana, Albania
4
Obstetrical and Gynecological Hospital “Mother Geraldine”, University of Medicine in Tirana, Tirana, Albania

Correspondence should be addressed to Gentian Vyshka; [email protected]

Received 11 July 2013; Accepted 28 August 2013

Academic Editors: D. Bachani, F. Ferrero, and G. N. Malaviya

Copyright © 2013 Lindita Yzeiraj-Kalemaj et al. This is an open access article distributed under the Creative Commons Attribution
License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Objective. In a prospective study, we have recruited two groups of pregnant women (the first one with preterm labor activity; the
second one with labor in term), trying to find a correlation between bacterial vaginosis (BV) and preterm birth activity. Other
parameters influencing the presence of BV have been studied as well, such as educational level and history of previous preterm
deliveries. Materials and Methods. Each group was composed of 75 women; recruitment stopped when the number was reached.
Bacteriological data were retrospectively collected from the follow-up visits that pregnant women had performed at the regional
hospital facility, where the study was performed. The diagnosis of BV was made according to Amsel criteria. Results. Our study
showed a significant correlation between BV and preterm labor. BV seems to be an independent risk factor for preterm labor. In the
study group, the prevalence of BV was 32%, whereas in the control group, the figure was 14.6% (𝑃 = 0.01). Conclusion. Highly risked
groups for a preterm birth activity, such as pregnant women presenting BV and with a low educational level, have to be followed
up and eventually treated cautiously in order to avoid early and late complications of preterm delivery.

1. Introduction have demonstrated that bacteria ascend toward endometrial

tissue and invade placenta as well, although the full impact of
Preterm labor activity is defined as the birth of a child before this ascending infection in relation to the early fetal develop-
the 37th week of gestation, and in terms of public health it has ment is still a conundrum [8].
a very large burden of disease, with fifteen million babies born Since large clinical and casuistic data have correlated BV
preterm annually [1]. Preterm birth is one of the main causes with specific complications of pregnancy, we have tried to
of perinatal morbidity and lethality. There are several factors study the role of its presence in a sample of Albanian pregnant
that might lead to a preterm birth, with lower genitourinary women, whose pregnancy and labor were followed up at our
tract infections playing an important role. Intrauterine infec- facility, during the period of January 1, 2010, till of December
tions might induce preterm labor activity before the rupture 31 of the same year. No other previous studies of this scope
of fetal membranes, although the factors leading to such a have been realized, to our knowledge, in Albania.
premature rupture of membranes are multiple [2, 3]. Large
studies have shown the role bacterial vaginosis (BV) seems to
2. Materials and Methods
play in the preterm labor [4].
BV is a widely present occurrence and probably the main The study was prospective and open label, with patients
cause of vaginitis among pregnant or nonpregnant women recruited till we composed a sample of 150 women. The first
[5]. The fact is however that the majorities of women present- group of 75 women was classified as pregnant subjects diag-
ing BV are asymptomatic and therefore remain untreated for nosed with preterm labor (between 24 and 37 weeks of ges-
a long period of time [6, 7]. Laboratory and clinical studies tation); the second group had the same number of probands
2 ISRN Infectious Diseases

Table 1: Exclusion criteria from the present study. Table 2: Amsel criteria (used at the present study).
Pregnant patients showing cervical incompetence Homogeneous vaginal discharge
Placenta previa Amine (fishy) odor when potassium hydroxide solution is added
Placental abruption to vaginal secretions
Premature rupture of fetal membranes Presence of clue cells (greater than 20%) on microscopy
Uterine anatomic disorders (bicornuate uterus, etc.) Vaginal pH > 4.5
Gemellary pregnancies

Therefore, we used the statistical model of logistic regression

and was composed of pregnant subjects admitted at the labor to ponder the role of other factors, such as level of education,
room in term (>37 weeks of gestation). Vaginal swab sam- previous abortions, and positive history of preterm labor in
ples were collected from each pregnant woman during the previous pregnancies.
prenatal care visits to our facility and were screened for BV. The multiple logistic regression statistical analysis sug-
The study was performed in the Regional Hospital of Fier, a gested that BV, positive history of preterm labor in previous
southern city of Albania. A detailed informed consent was pregnancies, and low education level are all independent risk
received from all participants in the study, with data treated factors for a preterm birth. Results are summarized in Table 3.
confidentially and anonymously. The hospital and the local Low education level and positive history of previous pret-
health authorities, competent to the territory, were informed erm labor resulted, being independent risk factors, have a
and approved the study. causative link with the presence of BV (Table 4). Thus, 28.4%
The main admission criteria were the preterm labor activ- of the patients with low education level (elementary school)
ity, defined as a minimum of four uterine contractions in resulted positive for BV; otherwise, only 14.5% of the patients
twenty minutes or eight contractions in forty consecutive with high education level (high school or university) were
minutes, causing a cervical dilatation of more than one centi- positive for BV (𝑃 = 0.08).
meter, and a shortening of column uteri with more than 80%, 82.6% of the patients having a history of previous preterm
when comparing the cervical length with the value measured labor activity presented BV as well, instead of only 12.4% of
through sonography during the 22nd week of gestation [9, the patients without a history of preterm labor that were con-
10]. sidered as having BV (𝑃 < 0.0001).
Exclusion criteria are summarized in Table 1.
The control group was composed of 75 women giving
birth to their child at term (more than 37 weeks of gestation). 4. Discussion
Vaginal swabs data were retrieved from previous consul-
tations (pregnancy follow-ups that are scheduled monthly) to BV is a frequent condition accompanying pregnancy.
our facility, and the presence of BV was evaluated. Although with an unclear mechanism, BV influences the out-
BV was considered as present when three out of four cri- come of labor activity and induces preterm birth. It seems
teria of Amsel resulted positive [7, 11]. Amsel criteria used in that the installation of BV implies the substitution of vaginal
the present study are summarized in Table 2. aerobic lactobacilli through anaerobic microorganisms such
Data were statistically analyzed through SPSS 21.0, and as Gardnerella vaginalis, Mycoplasma hominis, and other
odds ratio reports were extracted for several risk factors of strains, thus disturbing seriously the normal vaginal flora [12,
bacterial vaginosis, through the model of multivariate logistic 13]. It seems that anaerobic bacteria through specific products
regression. stimulate the decidual tissue; an increase of cytokine level
and of the release of A2 phospholipase, and prostaglandins
will lead to uterine contractions and preterm labor activity
3. Results [14, 15].
At the present study, 150 pregnant women divided in two In our study, we had a prevalence of BV of 23.3%, and the
equal groups (the 1st group with preterm labor activity and condition was consistently more frequent in patients having
the 2nd with pregnancy in term) were screened for the pres- a preterm labor, when compared with patients having birth
ence of BV. Age, number of pregnancies, previous abortions, activity at the term of the gestation.
and level of education were as well taken as notes. It was in 1984 when Eschenbach et al. showed a correla-
In the group of preterm pregnant women, we had 24 tion between BV and preterm birth; they had a prevalence of
patients with BV, whereas only 11 patients resulted positive for 49% of BV in the preterm birth group, but only 24% in the
BV in the 2nd group (pregnancies in term). We had therefore other (in term) group of pregnant women. The same group
a higher prevalence of bacterial vaginosis in women showing later demonstrated correlations between BV, chorioamnioni-
preterm labor activity, when compared with the other group, tis, and preterm labor activity [16].
respectively, 32% and 14,6% with an OR (odds ratio) equal to There have been large epidemiological studies trying to
2.73 (CI: 95%; confidence interval 1.22–6.11; 𝑃 = 0.013). determine the potential link between BV and preterm labor.
Our preliminary data suggested that BV might be an Series have shown a two-fold increase for preterm labor activ-
important risk factor leading to preterm labor activity; how- ity in women diagnosed with BV, especially when such a diag-
ever, several other factors might play an important role. nosis was made early during the pregnancy, since the second
ISRN Infectious Diseases 3

Table 3: Analysis of risk factors leading to preterm labor activity.

Number (%)
Variable OR 95% CI P value
Total Preterm In term
BV present 35 (23.3) 24 (32) 11 (14.6) 2.73 1.22–6.11 0.013
Positive history of preterm labor in previous pregnancies 23 (15.3) 20 (26.6) 3 (4) 9.60 2.70–34.04 0.0005
Low education level (elementary school) 95 (63.3) 60 (8) 35 (46.6) 6.00 2.65–13.5 <0.0001
High education level (high school and university graduates) 55 (36.6) 20 (26.6) 35 (46.6) 0.40 0.19–0.80 0.01

Table 4: Regression logistic model of risk factor for BV (bacterial vaginosis).

Number (%) presenting with BV OR 95% CI P value
Low education level (elementary school) 27 (28.4%) 2.33 0.97–5.58 0.05
High education level (high school and university graduates) 8 (14.5%) 0.42 0.17–1.02 0.08
Positive history of preterm labor in previous pregnancies 19 (82.6%) 32.9 9.93–109.28 <0.0001

trimester [12, 17]. A study found that BV diagnosed in the activity. A screening for BV during pregnancy is indispens-
second trimester suggested a high risk for an early rupture able, and its treatment is logical and necessary.
of membranes and preterm delivery in correlation with BV
accounting for 82.53% of the attributable risk for preterm References
birth [18]. In another study, a straight correlation was found
between low educational level and BV [19]. [1] M. G. Gravett, C. E. Rubens, Global Alliance to Prevent Pre-
It should be noted that different series trying to find asso- maturity, and Stillbirth Technical Team, “A framework for stra-
ciations between maternal education, bacterial vaginosis, and tegic investments in research to reduce the global burden of
preterm birth, in general, have reached controversial conclu- preterm birth,” American Journal of Obstetrics and Gynecology,
sions. If the role of bacterial vaginosis over the preterm birth vol. 207, no. 5, pp. 368–373, 2012.
is irrefutable, not all authors have their opinions converging [2] R. L. Naeye and E. C. Peters, “Causes and consequences of pre-
with regard to the association of the latter with the level of mature rupture of fetal membranes,” The Lancet, vol. 1, no. 8161,
pp. 192–194, 1980.
maternal education, with some still considering low level of
[3] T. Cobo, M. Kacerovsky, M. Palacio et al., “Intra-amniotic
education an independent risk factor [20, 21]. There have
inflammatory response in subgroups of women with preterm
been as well authors concluding that maternal education is prelabor rupture of the membranes,” PLoS ONE, vol. 7, no. 8,
becoming less protective against preterm birth, or anyhow Article ID e43677, 2012.
not conferring any longer more protection, when compared [4] C. A. Flynn, A. L. Helwig, and L. N. Meurer, “Bacterial vaginosis
with slightly lower education level of future mothers [22, 23]. in pregnancy and the risk of prematurity: a meta-analysis,”
In our study group, the women with low educational level Journal of Family Practice, vol. 48, no. 11, pp. 885–892, 1999.
presented a higher prevalence of BV when compared with [5] D. B. Nelson and G. Macones, “Bacterial vaginosis in pregnancy:
women with higher educational level, respectively, 28.4% and current findings and future directions,” Epidemiologic Reviews,
14.5%. We had also a significant finding when comparing the vol. 24, no. 2, pp. 102–108, 2002.
group of women having a preterm birth, who had a positive [6] L. Cristiano, N. Coffetti, G. Dalvai, L. Lorusso, and M. Lorenzi,
history of previous preterm deliveries in 26.6% of them; “Bacterial vaginosis: prevalence in outpatients, association with
otherwise, only 4% of the women giving birth to their child some micro-organisms and laboratory indices,” Genitourinary
in term have had a preterm labor in previous pregnancies. Medicine, vol. 65, no. 6, pp. 382–387, 1989.
However, the present study has its limitations, mainly related [7] R. Amsel, P. A. Totten, C. A. Spiegel, K. C. Chen, D. Eschenbach,
to the retrospective capture of the data, as well as the small and K. K. Holmes, “Nonspecific vaginitis. Diagnostic criteria
sample size collected to probe the associations between BV and microbial and epidemiologic associations,” American Jour-
nal of Medicine, vol. 74, no. 1, pp. 14–22, 1983.
and educational level in a logistic regression model, where
such an association was found only marginally. [8] J. F. Peipert, A. B. Montagno, A. S. Cooper, and C. J. Sung, “Bac-
terial vaginosis as a risk factor for upper genital tract infection,”
American Journal of Obstetrics and Gynecology, vol. 177, no. 5,
5. Conclusions pp. 1184–1187, 1997.
[9] K. Haram, J. H. S. Mortensen, and A.-L. Wollen, “Preterm deliv-
Bacterial vaginosis is a frequent finding during pregnancy. ery: an overview,” Acta Obstetricia et Gynecologica Scandinavica,
Our study reconfirmed the correlation between bacterial vag- vol. 82, no. 8, pp. 687–704, 2003.
inosis and preterm birth. Due to the fact that preterm deliv- [10] H. J. Lee, T. C. Park, and E. R. Norwitz, “Management of preg-
eries represent significant burden of disease, even in the off- nancies with cervical shortening: a very short cervix is a very
spring medical problems, BV has to be treated intensively. big problem,” Reviews in Obstetrics and Gynecology, vol. 2, no.
This has to be done especially in highly risked subgroups, 2, pp. 107–115, 2009.
such as pregnant women with low educational level, or [11] M. E. Egan and M. S. Lipsky, “Diagnosis of vaginitis,” American
women that have a positive history of previous preterm birth Family Physician, vol. 62, no. 5, pp. 1095–1104, 2000.
4 ISRN Infectious Diseases

[12] S. L. Hillier, R. P. Nugent, D. A. Eschenbach et al., “Association

between bacterial vaginosis and preterm delivery of a low-birth-
weight infant,” New England Journal of Medicine, vol. 333, no. 26,
pp. 1737–1742, 1995.
[13] H. Sharon, “Diagnostic microbiology of bacterial vaginosis,”
American Journal of Obstetrics and Gynecology, vol. 169, no. 2,
pp. 455–459, 1993.
[14] G. G. Donders, B. van Bulck, J. Caudron, L. Londers, A. Ver-
eecken, and B. Spitz, “Relationship of bacterial vaginosis and
mycoplasmas to the risk of spontaneous abortion,” American
Journal of Obstetrics and Gynecology, vol. 183, no. 2, pp. 431–437,
2000.
[15] R. F. Lamont, F. Anthony, L. Myatt, L. Booth, P. M. Furr, and D.
Taylor-Robinson, “Production of prostaglandin E2 by human
amnion in vitro in response to addition of media conditioned by
microorganisms associated with chorioamnionitis and preterm
labor,” American Journal of Obstetrics and Gynecology, vol. 162,
no. 3, pp. 819–825, 1990.
[16] D. A. Eschenbach, M. G. Gravett, K. C. Chen, U. B. Hayme, and
K. K. Holmes, “Bacterial vaginosis during pregnancy: An asso-
ciation with prematurity and postpartum complications,” in
Bacterial Vaginosis, P. A. Mardh and D. Taylor-Robinson, Eds.,
pp. 214–218, Almqvist and Wiksel, Stockholm, Sweden, 1984.
[17] T. Kurki, A. Sivonen, O.-V. Renkonen, E. Savia, and O. Yliko-
rkala, “Bacterial vaginosis in early pregnancy and pregnancy
outcome,” Obstetrics and Gynecology, vol. 80, no. 2, pp. 173–177,
1992.
[18] M. Purwar, S. Ughade, B. Bhagat, V. Agarwal, and H. Kulkarni,
“Bacterial vaginosis in early pregnancy and adverse pregnancy
outcome,” Journal of Obstetrics and Gynaecology Research, vol.
27, no. 4, pp. 175–181, 2001.
[19] E. R. Newton, J. Piper, and W. Peairs, “Bacterial vaginosis and
intra-amniotic infection,” American Journal of Obstetrics and
Gynecology, vol. 176, no. 3, pp. 672–677, 1997.
[20] T. R. Das, S. Jahan, S. R. Begum, and M. F. Akhtar, “Association
between bacterial vaginosis and preterm delivery,” Mymensingh
Medical Journal, vol. 20, no. 1, pp. 115–120, 2011.
[21] D. Desseauve, J. Chantrel, A. Fruchart et al., “Prevalence and
risk factors of bacterial vaginosis during the first trimester of
pregnancy in a large French population-based study,” European
Journal of Obstetrics Gynecology and Reproductive Biology, vol.
163, no. 1, pp. 30–34, 2012.
[22] A. M. El-Sayed and S. Galea, “Temporal changes in socioeco-
nomic influences on health: maternal education and preterm
birth,” American Journal of Public Health, vol. 102, no. 9, pp.
1715–1721, 2012.
[23] N. Auger, M. Abrahamowicz, A. L. Park, and W. Wynant,
“Extreme maternal education and preterm birth: time-to-event
analysis of age and nativity-dependent risks,” Annals of Epide-
miology, vol. 23, no. 1, pp. 1–6, 2013.
 MEDIATORS of

INFLAMMATION

The Scientific Gastroenterology Journal of

World Journal
Hindawi Publishing Corporation
Research and Practice
Hindawi Publishing Corporation
Hindawi Publishing Corporation
Diabetes Research
Hindawi Publishing Corporation
Disease Markers
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Journal of International Journal of

Immunology Research
Hindawi Publishing Corporation
Endocrinology
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Submit your manuscripts at

http://www.hindawi.com

BioMed
PPAR Research
Hindawi Publishing Corporation
Research International
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Journal of
Obesity

Evidence-Based
Journal of Stem Cells Complementary and Journal of
Ophthalmology
Hindawi Publishing Corporation
International
Hindawi Publishing Corporation
Alternative Medicine
Hindawi Publishing Corporation Hindawi Publishing Corporation
Oncology
Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014

Parkinson’s
Disease

Computational and
Mathematical Methods
in Medicine
Behavioural
Neurology
AIDS
Research and Treatment
Oxidative Medicine and
Cellular Longevity
Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation Hindawi Publishing Corporation
http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014 http://www.hindawi.com Volume 2014