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��ࡱ�>��	��������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������������9bjbj�w�w.>����,�������~	~	������������8D\L�CI���������H�H�H�H�H�H�H$SK��M��H9�4!��4!4!�H������H`:`:`:4!������H`:4!�H`:`:VB@�B������}q�����6HB�HI0CITBx�N�62�N�B�B��N��C���5&`:[�G�����H�H�8x���CI4!4!4!4!���������������������������������������������������������������������N���������~	�:Role of the vaginal microbiome in health and disease

Agnieszka Sikora1, Maria KozioB-Montewka1, MaBgorzata Tokarska-Rodak1, Anna Sikora2

1Department of Medical Microbiology, Medical University of Lublin, Poland

2 Department of Gynecology and Obstetrics and Pathology of Pregnancy
The Pope John Paul II Public Regional Hospital of Zamo[, Poland


Corresponding author
Agnieszka Sikora
Department of Medical Microbiology
Medical University of Lublin
Chodzki 1 Street
20-093 Lublin, Poland
phone/fax number: 81�742 37 81
e-mail: agnieszka.sikora24@wp.pl







Abstract 
The vaginal microbiome covers culturable and non-culturable microorganisms, and plays a fundamentally important role in health and disease, but yet this ecosystem remains incompletely characterized and its diversity has been poorly defined yet. Detailed knowledge about the vaginal microbiome and factors affecting its composition will help explain the pathophysiology of important perinatal conditions, including infections, infertility, and preterm birth, and will likely lead to new strategies to prevent infection-related morbidity in women and newborns.


Keywords: microbiome, vaginal microbiota, bacterial vaginosis














Introduction 
The term �microbiome� was first used by Joshua Lederberg�a in 2001 to define �the ecological community of commensal, symbiotic, and pathogenic microorganisms that literally share our body space� [1]. At present, the term �microbiome� refers to all the microorganisms and their genomes present in the human body. This term is frequently confused with the term �microbiota�, which is the microbial population present in different parts of human body including the respiratory, gastrointestinal and urogenital tracts [2]. The human microbiota contains mainly bacteria, archea, fungi, and viruses [3-5]. Vast majority of research on human microbiota has been focused on bacteria [4]. 
Before the completion of the Human Genome Project (HGP), some researchers predicted the identification of about 100 000 genes in the human genome. It was surprising that human genome contains only about 20 000 protein-coding genes [4, 6]. Human body is habitant of at least 10 times more microorganisms that of the number of cells of human body, moreover, the number of genes of these microorganisms (about 3.30 million) is 150 times higher than in human body [6,7]. The majority of those microorganisms is found in the gastrointestinal tract, especially in the gut where the number of microbes is approximately 1012 � 1014. Therefore, humans are a type of �superorganism� which is composed of human body and symbiotic microorganisms [4]. According to researchers, human diseases are not only body related and thus the commensal microbiota in human health and disease must also taken into consideration [4].
The human microbiome can be divided into a �core� microbiome and a �variable� microbiome (Figure 1), [8, 9]. The core microbiome is common to all or vast majority of humans, consists of certain predominant species/types of microorganisms which are present in the healthy conditions at different regions of the human body [8, 9]. It makes up about 70% of the total bacterial population [10]. The variable microbiome is formed by a temporary population of microorganisms. It creates individuality and may be due to a combination of several factors such as host genotype, host physiological status including the properties of the innate and adaptive immune systems, host pathobiology � disease status, host lifestyle including diet, host environment and the presence of transient populations of microorganisms that cannot persistently colonize a habitat [8]. Analyzing the human microbiome the above factors must be taken into consideration. Although individual parts of microbiota are at similar sites of the body, there are differences at the species/strain level of the microbiome that can be as unique to the individual as the fingerprint is [9].
The vaginal microbiome plays a fundamentally important role in health and disease, yet this ecosystem remains incompletely characterized and its diversity poorly define. The vaginal microbial flora is thought to provide protection against infection by means of a number of different mechanisms [11]. They are colonization resistance mechanism and active production of various antimicrobial compounds, which stimulate an immune response. Disturbances in the composition of the vaginal microbiota may promote bacterial vaginosis (BV) and increase the risk of urinary tract infections and sexually transmitted infections (STIs), including the acquisition of human immunodeficiency virus (HIV) or Neisseria gonorrhoeae [11-13]. The occurrence of bacterial vaginosis in women of reproductive age is associated with an increased risk of pelvic inflammatory disease (PID), endometritis, and infertility [11, 13, 14]. In pregnant women, BV increases the risk of post-abortal sepsis, early miscarriage recurrent abortion, late  miscarriage, preterm prelabor rupture of membranes (PPROM), spontaneous preterm labor (SPTL), ectopic pregnancy and preterm delivery of low birth weight infants, histological chorioamnionitis and postpartum endometritis [11,13]. As a result, abnormal changes in the vaginal microbiota may predispose to ascending colonization of the genital tract (pelvic inflammatory disease, PID), infiltration of the fetal membranes, microbial penetration of the amniotic cavity and fetal damage [11]. Preterm birth of infectious etiology is associated with high perinatal mortality and morbidity, and a high cost to the healthcare system [11]. So far, most of information about the composition of the vaginal flora comes from cultivation-dependant techniques [11]. In recent years, the development and introduction of cultivation-independent molecular-based techniques have provided new information about the composition of normal vaginal flora as well as abnormal colonization of the genital tract which complements existing knowledge from cultivation-dependent techniques [11]. 
Recently published studies showed that the vaginal microbiome is heterogeneous within an individual but this is just the beginning [14, 15]. Although two recent work have examined racial differences and host genotype in vaginal microbial communities, the impact of other variables that might contribute to microbiome composition and diversity, such as age, race/ethnicity, other socio-demographics, medications, medical conditions, sexual activity, hygiene or hormone status (normal menstrual cycle, contraception, pregnancy, menopause) is still unknown [14, 15]. For example, Zhou et al. studied differences in the composition and structure of bacterial communities in the vaginas of Caucasian and black women in North America. Researchers found differences in the composition of the vaginal flora in these ethnic groups, which may account for the differential risk to BV and various vaginal infections [14].  It is therefore necessary for additional high-throughput genomics-based approaches to characterize the vaginal microbiome [16]. New information of vaginal microbiome might help to elucidate the composition and function of normal vaginal flora, and microbial diversity, diagnosis and treatment assessment in various pathological conditions in gynecology and obstetrics [11]. 

Human Microbiome Project
The Human Microbiome Project (HMP) was launched by the National Institutes of Health (NIH) in 2007 in order to the characterize the human microbiome in five different body sites � the nasal passages, the oral cavities, the gastrointestinal tract, the urogenital tract, and the skin, and to analyze its role in health and disease [6]. It is essential to understand the role of microbial genes that influence the metabolic and physiological processes and predisposition of morbidity to various diseases [6]. Currently, many researchers have focused on the composition and function of the intestinal microbiota and the relationship between intestinal microbiota and metabolic diseases including obesity, metabolic syndrome, diabetes and intestinal disorders such as inflammatory bowel disease, irritable bowel syndrome or colorectal cancer [4].
One of the priorities of the HMP is to understand the human microbiome using new DNA sequencing technology obtained from samples taken from different areas of the body from healthy volunteers, and to determine whether the composition of microbiome is releted to the health status [6]. This is to provide a reference database of genome and metagenome sequences and an estimation of the microbial community structure at different body sites in healthy individuals [16].
	Vaginal Human Microbiome Project has been funded as a part of Human Microbiome Project and was undertaken to define more completely the human vaginal microbiome in health and disease. The aim of these project is to investigate whether genes of the host contribute to the composition of the vaginal microbiome and which changes in the vaginal microbiome are associated with common infectious diseases and non-infectious pathological host [6]. In the project thousands of woman from relevant clinical settings will be tested to determine the relationship between the vaginal microbiome and different physiological and infectious conditions; and hundreds of monozygotic and dizygotic twins will be examined to assess the influence of genetic and environmental factors on the composition of the vaginal microbiome [17]. To test the vaginal microbiome 16S rRNA genes, metagenome and metatranscriptome sequencing utilizing next-generation sequencing technologies and other molecular techniques are used in combination with metabolomics. The aim was to assess the diversity of microbial species, genes, and functions of the microbiome associated with these samples [6]. 
Discovering the factors that influence the qualitative and quantitative composition of microorganisms and their interactions with the host may in the future contribute to improving the condition of the host due to monitoring and manipulation of it�s microbiome [8]. 

Techniques for analyzing vaginal microbiome
	Most of our current knowledge of the human microbiome came fromstudies based on the isolation and phenotypic identification of microorganisms (�traditional culture�based techniques�), [11,12]. The introduction of genotyping methods, including sequence analysis of a highly conservative region of the small ribosomal subunit of the 16S rRNA gene showed that we are not able to cultivate 60% to 80% microorganisms that make up the human microbes [11, 18]. The 16S rRNA gene is useful because it is present in all bacteria and yet also has areas of heterogeneity which can be used to identify bacteria or to infer phylogenetic relationships [11]. Traditional cultivation-based studies have the disadvantage that they may fail to isolate or detect large numbers of fastidious microorganisms, or identification tests may not be available [11]. An unknown number of species which are identified by molecular methods are cultifiable, but have not been identified by cultivation methods because of the lack of phenotypic tools for the species or inappropriate media [11]. 

Molecular research of vaginal microbiota is based on nucleic acid extraction, amplification, and sequencing of variable regions of the 16S rRNA gene using oligonucleotide primer sequences [19]. All of the bacteria present in the specimen are represented by the PCR amplicons. The resulting isolated 16S rRNA amplicons are separated using a variety of means, then sequenced and sequenced fragments are checked and compared to the web databases such as the Ribosomal Database Project (RDP), [19]. The sequences for which close matches have not been found are likely to be previously unknown organisms. The methods used for the separation of the amplicons for sequencing vary widely [19]. Early studies were carried out using denaturing gradient gel electrophoresis (DGGE) to separate amplicons. Amplicons forming distinct bands in the gels are sampled, re-amplified, and then sequenced. DGGE-based studies led to the discovery of new microorganisms as belonging to the vaginal microbiota not previously recognized by the cultivation-dependent techniques, for example Atopobium vaginae and Lactobacillus iners [19-21]. 
Many bacterial 16S rRNA gene-dependent methods, including ribosomal intergenic spacer analysis (RISA), and terminal restriction fragment length polymorphism (TRFLP), DNA microarray and fluorescence in situ hybridization (FISH), have emerged as molecular techniques; however, the information obtained with the above methods is limited [4]. The new high-throughput molecular-based techniques has opened new avenues in the knowledge of the phylogenetic framework of the human microbiota. They also allow the identification of new, previously uncategorized vaginal bacterial populations [18]. 

Healthy vaginal microbiota
	Culture and microscopy (Gram staining) of normal vaginal flora typically shows a predominance of Lactobacillus species [11, 22]. Prior to the development of molecular-based techniques, vaginal Lactobacillus were generally identified by culture-dependent methods only to the genus level [11].  
The first reports on the presence of vaginal microbiota date from 1892 when Albert D�derlein reported on the presence of Gram-positive, nonspore-forming rods, and high morphological variation [23]. By 1980, it was believed that the vaginal flora was dominated by Lactobcillus acidophilus species (bacillus D�derlein's), [23]. However, further studies using a variety of molecular based techniques allowed the isolation of the nine species in the complex L. acidophilus: L. acidophilus, Lactobacillus amylolyticus, Lactobacillus amylovorus, Lactobacillus crispatus, Lactobacillus gallinarium, Lactobacillus gasseri, Lactobacillus iners, Lactobacillus jensenii, and  Lactobacillus johnsonii (Table 1), [22, 24]. 
Cultivation-based methods and identification based on biochemical characteristics do not detects the presence of various species of the Lactobacillus in vaginal. For example, selective media such as Rogosa medium or MSR agar (Man, Rogosa and Sharpe medium) are normally used to culture lactobacilli, so the use of cultivation-based techniques, even those followed by molecular methods, will not detect L. iners because it only grows on blood agar [23]. Based on molecular methods (polymerase chain reaction and denaturing gradient gel electrophoresis) a lactic acid producing bacterium � L. iners, coming from the vaginal swab of healthy postmenopausal women was first isolated [21]. Numerous studies show that L. iners is one of the most often isolated species from vaginal mucus of healthy women in reproductive age [11]. In contrast to L. crispatus, which is rarely dominant in BV, L. iners can be detected at high levels in most subjects with and without BV, and in three studies it was the only Lactobacillus species detected in BV positive women [25-28]. This indicated that L. iners may be better adapted to the conditions associated with BV, i. e. the polymicrobial state of the vaginal flora and elevated pH [11]. 
	Recent studies of the vaginal microbiome based on the molecular methods suggest that Lactobacillus species do not predominate in healthy women of reproductive age. The vaginal microbiota of a significant proportion of healthy women might be colonized by other species such as Megasphaera, Atopobium, Leptotrichia. However, several studies indicate that Atopobium species may be associated with BV [29].  
	Ravel et al. showed that the vaginal microbiota can be divided in five major microbial communities (designated I, II, III, IV, and V) based on samples from four ethnic groups: white, black, Hispanic, and Asian in North America. The most diverse communities were those of group V. In addition to these groupings, there were two singletons: one was dominanted by Lactobacillus � about 99% of the community, and the other by Enterococcus spp. � about 79% of the community [30]. The microbial communities belonging to group I (26,2%), II (6,3%), III (34,1%), and V (5,3%) were dominated by L. crispatus, L. gasseri, L. iners, and L. jensenii, respectively and were isolated mainly from white and Asian women. The remaining 27% of women forming community group IV, mainly black and Hispanic, were found to be part of a large heterogeneous group. Group IV was characterized by strictly anaerobic bacteria, including Prevotella, Dialister, Atopobium, Gardnerella, Megashaera, Peptoniphilus, Sneathia, Eggerthella, Aerococcus, Finegoldia, and Mobiluncus. Interestingly, communities dominated by species of Lactobacillus other than L. crispatus have slightly higher pH, ranging from 4.4 (group III) to 5.0 (group II), indicating that these communities as a whole might not produce as much lactic acid as those of group I or might have different buffering capabilities [30]. 

Lactobacillus spp. protects against pathogens by producing antimicrobials, such as lactic acid, hydrogen peroxide (H2O2), antibiotic toxic hydroxyl radicals, bacteriocins, and probiotics [11, 31]. 
The lactic acid production by Lactobacillus species is important defense mechanism that prevents the growth of acid-sensitive bacterial species, such as those associated with BV [17].  
Lactobacilli differ in their ability to produce H2O2 and in the prevalence and concentration of H2O2 is associated with the development of BV and vaginal infections [17]. By molecular methods, we can evaluate the production of H2O2 to individual species or strains of the same species of Lactobacillus rather than the genus as a whole [32-34].
Song et al. showed in Japanese healthy women that the predominant lactobacillus species were L. crispatus, L. gasseri, and L. vaginalis. All strains of L. crispatus were exclusively strong H2O2 producers, whereas 41% and 59% of L. gasseri strains were strongly and weakly positive for H2O2 respectively [33]. 
Other studies indicate that the L. crispatus in particular is known to produce hydrogen peroxide, which together with host myeloperoxidase and halide ions (chloride), forms strong toxic oxidants harmful to other invading microorganisms [29]. 
The reports suggested that H2O2 � produced by Lactobacillus species in the vagina may have protective effect against vaginal colonization by pathogenic microorganisms, such as those that cause bacterial vaginosis [34]. Moreover, H2O2 is able to reduce the incidence of ascending infections of the uterus and the subsequent production of proinflammatory molecules which are important in the pathogenesis of preterm birth and chorioamnionitis [34]. This hypothesis is supported by Wilks et al. The researchers report the identification and H2O2 production of lactobacilli isolated from vaginal swabs collected at 20 weeks' gestation from a population of pregnant women at high risk of preterm birth. The Wilks et al. also report the correlation between identification and H2O2 production in relation to the outcomes of chorioamnionitis and preterm birth. Lactobacilli were identified by partial 16S rRNA gene sequencing and H2O2 production was determined by a semiquantitative method. The most commonly isolated species were L. crispatus, L. gasseri, L. vaginalis and L. jensenii. Amounts of H2O2 produced by lactobacilli varied widely. The presence of lactobacilli producing high levels of H2O2 in the vagina of this population of pregnant women was associated with a reduced risk of bacterial vaginosis at 20 weeks' gestation and subsequent chorioamnionitis. L. jensenii and L. vaginalis produced the highest levels of H2O2 [34].
The absence of H2O2-producing lactobacilli may be associated with several unhealthy vaginal conditions and states including bacterial vaginosis, vaginal colonization of pathogens, preterm birth, and endometriosis [17]. 
In vaginal Lactobacillus strains also produce bacteriocins � antibacterial peptides that, like lactic acid, induce membrane permeabilization of Gram-negatives. So far, two types of bacteriocins have been identified. One of the bacteriocins, known as lactocin 160, has been shown to target the cytoplasmic membrane of G. vaginalis, suggesting that it is likely to be a biologically relevant defense mechanism [17]. 
Lactobacillus species are thought to compete for binding to receptors on vaginal epithelial cells (vaginotropism) and numerous researches have demonstrated that they can inhibit adherence of urogenital pathogens including Staphylococcus aureus, Streptococcus agalactiae, Gardnerella vaginalis, Neisseria gonorrhoeae, Escherichia coli, Klebsiella pneumonia, Pseudomonas aeruginosa, and Candida albicans [17, 31]. 
In addition, the natural defense mechanisms of the vagina include production of endogenous defensins (including HNP1�3), secretory leukocyte protease inhibitor (SLPI), cytokines, and endocervical mucous ant they also protect against infections [35]. 
The vaginal epithelium and microbiota vary considerably across periods of a woman's life and is closely correlated with the activity of the hormone � estrogen (Figure 2), [17, 36]. In premenarchal girls the vaginal microbiota is composed of anaerobic and aerobic bacteria, mostly similar to that of the skin and the periurethral area and the vaginal pH is alkaline or neutral [29]. Another step in characterized by a gradual change of this microbiota when the estrogen level increases � the vaginal epithelium will thicken and become loaded with glycogen that by endogenous degradation will result in pH close to 5 [29]. The acidity and high concentration of glycogen in the stratified vaginal epithelium will favor rectal Lactobacillus spp., mostly from the gut microflora, to colonize the vagina and will achieve a number of 107-108 per gram vaginal fluid [29]. Acidic environment of the vagina maintains the appropriate pH (<4.5), which also inhibits the proliferation of pathogenic microorganisms and stimulates the immune system [17]. As estrogen levels gradually decline during menopause, the glycogen content in vaginal epithelial cells also declines, leading to a varying degree of depletion of Lactobacillus species [17]. 

Vaginal microbiota during bacterial vaginosis
 	Bacterial vaginosis (BV) is a gynecologic condition of unknown etiology and is traditionally characterized by a relatively low abundance of vaginal Lactobacillus spp. accompanied by polymicrobial anaerobic overgrowth including G. vaginalis, Prevotella spp., Mobiluncus spp., Ureaplasma urealyticum, and Mycoplasma hominis. However, the majority of bacterial species (>99%) have not been cultivated in the laboratory. Molecular approaches now enable their identification [37]. In the past several years, investigators used 16S rRNA gene sequence-based analysis to study the vagina microbiome [37]. These studies have found a multitude of bacteria that could not be identified by traditional culture-based methods. Recently, molecular studies have shown that Atopobium vaginae, Megasphaera, members of the candidate division TM7, Eggerthella-like uncultured bacteria, and three newly described members of the Clostridiales order have high specificity for BV [37]. 
Fredricks et al. have used molecular methods to identify several uncultivated microorganisms which are highly specific indicators of BV. The BV-associated bacteria in the Clostridiales order � BVAB1, BVAB2, BVAB3 were identified using broad-range 16S rRNA assays, and they were validated using a combination of fluorescence in situ hybridization (FISH) and bacterium-specific polymerase chain reaction (PCR). These bacteria represent the large variety of microbes that are present in microbiota of women with BV, but it is not yet known whether these microorganisms are single pathogens that cause BV or whether BV is caused by complex communities of bacteria. Under fluorescence microscopy, BVAB 2 appeared to be a short, straight rod that was wider than BVAB1, whereas BVAB3 was relatively long, wide, straight, lancet-shaped rod [26]. 
BV occurs in 33% to 36% of women attending sexually transmitted disease clinics, 16% to 20% of pregnant women, and in up to 25% of women attending gynaecologic outpatient clinics [38]. BV occurs more frequently among women who report sex with other women, and those who report new or a higher number of male sex partners. Other risks include douching, intrauterine device, Black race, hormonal contraception, smoking, menses, and chronic stress [35]. 
Clinically, bacterial vaginosis is diagnosed by the presence of three of the following four criteria (Amsel�s criteria): 1. presence of thin, gray-white homogenous vaginal discharge, 2. A positive KOH whiff test � the release amine odor following addition of 10% potassium hydroxide KOH to vaginal secretions, 3. presence of clue cells (vaginal epithelial cells with indistinct borders due to attached bacteria) in the vaginal fluid, and 4. vaginal pH value greater than 4.5 [13, 17, 37]. Alternatively, BV can be diagnosed using the Nugent criteria, which involves scoring Gram-stained vaginal smears to quantify bacterial populations. It has been shown to correlate well with clinical criteria and its an effective way to screen for asymptomatic BV [17]. It is estimated that asymptomatic BV occurs in 50% of all women with BV. 
Nugent score as a 1-10 point scoring based on the shift from a predominance of Lactobacillus spp. with few other morphotypes (grade I: scores 1-3 = negative) to a more mixed flora (grade II: scores 4-6 = intermediate) to a predominance of Gardnerella spp., and Gram-negative anaerobic bacterial morphotypes including Mobiluncus (grade III: scores 7-10 = positive), [29]. Nugent scoring is recommended to be used in research studies because of its reproducibility. The sensitivity and specificity of the Amsel criteria is 70% and 94% respectively, when compared with Nugent score [37]. 
Epidemiologically studies demonstrated that BV is associated with an increased risk of gynecologic and obstetric complications. Gynecologic conditions associated with BV include pelvic inflammatory disease (PID), postoperative infection such as postabortion endometritis and pelvic cuff cellulitis following hysterectomy, cervicitis, sexually transmitted infections, including human immunodeficiency virus (HIV), and possibly cervical intraepithelial neoplasia (CIN), [16, 38]. Transmission of sexually transmitted infections is also associated with BV, since BV increases viral replication and vaginal shedding of HIV-1 and herpes simplex virus type 2 (HSV-2), [37]. The obstetrical risks associated with BV include premature rupture of membranes, preterm labor and delivery, chorioamnionitis, and pastpartum endometritis [24, 38]. BV has a strong positive association with preterm birth. However, the pathophysiologic pathways linking BV and preterm birth are still unclear and are the focus of much current research [37, 39]. 
Specific organisms found in BV are associated with an increased incidence of spontaneous preterm birth. Mycoplasma hominis and Ureaplasma urealyticum have been isolated from the cord blood of approximately 23% of neonates born at less than 32 gestational weeks [39]. Approximately 10% to 15% of women with BV experience preterm birth. The risk of preterm delivery is increased regardless of whether the women are symptomatic or asymptomatic. However, most women who have BV, diagnosed either clinically or microscopically, do not give birth preterm. Recent theories posit a gene-environment interaction between BV and preterm birth [37, 39, 40] . 
There are several possible factors that may operate independently or in combination to increase the risk of preterm birth in women with BV [39]. Microorganisms associated with BV may ascend from the lower genital tract to the upper genital tract, leading to premature rupture of membranes, chorioamnionitis, and subsequent preterm birth [39]. Next factors are proteolytic enzymes produced by BV associated microorganisms in the vagina and they may alter the permeability of the mucosal epithelium, permitting ascending infection by other, more pathogenic bacteria [39]. The local innate immunity regulates the response within the vagina and cervix to the presence of BV microorganisms through a network of pro-inflammatory cytokines, chemokines, and growth factors. The differential risk of preterm birth associated with BV may be related to immune hyporesponse or hyperresponse. Hyporesponse may lead to ascending infection, whereas hyperresponse may experience more inflammatory pathways to preterm delivery [37, 39].  
Although BV itself is not usually an inflammatory condition, many women with abnormal vaginal microbiota who give birth prematurely have a concomitant inflammatory process. Leukocytes are not typically seen in the vaginas of women with BV. However, proinflammatory cytokines, such as interleukin 1, may be present. Increased inflammatory cytokines are involved in local prostaglandin production, which may trigger preterm labor [42, 42]. 

In conclusion, the microbiome of the vaginal plays an important role in health and disease, promoting more comprehensive study. The improvements in cultivation techniques and the development of molecular-based identification methods have enabled us to recognize that the microbiota of the female genital tract is extraordinarily complex and dynamic in nature, with significant inter-individual variability. Detailed knowledge about the vaginal microbiome and factors affecting its composition will help explain the pathophysiology of important perinatal conditions, including preterm birth, and will likely lead to new strategies to prevent infection-related morbidity in women and newborns.

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&Fd��a$gd�u�Cauci S, Culhane JF, Di Santolo M, McCollum K (2008) Among pregnant woman with bacterial vaginosis, the hydrolytic enzymes sialidase and prolidase are positively associated with interleukin-1 beta. Am J Obstet Gynecol 198: 1-7.




	 








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