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Nugent Score Related to Vaginal Culture in Pregnant Women

From the Departments of Medicine and Pathology, Channing Laboratory, Brigham and Women’s Hospital and Harvard Medical School, Boston, Massachusetts.

Address reprint requests to: Mary L. Delaney, MS, Channing Laboratory, Departments of Medicine and Pathology, Brigham and Women’s Hospital, 181 Longwood Avenue, Boston, MA 02115; E-mail: mdelaney{at}rics.bwh.harvard.edu

	ABSTRACT

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
OBJECTIVE: To relate Gram-stained smears, using the Nugent criteria, to quantitative and qualitative vaginal cultures in pregnant women.

METHODS: Two independent evaluators using the Nugent criteria, a standardized method of Gram-stain interpretation designed to detect bacterial vaginosis, scored 104 vaginal smears from pregnant women. The quantitative and qualitative vaginal cultures were assessed at the same time and the results expressed as log₁₀ colony-forming units per gram of vaginal secretion. The Nugent scores were compared with the microbiologic findings.

RESULTS: The prevalence of normal, intermediate, or bacterial vaginosis vaginal flora as determined by Gram stain was 68%, 21%, and 11%, respectively. A comparison of the mean bacterial counts with the Nugent score showed a weak negative correlation for Lactobacillus species and a positive correlation for gram-variable and gram-negative rods. Additional analysis revealed a strong positive correlation between the mean bacterial counts analyses of Peptostreptococcus, a genus not included in the Nugent scoring system, and the Nugent score. In addition, the Prevotella counts correlated strongly with both the Nugent score and the Peptostreptococcus counts. The quantitative counts for Lactobacillus did not vary significantly among the three defined groups of vaginal microflora; however, significant increases in the concentrations of Gardnerella vaginalis and Prevotella were found as the Nugent score increased.

CONCLUSION: A strong correlation was found among the gram-variable and gram-negative genera comprised by the Nugent score. Peptostreptococcus also correlated strongly with the Nugent score and with the Prevotella counts, suggesting that this genus may play a role in determining vaginal health.

The vaginal microflora is a complex ecosystem in which both the microorganisms present and their concentrations are indicative of the vaginal health of the individual. Bacterial vaginosis (BV) affects 10–15% of women of reproductive age and has been associated with a variety of genital tract infections and pregnancy complications,^1–6 including pelvic inflammatory disease, premature rupture of membranes, preterm labor and delivery, and postpartum infection. Bacterial vaginosis has been defined as a complex microbiologic condition characterized by a shift in the vaginal flora from the dominant Lactobacillus species to a polymicrobial flora that includes Gardnerella vaginalis, Prevotella, Peptostreptococcus, Mobiluncus, Mycoplasma hominis, and Ureaplasma urealyticum. The clinical diagnosis of BV requires that three of the following four criteria be present: an elevated vaginal pH (greater than 4.5); adherent white vaginal discharge; vaginal epithelial cells covered with adherent bacteria, "clue cells," in a wet mount preparation; and the release of volatile amines by the addition of potassium hydroxide to a small amount of vaginal fluid.⁷ As an alternative to the clinical diagnosis of BV, the evaluation of vaginal smears has been used to assess the health of vaginal microflora. The Nugent criteria form a standardized method of Gram-stain interpretation designed to evaluate the vaginal microflora to detect BV.⁸ Vaginal swab smears are graded on a 10-point scale based on the presence or absence of Lactobacillus morphotypes, gram-variable and gram-negative rods, and curved gram-negative rods. The criteria were designed to provide a scoring system to evaluate the alteration in vaginal microflora from the normal to the abnormal BV state as a continuum rather than a dichotomy. In the present study, quantitative and qualitative vaginal cultures were done and vaginal smears were evaluated according to the Nugent criteria. The correlations between the bacterial counts and Nugent score and among the various genera associated with BV are presented.

	MATERIALS AND METHODS

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This study was conducted as part of a larger project collecting quantitative data on the microbiologic population in pregnant women in two high-risk cohorts for preterm delivery (prior preterm birth and bleeding during the current pregnancy) and a low-risk cohort (no prior preterm birth or bleeding) to formulate a model to determine the bacteriologic factors promoting preterm labor. Eligible women were identified by the study nurse and approached during routine antenatal care visits at the outpatient clinic of the Brigham and Women’s Hospital (Boston, MA). After written informed consent was given, vaginal samples were obtained from 104 pregnant women at 20 weeks of gestation. Women were excluded from the study for any of the following reasons: age younger than 15 years, language barrier, in vitro fertilization, multiple gestation, previous pregnancy loss at less than 24 weeks’ gestation because of sepsis, progesterone suppository use, renal disease, antimicrobial therapy within 4 weeks of initial sampling, cervical cerclage, placenta previa, Rh isoimmunization, chronic hypertension with medication, pregnancy-induced hypertension, insulin-requiring diabetes, or steroid use. The demographic data, including age, race, educational level, and insurance coverage, are provided in Table 1.

The vaginal samples for microbiologic culture were obtained by the double swab technique.⁹ In brief, the study nurse inserted two swabs simultaneously into the vaginal vault. The swabs were rotated against the upper vaginal walls to achieve saturation and carefully removed. The preweighed swab was returned to the sterile preweighed tube and the other swab was placed in 10.5 mL of prereduced Amies transport medium without charcoal (PML Microbiologicals, Tualatin, OR). Both swabs were transported to the microbiology laboratory for processing within 2 hours. The preweighed swab and tube were reweighed, and the difference was recorded as the sample weight. The swab samples were passed into an anaerobic chamber (Coy Laboratory Products, Grass Lake, MI) and agitated on a vortex mixer for 3–5 minutes until the sample was completely dispersed. Serial dilutions of the sample were made in phosphate-buffered saline, and the undiluted sample, as well as aliquots of each dilution, were plated onto various selective and nonselective media. The culture media for recovering anaerobes were prereduced brucella-base agar with 5% sheep blood enriched with hemin and vitamin K₁ and prereduced brucella-base agar with 5% laked sheep blood, 100 µg/mL kanamycin, and 7.5 µg/mL vancomycin and supplemented with hemin and vitamin K₁. The media for the recovery of the facultative anaerobes were 5% sheep blood in tryptic soy agar and mannitol salt agar. Chocolate agar was used for the recovery of G vaginalis (PML Microbiologicals). Anaerobic culture plates were incubated in an anaerobic chamber for a minimum of 120 hours at 35C before enumeration. Tryptic soy agar and mannitol salt agar plates were incubated in air and chocolate agar plates in 5% carbon dioxide for 48 hours. After incubation, the various colony types were enumerated, isolated, and identified by established criteria.¹⁰ Gram-negative or gram-variable, catalase-negative pleomorphic rods were presumptively identified as G vaginalis, and identification was confirmed by the Microbial Identification System (Microbial ID, Newark, DE). Gram-positive, catalase-negative microaerophilic or anaerobic bacilli that produced a large amount of lactic acid, as determined by gas-liquid chromatography, were classified as Lactobacillus species without being further identified. Obligate anaerobes were classified by gas-liquid chromatographic analysis of glucose fermentation products, and the final identification was performed with the Microbial Identification System or the Rapid ANA II system (REMEL, Norcross, GA). All estimates of population size were expressed as log₁₀ colony-forming units per gram of vaginal secretions (log₁₀ cfu/g).

After identification, Lactobacillus isolates for each sample were tested for production of H₂O₂ by a modified method described previously by Eschenbach et al.¹¹ Each isolate was inoculated onto MRS agar containing tetra methyl benzidine hydrochloride hydrate (0.375 mg/mL, Sigma, St. Louis, MO) and horseradish peroxidase (1 mg/mL, Sigma) and incubated in an anaerobic chamber for 2–3 days. The plates were removed from the chamber and exposed to ambient air. The presence of H₂O₂ was detected by the production of a blue pigment in and surrounding the H₂O₂-producing colonies.

The bacterial concentrations for the various groups were compared by one-way analysis of variance (Instat, Graph Pad Software, San Diego, CA). Linear regression analysis was used to determine the correlation between the Nugent score and the bacterial concentrations (Statistica, Statsoft, Tulsa OK).

	RESULTS

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Of the 104 smears examined using the Nugent criteria, 71 (68%) were graded as normal, 22 (21%) as intermediate, and 11 (11%) as BV. The mean counts for the individual components comprising the Nugent score were determined. The mean count for Lactobacillus was 9.08 ± 0.50 log₁₀ cfu/g, 8.81 ± 0.80 log₁₀ cfu/g, 8.55 ± 0.84 log₁₀ cfu/g, 8.75 ± 0.58 log₁₀ cfu/g, and 8.30 ± 0.80 log₁₀ cfu/g for a Nugent score of 0, 1, 2, 3, and 4, respectively. The gram-variable and gram-negative score comprised G vaginalis and Prevotella. The mean count for G vaginalis was 5.90 log₁₀ cfu/g, 8.04 ± 0.55 log₁₀ cfu/g, 7.10 ± 2.30 log₁₀ cfu/g, 8.04 ± 0.58 log₁₀ cfu/g, and 9.12 ± 1.00 log₁₀ cfu/g for the corresponding Nugent score of 0, 1, 2, 3, and 4, respectively. For Prevotella, the count was 4.98 ± 0.70 log₁₀ cfu/g, 4.65 ± 1.01 log₁₀ cfu/g, 4.97 ± 1.07 log₁₀ cfu/g, 4.80 ± 0.81 log₁₀ cfu/g, and 7.81 ± 1.56 log₁₀ cfu/g for the corresponding Nugent score of 0, 1, 2, 3, and 4, respectively. Mobiluncus was not detected by culture because the culture methods used were not adequate for the optimal detection of this fastidious organism when not part of the dominant microflora. Nevertheless, Mobiluncus was seen in 15 of the Gram stains: 2 with Nugent scores in the normal range, 4 with intermediate scores, and 9 with BV scores. A grade of 2 (5–30 morphotypes per field) was assigned to three of the nine smears with total scores in the BV range, one smear with a total score of 9, and two smears with a total score of 10.

The mean log counts and the frequency of isolation for the various genera that make up the total Nugent score and Peptostreptococcus, a genus associated with BV, are shown in Table 2. The mean log count for Lactobacillus varied little among the different groups. In contrast, for both G vaginalis and Prevotella, the counts increased significantly as the total Nugent score increased. The mean count for G vaginalis in the normal, intermediate, and BV groups was 7.22 log₁₀ cfu/g, 8.43 log₁₀ cfu/g, and 9.64 log₁₀ cfu/g, respectively. The G vaginalis counts in BV group were significantly higher than those in the normal group (P < .001) and the intermediate group (P < .05). The mean log count for Prevotella was 4.73 log₁₀ cfu/g, 6.38 log₁₀ cfu/g, and 8.42 log₁₀ cfu/g for the normal, intermediate, and BV groups, respectively. The Prevotella counts were significantly different among the three groups (P < .01 for normal versus intermediate and P < .001 for BV versus normal or intermediate). The mean log count for Peptostreptococcus, which is not a component of the Nugent score, also increased significantly as the total Nugent score reached values indicative of BV. Again, the differences were statistically significant among the groups (P < .001 for normal versus BV and P < .05 for intermediate versus BV). The mean vaginal pH increased from 4.53 in the normal group to 5.50 in the BV group. The pH in the normal group was significantly lower than in the intermediate (P < .05) or BV group (P < .01). Also the pH values for the intermediate group were significantly lower than those for the BV group (P < .01).

View this table: [in this window] [in a new window]   Table 2. Mean Counts,* Frequency of Isolation, and pH for Vaginal Cultures Categorized by Nugent Score

The frequency of isolation for Lactobacillus, G vaginalis, Prevotella, and Peptostreptococcus are shown in Table 2. Lactobacillus was isolated as the dominant microflora most frequently in the normal group (97%) and decreased to 82% in the BV group. The frequency of isolation for G vaginalis increased dramatically from the normal group to the intermediate and BV groups (8%, 54%, and 91%, respectively). Prevotella was isolated in 91% of the BV group samples and in 41% and 32% of the normal and intermediate group samples, respectively. The frequency of isolation for Peptostreptococcus also increased as the Nugent score increased (59%, 59%, and 82% corresponding to the normal, intermediate, and BV groups, respectively). The frequency of isolation for the various genera varied significantly among the groups tested.

The proportion of H₂O₂ nonproducing strains of Lactobacillus did not differ significantly among the three groups (28%, 23%, and 36% for the normal, intermediate, and BV groups, respectively). However, the proportion of H₂O₂ producing strains of Lactobacillus either alone or together with H₂O₂ nonproducing strains decreased significantly from 65% and 64% in the normal and intermediate groups, respectively, to 0 in the BV group (P < .001). This result could be inexact because five of the nine Lactobacillus strains from the BV group could not be tested for H₂O₂ production because they were not viable at the time of testing.

The percentage of each bacterial component (Lactobacillus, G vaginalis, and Prevotella) of the Nugent score based on the total bacterial count, calculated by adding the mean log count of each component, was determined. The total count for the normal group primarily comprised Lactobacillus (98%), and the BV group comprised G vaginalis (80%). Although the mean count for Lactobacillus remained similar among the groups, the proportion of the total count corresponding to Lactobacillus decreased dramatically (98%, 63%, and 15% for the normal, intermediate, and BV groups, respectively). In contrast, the mean count of G vaginalis, as well as the proportion of the total count comprised by G vaginalis, increased dramatically (2%, 36%, and 80% for the normal, intermediate, and BV groups, respectively). The proportion of the total count attributable to Prevotella increased from less than 0.001% in the normal and intermediate groups to 5% in the BV group.

We compared the total Nugent score with the highest recorded quantitative result for each specimen. The best correlation was between the Prevotella counts and the Nugent score (r² = 0.73), followed by the correlation between the G vaginalis counts and the Nugent score (r² = 0.59). Only a very weak negative correlation was found between the Lactobacillus count and the total Nugent score (r² = -0.11). It is interesting that the correlation between the Peptostreptococcus count and the Nugent score yielded a correlation of r² = 0.48. This observation suggests that Peptostreptococcus, although not specifically scored by the Nugent system, may, in fact, be present in substantial numbers during BV. In examining the correlations among the various genera associated with BV, a strong correlation was noted between Prevotella and Peptostreptococcus (r² = 0.77) and a lesser correlation between G vaginalis and Prevotella (r² = 0.59).

	DISCUSSION

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
The vaginal microflora associated with BV during pregnancy has been evaluated by a number of investigators.^12–16 The methods used in these studies to assess the bacterial load have included vaginal swabs diluted in transport media or vaginal wash samples plated directly onto various media. None of these methods provide a denominator for comparing the bacterial counts. In vaginal wash samples, an inherent variability exists because vaginal fluids are randomly diluted depending on the amount of vaginal fluid present before the introduction of saline into the vaginal vault. This variability is also present for vaginal swabs because the amount of vaginal fluid absorbed by the swab is not known. Nevertheless, these studies have reported that G vaginalis, M hominis, and Prevotella are the predominant bacteria isolated from women with BV. In the current study, we performed quantitative vaginal cultures to determine the actual bacterial concentrations for the three categories assigned by the Nugent score: normal, intermediate, and BV. The results demonstrated a significant increase in the counts of G vaginalis, Prevotella, and Peptostreptococcus occurred as the Nugent score approached values indicative of BV.

The intermediate grade has been described by several investigators as a mixed microbial flora acting as a transitional phase between normal and BV flora. Subsequent sampling of women in this intermediate grade revealed that some transition to normal flora and others acquire BV.^14,16 In our study, the presence of similar concentrations of Lactobacillus and G vaginalis in this group further demonstrates this transitional phase. It is the emergence of this intermediate phase that requires additional study to determine the factors that influence the vaginal microflora and lead to the initial overgrowth of G vaginalis and subsequent increases in Prevotella and Peptostreptococcus populations.

The presence of G vaginalis is not restricted to women with clinical signs of BV. In fact, G vaginalis was isolated in both the normal and intermediate groups in this study. It was not until an overgrowth of anaerobic bacteria occurred, including Prevotella and Peptostreptococcus, that the Nugent scores approached the abnormal values indicative of BV. It had been postulated by several investigators that a synergistic mechanism exists among the bacteria involved in BV.¹⁷ We earlier reported such a relationship between G vaginalis and Prevotella involving ammonia utilization.¹⁸ Our current findings also revealed a positive correlation between the bacterial counts of G vaginalis and Prevotella, further confirming the synergistic relationship between these organisms. A strong correlation was also found between Prevotella and Peptostreptococcus, indicating another possible synergistic relationship. Previous work in this laboratory has demonstrated a synergy involving amino acid use for these two genera.¹⁹

The vaginal microflora is a complex ecosystem that fluctuates during the various stages of life, including premenarche, menses, pregnancy, and menopause. Any alterations in this balance may play an important role in the development of disease. The current dogma describes Lactobacillus as the organism responsible for the control and maintenance of the vaginal microflora, and any decrease in the concentration of this genus results in an abnormal microflora. Donders et al¹² suggest that the decrease in Lactobacillus precedes the pathogenic bacterial overgrowth by G vaginalis and anaerobic bacteria. Furthermore, several investigators have postulated that H₂O₂ production by Lactobacillus regulates the growth of other organisms in the vagina.^11,20–22 In the present study, neither the quantitative counts nor the frequency of isolation of Lactobacillus varied significantly among the three defined groups of vaginal microflora; however, there did appear to be a decrease in the number of H₂O₂-producing Lactobacillus in the BV group. Furthermore, we saw significant increases in several genera, including G vaginalis, Prevotella, and Peptostreptococcus. It is the overgrowth by these pathogenic bacteria that overwhelm the normal constituents of vaginal microflora and account for the higher total bacterial counts. The Nugent scoring system represents this shift in the total score and proved to be a useful tool in evaluating the vaginal microflora. The weak negative correlation between the Lactobacillus count and the Nugent score, represented by the broad range of values for any given Nugent score, further demonstrates that Lactobacillus does not diminish significantly during BV. However, a strong positive correlation was found between the counts for G vaginalis and Prevotella and the Nugent score. The positive correlation between the Peptostreptococcus counts and the Nugent score suggests that Peptostreptococcus, although not specifically scored by the Nugent system, may be an indicator of the vaginal health of the individual during pregnancy.

	Footnotes

 
This study was supported by grant RO1 HD35667 from the National Institutes of Health.

The Microbiology and Prematurity Study Group consists of the following: Robin Ross, PhD, Mei-Ling Lee, PhD, Andrea M. DuBois, BS, Wendy Osterling, BS, and David G. Aiello, BS, Channing Laboratory, Brigham and Women’s Hospital, Boston, MA; and Ruth Tuomala, MD, Ellice Lieberman, MD, Amy Cohen, BA, Dorothy Pender, RN, and Linda Steele, MT(ASCP), Department of Obstetrics and Gynecology, Brigham and Women’s Hospital, Boston, MA.

PII S0029-7844(01)01402-8

Received October 25, 2000. Received in revised form February 2, 2001. Accepted March 8, 2001.

	REFERENCES

TOP ABSTRACT MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
1. Donders GG, Van Bulck B, Caudron J, Londers L, Vereecken A, Spitz B. Relationship of bacterial vaginosis and mycoplasmas to the risk of spontaneous abortion. Am J Obstet Gynecol 2000;183:431–7.[Medline]

2. Hillier SL, Krohn MA, Cassen E, Easterling TR, Rabe LK, Eschenbach DA. The role of bacterial vaginosis and vaginal bacteria in amniotic fluid infection in women in preterm labor with intact fetal membranes. Clin Infect Dis 1995;20(suppl 2):S276–8.

3. Hay PE, Lamont RF, Taylor-Robinson D, Morgan DJ, Ison C, Pearson J. Abnormal bacterial colonisation of the genital tract and subsequent preterm delivery and late miscarriage. BMJ 1994;308:295–8.[Abstract/Free Full Text]

4. Watts DH, Krohn MA, Hillier SL, Eschenbach DA. Bacterial vaginosis as a risk factor for post–cesarean endometritis. Obstet Gynecol 1990;75:52–8.[Abstract/Free Full Text]

5. Silver HM, Sperling RS, St Clair PJ, Gibbs RS. Evidence relating bacterial vaginosis to intra-amniotic infection. Am J Obstet Gynecol 1989;161:808–12.[Medline]

6. Martius J, Krohn MA, Hillier SL, Stamm WE, Holmes KK, Eschenbach DA. Relationships of vaginal Lactobacillus species, cervical Chlamydia trachomatis, and bacterial vaginosis to preterm birth. Obstet Gynecol 1988;71:89–95.[Abstract/Free Full Text]

7. Amsel R, Totten PA, Spiegel CA, Chen KC, Eschenbach D, Holmes KK. Nonspecific vaginitis. Diagnostic criteria and microbial and epidemiologic associations. Am J Med 1983;74:14–22.[Medline]

8. Nugent RP, Krohn MA, Hillier SL. Reliability of diagnosing bacterial vaginosis is improved by a standardized method of gram stain interpretation. J Clin Microbiol 1991;29:297–301.[Abstract/Free Full Text]

9. Onderdonk AB, Polk BF, Moon NE, Goren B, Bartlett JG. Methods for quantitative vaginal flora studies. Am J Obstet Gynecol 1977;128:777–81.[Medline]

10. Murray PR, Baron EJ, Pfaller MA, Tenover FC, Yolken RH. Manual of clinical microbiology. Washington, DC: American Society for Microbiology, 1995.

11. Eschenbach DA, Davick PR, Williams BL, Klebanoff SJ, Young-Smith K, Critchlow CM, et al. Prevalence of hydrogen peroxide-producing Lactobacillus species in normal women and women with bacterial vaginosis. J Clin Microbiol 1989;27:251–6.[Abstract/Free Full Text]

12. Donders GG, Bosmans E, Dekeersmaecker A, Vereecken A, Van Bulck B, Spitz B. Pathogenesis of abnormal vaginal bacterial flora. Am J Obstet Gynecol 2000;182:872–8.[Medline]

13. Thorsen P, Jensen IP, Jeune B, Ebbesen N, Arpi M, Bremmelguard A, et al. Few microorganisms associated with bacterial vaginosis may constitute the pathologic core: A population-based microbiologic study among 3596 pregnant women. Am J Obstet Gynecol 1998;178:580–7.[Medline]

14. Rosenstein IJ, Morgan DJ, Sheehan M, Lamont RF, Taylor-Robinson D. Bacterial vaginosis in pregnancy: Distribution of bacterial species in different Gram-stain categories of the vaginal flora. J Med Microbiol 1996;45:120–6.[Abstract]

15. Hillier SL, Krohn MA, Nugent RP, Gibbs RS, for the Vaginal Infections and Prematurity Study Group. Characteristics of three vaginal flora patterns assessed by Gram stain among pregnant women. Am J Obstet Gynecol 1992; 166:938–44.[Medline]

16. Hillier SL, Nugent RP, Eschenbach DA, Krohn MA, Gibbs RS, Martin DH, et al, for the Vaginal Infections and Prematurity Study Group. Association between bacterial vaginosis and preterm delivery of a low-birth-weight infant. N Engl J Med 1995;333:1737–42.[Abstract/Free Full Text]

17. Cauci S, Scrimin F, Driussi S, Ceccone S, Monte R, Fant L, et al. Specific immune response against Gardnerella vaginalis hemolysin in patients with bacterial vaginosis. Am J Obstet Gynecol 1996;175:1601–5.[Medline]

18. Pybus V, Onderdonk AB. Evidence for a commensal, symbiotic relationship between Gardnerella vaginalis and Prevotella biviua involving ammonia: Potential significance for bacterial vaginosis. J Infect Dis 1997;175:406–13.[Medline]

19. Pybus V, Onderdonk AB. A commensal symbiosis between Prevotella biviua and Peptostreptococcus anaerobius involves amino acids: Potential significance to the pathogenesis of bacterial vaginosis. FEMS Immunol Med Microbiol 1998;22:317–27.[Medline]

20. Hawes SE, Hillier SL, Benedetti J, Stevens CE, Koutky LA, Wolner-Hassen P, et al. Hydrogen peroxide-producing lactobacilli and acquisition of vaginal infections. J Infect Dis 1996;174:1058–63.[Medline]

21. Hillier SL, Krohn MA, Klebanoff SJ, Eschenbach DA. The relationship of hydrogen peroxide-producing lactobacilli to bacterial vaginosis and genital microflora in pregnant women. Obstet Gynecol 1992;79:369–73.[Medline]

22. Hillier SL, Krohn MA, Rabe LK, Klebanoff SJ, Eschenbach DA. The normal vaginal flora, H₂O₂-producing lactobacilli, and bacterial vaginosis in pregnant women. Clin Infect Dis 1993;16(suppl 4):S273–81.

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Services Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Delaney, M. L. Articles by Onderdonk, A. B. Search for Related Content PubMed PubMed Citation Articles by Delaney, M. L. Articles by Onderdonk, A. B.