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ORIGINAL RESEARCH |
From the Division of Adolescent Medicine, Department of Pediatrics and Department of Laboratory Medicine, University of California, San Francisco; Beaufort Naval Hospital, Beaufort, South Carolina; and Naval Special Warfare Group ONE, San Diego, California.
Address reprint requests to: Sophia Yen, MD, 3333 California Avenue, Suite 245, Box 0503, San Francisco, CA 94143; E-mail: syen{at}itsa.ucsf.edu.
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ABSTRACT |
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 ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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METHODS: A cross-sectional study of 1938 women was conducted. Self-collected vaginal swabs were applied to a colorimetric pH test card and a glass slide for Gram stain evaluation according to the Nugent criteria. Papanicolaou smears and samples for sexually transmitted diseases screening were collected during routine entry pelvic examinations.
RESULTS: Bacterial vaginosis prevalence was 27%, with 28% in sexually experienced and 18% in non–sexually experienced women (P = .001). Bacterial vaginosis prevalence was 11% in Asian/Pacific Islanders, which was lower than in other nonwhite ethnic groups (P =.004). Clinically, bacterial vaginosis was directly related to multiple sexual partners (P = .026), self-report of vaginal discharge (P = .001), self-report of vaginal odor (P < .001), and concurrent Chlamydia trachomatis infection (P = .002), and inversely related to hormonal contraceptive use (P = .013). Vaginal discharge did not achieve statistical significance in multivariate analysis. Compared with the Nugent criteria, the sensitivities and specificities for bacterial vaginosis diagnosis were as follows: colorimetric pH test: 72% and 67%; Papanicolaou smear: 72% and 79%, respectively.
CONCLUSION: Among these diverse young women, bacterial vaginosis occurs commonly in both sexually experienced and inexperienced young women and differs by race and ethnicity. The pH colorimetric test and Papanicolaou smear performed moderately well as screening tools for bacterial vaginosis. The inverse relationship of bacterial vaginosis with hormonal contraceptive use and its direct relationship with C trachomatis need further study.
Bacterial vaginosis is the most common cause of vaginal discharge in the United States.1 It is a clinical syndrome associated with the presence of a group of microorganisms rather than a single etiologic agent. Bacterial vaginosis is characterized by a shift in the vaginal flora from the normal Lactobacillus-dominant species to a mixed flora, including Gardnerella vaginalis, Bacteroides species, Mobiluncus species, and Mycoplasma hominis. Bacterial vaginosis is associated with reproductive health morbidity, including pelvic inflammatory disease,2–4 preterm birth, premature rupture of membranes,5 chorioamnionitis,6 spontaneous abortion,7 and post–gynecologic surgery infection.8 From the available studies that focus largely on sexually transmitted disease (STD) clinic patients and pregnant women, bacterial vaginosis prevalence is estimated to range from 7% among asymptomatic women attending general practice clinics9 to 46% among women attending STD clinics.10
Traditionally, bacterial vaginosis diagnosis is defined clinically by the presence of three of the four Amsel criteria: 1) vaginal pH > 4.5, 2) presence of adherent white discharge, 3) detection of "clue cells" by wet mount, and 4) presence of an amine odor after the addition of potassium hydroxide (also known as the "whiff" test).11 Additional laboratory-based methods of bacterial vaginosis diagnosis have included culture for G vaginalis, biochemical tests for metabolic by-products of vaginal bacteria (gas chromatography),11 and colorimetric tests for enzymes produced by bacterial vaginosis organisms (sialidase).12 However, these methods remain research tools and are not widely available in clinical settings. The Papanicolaou smear has also been examined as a potential tool to diagnose bacterial vaginosis because of its widespread use, but reported results have been only fair (sensitivity 32–55%).13,14
Most recently, researchers have adopted Gram stain evaluation of vaginal secretions as the gold standard for bacterial vaginosis diagnosis because of its higher sensitivity15,16 and reproducibility (r = .82)17 than the clinically based Amsel criteria.18 The best Gram method is considered to be that of Nugent et al.17 In this method, a standardized scoring system ranging from 0 to 10 points is used. However, many clinicians have not adopted this Gram stain method for diagnosis of bacterial vaginosis because it requires more time to perform and a trained laboratory technician to read the slides. Recently, new methods, such as a colorimetric pH and amine detection card, have been developed to achieve a rapid "point-of-care" diagnosis of bacterial vaginosis. These new techniques eliminate the need for microscopy to detect "clue cells,"16 which is time-consuming, and the "whiff" test, which is a subjective assessment for the presence of amines by the clinician.
Because of the evolving importance of bacterial vaginosis to women’s reproductive health and new diagnostic tools becoming available to the practitioner, we undertook this study to 1) estimate the prevalence of bacterial vaginosis by Nugent Gram stain criteria in a healthy, nonpregnant, nonclinic sample of both sexually experienced and inexperienced young women from throughout the United States, 2) examine sociodemographic factors (race or ethnicity) and clinical factors (sexual behavior, contraception, current or past STDs) associated with a bacterial vaginosis diagnosis, and 3) assess the performance of a rapid colorimetric pH test card and the Papanicolaou smear as screening methods for bacterial vaginosis compared with the Nugent Gram stain criteria.
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MATERIALS AND METHODS |
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ABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Voluntary, written, informed consent to participate in the study was obtained by female civilian research assistants before data collection. Women were free to decline participation and were not penalized in any manner if they did so. The institutional review boards of the University of California, San Francisco and the Beaufort Naval Hospital in South Carolina approved the protocol.
The participants reported their reproductive health history, including STD history and current gynecologic symptoms, on a standard clinic form before undergoing a pelvic examination in the Well Women’s Clinic. Sexual experience was defined for the purposes of this study as having had vaginal intercourse at least once.
For the first-void urine and self-collected vaginal swabs, participants received specific instructions from research assistants on the proper collection of the first-void urine (first 20 mL in a marked cup) and three self-collected vaginal swabs (insert each swab 1 to 2 inches, rotate swab around in vagina three times, and place in plastic transport tube). Self-collected low vaginal swabs are increasingly being used for STD diagnosis and screening and have been found to be more sensitive than and as specific as urine samples.19–22 One cotton swab was used for Trichomonas vaginalis detection. One of the Dacron swabs was used for bacterial vaginosis Gram stain analysis and colorimetric pH testing. The second Dacron swab was used for LCx testing (Abbott Laboratories, Abbott Park, IL) for Chlamydia trachomatis and Neisseria gonorrhoeae. The vaginal samples were transported to the clinic’s laboratory within 5 minutes of collection. Vaginal and first-void urine samples targeted for identification of C trachomatis and N gonorrhoeae were kept at 4C immediately after collection in the clinic and frozen at -70C in the hospital freezer within 24 hours of collection. They were shipped overnight air freight to the to the laboratory based at San Francisco General Hospital (J. Schachter, PhD, laboratory director) in batches, maintaining the cold chain with specialized shipping containers with dry ice.
During the routine pelvic examination, endocervical samples were obtained for C trachomatis and N gonorrhoeae with the LCx kit swabs according to the manufacturer’s directions, and endocervical samples for Papanicolaou smears were obtained with a cytobrush applied to a glass slide and fixed with a preservative spray. After the clinician collected the endocervical swabs, specimens were transported maintaining the cold chain to the Navy Hospital.
For C trachomatis and N gonorrhoeae testing, vaginal, first-void urine, and endocervical samples were processed according to manufacturer’s directions for ligase chain reaction tests (LCx). A positive on any of the samples (vaginal, first-void urine, or endocervical) was considered positive for infection with the respective organism for our analysis purposes. (It is important to note that 90% of the chlamydia tests were run by LCx before March 1, 2001, before problems with false positives were encountered due to changes by the manufacturer. All positives identified in the final 10% of samples run after March 1, 200l were retested and confirmed).
For T vaginalis testing, the second self-collected vaginal swab was tested for T vaginalis with the Trichomonas In-Pouch TV (Biomed Diagnostics, San Jose, CA) according to the manufacturer’s instructions. They were incubated in pouches at collection at 37C and read for the presence of T vaginalis at 2 and 5 days of inoculation by trained research assistants.
To diagnose bacterial vaginosis according to the Nugent Gram stain criteria (the Nugent criteria), the vaginal swabs were rolled onto glass slides within 5 minutes of the self-collection. The slides were then air-dried, stored, and transported in batches by overnight air freight on a monthly basis to the laboratory based at San Francisco General Hospital. The slides were Gram-stained and evaluated by a trained laboratory technologist (JM). The Nugent criteria score vaginal flora as normal (0–3), intermediate (4–6) and positive (7–10) for bacterial vaginosis.17 Only Gram stains with Nugent scores of 7–10 were considered positive for bacterial vaginosis.
To assess vaginal pH (FemExam pH and Amine TestCard, Litmus Concepts Inc., Santa Clara, CA), after the self-collected swab was applied to a glass slide (for bacterial vaginosis), the swab was then applied to the FemExam test card to detect elevated pH, according to the manufacturer’s directions. If the pH was >4.6, the pH test area shows a blue plus (+) sign. Readings were performed in the clinic’s laboratory by a trained research laboratory technician, who was unaware of the woman’s history and the clinician’s findings on examination. (The amine portion of test card was not included in analysis because the test could not be performed according to manufacturer’s directions, ie, immediately at bedside.)
At the Beaufort Naval Hospital’s regional laboratory, one cytopathologist reviewed the endocervical Papanicolaou examination slides according to standard Bethesda criteria.23 The cytopathologist was unaware of the presence or absence of vaginal symptoms in the women and of the purpose of the study. Papanicolaou diagnoses consistent with bacterial vaginosis were defined as a report specifying "clue cells and/or non-specific vaginitis."
The associations between Nugent criteria diagnoses of bacterial vaginosis and race or ethnicity, contraceptive use, history of sexually transmitted infections, and history of sexual activity were examined with 
2 and Fisher exact tests where applicable. In the case of ethnicity, the 15 post hoc pairwise comparisons were assessed with Fisher exact tests and a modified Bonferroni correction to control for type I error.24 Significant correlates were included in a logistic regression model to determine whether those univariate relationships remained while adjusting for other significant correlates. The sensitivity, specificity, and positive and negative predictive values of the pH colorimetric test and Papanicolaou smears were assessed with the Nugent criteria used as the diagnostic standard.
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RESULTS |
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Selected demographic and clinical characteristics of the study sample are shown in Table 1
. The study participants were on average 19.1 years old (standard deviation = 2.1 years, range 17–33; 75% were between ages 17–19 years), ethnically and racially diverse, and most had experienced vaginal sexual intercourse in their lifetime (86%). Of the participants, 19% reported vaginal discharge, and 6.6% reported vaginal odor. Findings consistent with bacterial vaginosis were reported on 35% of Papanicolaou smears. Of the sexually experienced participants, 11.4% were infected with C trachomatis, 2.3% with N gonorrhoeae, and 1.7% with T vaginalis.
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). Post hoc comparisons revealed that the lower bacterial vaginosis prevalence in Asian/Pacific Islanders was significantly different when compared with blacks and Hispanics. No other ethnic differences achieved statistical significance.
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). Among those sexually experienced, having multiple sexual partners in the past 3 months (P = .026) and C trachomatis (P = .002) infection were found to be associated with bacterial vaginosis. In contrast, there was an inverse relationship between a bacterial vaginosis diagnosis and report of hormonal contraceptive use (P = .013) (Table 4). Bacterial vaginosis was not significantly associated with prior STD history, barrier contraception use, nor with current T vaginalis or N gonorrhoeae infections.
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).
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). The comparisons of whites to Asian/Pacific Islanders and members of other ethnic groups to Asian/Pacific Islanders were in the expected direction but did not achieve statistical significance as defined by the Bonferroni correction. The logistic regression model achieved good fit as assessed by the Hosmer-Lemeshow goodness-of-fit test (28 = 8.80, P = .359). Calculations to assess the performance profiles of the pH colorimetric test and Papanicolaou smear showed that the sensitivity and specificity of a positive pH test were 72% and 67%, respectively (95% CIs 68%, 76% and 64%, 70%, respectively). The performance of the Papanicolaou smear yielded a sensitivity of 72% (95% CI 68%, 76%) and a specificity of 79% (95% CI 77%, 81%) for detection of bacterial vaginosis with the Nugent criteria used as the standard.
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DISCUSSION |
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Our sample of 263 young women who report never experiencing vaginal intercourse is the largest sample of non–sexually experienced women to date evaluated for bacterial vaginosis with the Nugent criteria by five-fold (based on a systematic search with the PubMed search engine; search terms "bacterial vaginosis," "virgin," "sexual," "experience," "gardnerella"; including all languages; covering the dates mid1960s until June 2003 and based on review of all articles in this bibliography). Previous smaller studies of non–sexually experienced young women and girls in which Amsel criteria were used showed prevalences ranging from 0% (n = 18)11 to 12% (n = 52).28 Our higher prevalence among both the sexually experienced and non–sexually experienced women is most likely due to our use of the Nugent criteria for diagnosis, which is more sensitive than the clinically based Amsel criteria. Previous studies have shown that the Amsel criteria have a sensitivity of only 35–56% and specificity of 96–99% when compared with the Nugent criteria.15,16 It is also possible that the young women underreported prior sexual experience if such activity was involuntary. Finally, our reported prevalence among the sexually experienced cohort is consistent with previous studies in which the Nugent criteria were used.16,18,26,27
Given our large sample, we were able to examine bacterial vaginosis prevalence by race and ethnicity and found a significantly lower rate among Asian/Pacific Islanders compared with Native Americans, blacks, and Hispanics. This is consistent with previous studies, which showed a trend toward lower rates of bacterial vaginosis in pregnant Asian/Pacific Islanders and British Asians.29 Although bacterial vaginosis is not a sexually transmitted infection, these findings follow the pattern of infection for a number of STDs. However, the lower prevalence among Asian/Pacific Islanders remained significant despite adjusting for all the other significant correlates, including sexual experience and C trachomatis infection status. Perhaps the difference in prevalence by ethnicity could be explained by differences in douching practices (which has been associated with bacterial vaginosis26) or foreign body use (eg, tampons,26 sex toys, etc) that might affect the vaginal ecosystem, as well as biologic factors, which might vary by ethnicity, that we did not examine in this study. More detailed studies on behavioral and biologic factors associated with bacterial vaginosis among diverse ethnic or racial groups are clearly warranted.
Frequently, clinicians diagnose vaginal infections by syndromic diagnosis, relying mainly on history and the observation of discharge.30 Clinicians are accustomed to investigating vaginal discharge, but our findings of the association of bacterial vaginosis and self-reported vaginal odor adds another symptom for which clinicians can query their patients. Our findings support the use of pH to assist in the diagnosis of bacterial vaginosis for clinicians without access to microscopy, given its reasonable sensitivity (72%) but keeping in mind its lower specificity (67%), when compared with the Nugent criteria as the gold standard for diagnosis. The Papanicolaou smear might prove to be useful under some circumstances to screen for bacterial vaginosis. We found the sensitivity and specificity for the Papanicolaou smear (70% and 79%, respectively) to be comparable to and consistent with previous studies reporting sensitivities ranging from 55% to 89% and specificities from 85% to 96%.14,16 If bacterial vaginosis is determined to pose a significant morbidity for nonpregnant women, the Papanicolaou smear might be a reasonable "first-line" screening tool during routine gynecologic examinations of healthy populations, given its moderate performance and that it adds no cost to the routine pelvic examination of adult women.
Finally, regarding clinical correlates of bacterial vaginosis, our finding of an increased prevalence of bacterial vaginosis among those women with C trachomatis infection is supported by other research,31 which suggest that bacterial vaginosis might facilitate STD infection by decreasing local secretory leukocyte protease inhibitor levels. Although we did not find an association between N gonorrhoeae and T vaginalis infection and bacterial vaginosis, this is most likely due to the low number of positives (39 and 28, respectively), given that the difference in bacterial vaginosis prevalence was the same as that with C trachomatis infection. Furthermore, the finding of an association between hormonal contraception and bacterial vaginosis, which suggests a possible protective factor against bacterial vaginosis, has been described by other groups as well.26,32–36 Given that our study is cross-sectional, no causal relationship can be determined. Further research is indicated to explain the associations between bacterial vaginosis and both C trachomatis and hormonal contraception.
In summary, bacterial vaginosis is prevalent among young women who have and have not experienced vaginal intercourse and varies by race or ethnicity. The Papanicolaou smear and pH testing performed moderately well as screening tests for bacterial vaginosis. Finally, this study reinforces the need for more research on the inverse relationship between bacterial vaginosis and hormonal contraceptive use and the direct relationship between bacterial vaginosis and C trachomatis infection.
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Footnotes |
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The authors thank Kelli Betsinger, BA, and Alex Dubovtsev, PhD, for performance of the laboratory tests; and Jesse Canchola, MS, Jason Chang, BS, and Lance Pollack, PhD, for their statistical expertise.
doi:10.1016/S0029-7844(03)00858-5
Received April 10, 2003. Received in revised form July 9, 2003. Accepted July 17, 2003.
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REFERENCES |
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