CAN KNOWN RISK FACTORS EXPLAIN RACIAL DIFFERENCES IN THE OCCURRENCE OF BACTERIAL VAGINOSIS? Roberta B. Ness MD, MPH, Sharon Hillier, Holly E. Richter, PhD, MD, David E. Soper, MD, Carol Stamm, MD, Debra C. Bass, MS, Richard L. Sweet, MD, and Peter Rice Pittsburgh, Pennsylvania; Birmingham, Alabama; Charleston, South Carolina; Denver, Colorado; Boston, Massachusetts
Background: Black women are more likely to have bacterial vaginosis (BV) than are nonHispanic white women. We examined whether this disparity can be explained by racial differences in known BV risk factors. Methods: Nine hundred black and 235 white women were enrolled from five US sites. At baseline, structured interviews were conducted and vaginal swabs self-collected for Gram-stain and culture. Results: Black women were more likely than white women to have BV/intermediate vaginal flora. They also were more likely to be older, have lower educational attainment and family incomes, have a history of a sexually transmitted disease, and douche. After adjustment for demographic and lifestyle factors, blacks remained at elevated risk for BV/intermediate flora (OR 2.2, 95% Cl 1.5-3.1). Blacks also were more likely to have specific BV-related vaginal microflora, as well as gonococcal or chlamydial cervicitis (OR 2.2, 95% Cl 1.2-3.8) after adjustment for known BV risk factors. Conclusion: Risk factor differences did not explain the observed racial disparity in the occurrence of BV, BV-related microflora, or gonococcal or chlamydial cervicitis. These findings highlight our limited understanding of the factors accounting for the occurrence of bacterial vaginosis and cervicitis among black and white women. (J Natl MedAssoc. 2003;95:201-212.)
02003. From the University of Pittsburgh and Magee Womens Hospital, Pittsburgh, Pennsylvania; University of Alabama School of Medicine, Birmingham, Alabama; Medical University of South Carolina, Charleston, South Carolina; Denver Health Medical Center, Denver, Colorado; Boston Medical Center, Maxwell Finland Laboratory, Boston, Massachusetts. Address correspondence to: Roberta B. Ness, University of Pittsburgh, Graduate School of Public Health, Room 517 Parran Hall, 130 DeSoto Street, Pittsburgh, PA 15261; phone (412) 624-3045; fax (412) 624-1056; or send e-mail to
[email protected]. JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
Key words: bacterial vaginosis + BV * cervicitis * gynecology Growing literature suggests that black women are more likely than non-Hispanic white women to have clinical and microbiologic evidence of bacterial vaginosis (BV), a condition in which the normally protective hydrogen peroxide producing (H202+) lactobacilli are overVOL. 95, NO. 3, MARCH 2003
201
grown by disease-promoting endogenous anaerobic and facultative aerobic bacteria, including Gardnerella vaginalis, Mycoplasma hominis, Mobiluncus species, and anaerobic Gram negative rods.1 Reported rates of BV range from 9% to 57% among reproductive age women with the variability explained by sexual patterns, BV definition, and race. 2-5 The association between black race and BV has been demonstrated among both pregnant and non-pregnant women in the US and non-pregnant women in the UK.25 Caution in the interpretation of this link is warranted, however, since a number of sociodemographic and lifestyle factors increase the risk of BV and are more common among black women. These sociodemographic and lifestyle factors, which include douching, low income and low educational attainment, number of sexual partners, a history of sexually transmitted infection including PID, previous pregnancies, and lack of hormonal contraceptive use, may produce the appearance of a relationship between race and BV when, indeed, such a relationship does not, in truth, exist.3,6,7 Since race is a social construct,8'9 it is rational to suggest that relevant lifestyle, sociodemographics and healthcare factors could explain racial differences in the occurrence of BV. A handful of previous reports have assessed whether race is a predictor for BV, independent of other risk factors, with divergent results. One cross-sectional study and a prospective cohort study, both ascertaining women from STI clinics, did not find race to be an independent predictor,4'10 whereas three cross-sectional studies, drawing on more diverse populations, two conducted in pregnant women2'11 and one in nonpregnant women, did find race to predict BV
status.3 We report here, among black and nonHispanic white women participating in the baseline examination of the GYN Infections FollowThrough (GIFT) Study, the associations between known risk and protective factors for BV. We then assess the degree to which known risk fac-
202 JOURNAL OF THE NATIONAL MEDICAL ASSOCIATION
tors for BV might explain racial differences in vaginal microecology.
METHODS Patient selection Between May 1999, and June 2001, women 13 to 36 years of age were recruited from five sites located in the eastern, southern, and western regions of the US into the GYN Infections Follow-through (GIFT) Study, a cohort investigation of the health consequences of douching. Human subjects approval was obtained at each participating institution and all women signed informed consent. Women enrolled from public and private gynecology clinics, student health services, and health departments, were eligible for the GIFT study if they were not specifically seeking care for an STI, yet were at elevated risk based on a previous risk stratification paradigm for chlamydial cervicitis, as described below.12 To be eligible, a woman had to have a score of three points or more on an algorithm wherein points were derived as follows: age 24 or less = 1; black race = 2; never pregnant = 1; two or more sexual partners = 1; douched at least once per month = 2; any sexually transmitted infection, including N. gonorrhoeae, C. trachomatis, and TJ vaginalis = 2. Of 2740 women screened for study entry, 853 (31.1%) did not meet these inclusion criteria. An additional 259 (9.5%) women were excluded on the basis of a priori criteria including: currently pregnant by beta HCG testing, currently married, never having had sexual intercourse, having had a prior hysterectomy, salpingectomy, or tubal ligation, or being on antibiotics at baseline (because of their lower sexually transmitted disease risk);12 z having pelvic tenderness on examination at baseline. Among the 1628 women who were eligible for the study, 1200 (73.7%) agreed to study participation, 1135 of whom identified themselves as black or non-Hispanic white and are the focus of these analyses. VOL. 95, NO. 3, MARCH 2003
Table 1. NUMBER (%) OF BLACK AND WHITE WOMEN WITH SELECTED BACTERIAL VAGINOSIS RISK FACTORS Age 25+ 19-24 13-18 Education > HS graduate HS graduate < HS graduate Marital Status Living as married Never married 809 Divorced/widow/other Income
3$20,000 $10,000-19,000238 < $10,000 History of: PID
Chlamydia
p
Whites
Blacks N
%
N
%
286 554 60
31.8 61.6 6.7
28 190 17
11.9 80.9 7.2
p= .000
436 277 187
48.4 30.8 20.8
159 41 35
67.7 17.4 14.9
p= .000
46 89.9 45
5.1 216 5.0
7 92.3 11
3.0 p= .379 4.7
154 29.0 428
18.8 33 52.2
120 15.6 59
56.6
27.8
p= .000
136 390 355 227 254
15.2 43.6 40.2 25.4 28.5
19 50 52 19 26
8.1 21.5 22.2 8.2 11.1
p= .005 p= .000 p= .000 p= .000 p= .000
64.7
52
21.1
p= .000
61.2 7.3 31.4
80 41 114
34.0 17.4 48.5
p=.000
15.3 71.0 13.7 16.5 5.2
35 144 56 70 19
14.9 61.3 23.8 35.0 8.1
p= .001 p= .000 p= .095
9.4 43.3
31 116
13.2 49.4
p= .079 p = .098
36.2 22.6 16.5 24.7 48.2
88 31 35 46 69
44.0 15.5 17.5 23.0 29.4
p= .087
51.9 5.8
70.6 4.3 25.1
p= .000
42.3'
166 10 59
51.9 16.7 13.8 17.6
166 13 28 28
70.6 5.5 11.9 11.9
p= .000
BV Gonorrhea Trichomoniasis Gravidity Ever pregnant 582 Tobacco smoking 550 Never 66 Former 282 Current Number of Partners (past 2 months) None 138 639 One 32 123 New partners (past 2 months)126 Anal sex (past 2 months) 47 Sex with menses 84 (past 2 months) Hormonal contraceptives 390 (past 2 months) Condom use (past 2 months) 276 none £ 5/10 times 172 6-9/10 times 126 10/10 times 188 Douched (past 2 months) 433 Douching frequency Never 467 < 1 time/month 52 3 1 time/month 381 Douching recency Never 467 0-7 days 150 124 8-21 days 322 days 158
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p= .000
VOL. 95, NO. 3, MARCH 2003 203
Identification of Bacterial Vaginosis
Potential Risk Factors
At baseline, study staff taught each subject how to self-collect vaginal specimens using a Q-tip®like cotton swab. Vaginal swabs were smeared onto slides by study staff at the bedside and these slides were air dried and later Gram-stained at a centralized, expert microbiology laboratory under the direction of one of us (SLH). As per Nugent et al.,13 a score of 0-10 was assigned in light of the relative proportions of large Gram-positive rods (lactobacilli), small Gram-negative or Gram-variable rods (Bacteroides or Gardnerella), and curved Gram-variable rods (Mobiluncus). A score of 0-3 was interpreted as consistent with normal vaginal flora; a score of 4-6, corresponding to disturbed flora, was designated as intermediate; and a score of 7-10 was considered to be bacterial vaginosis.
In a standardized 20-minute interview conducted by trained research staff at each center, women were asked about demographic factors including age, race, highest level of educational attainment, income, marital status, and gravidity. They reported relevant lifestyle behaviors such as tobacco smoking, number of sexual partners in the past two months, acquisition of a new partner in the past two months, various types of contraceptive use, and sex with menses. Furthermore, they were asked to recall past episodes of sexually transmitted infections including PID, gonococcal cervicitis, chlamydial cervicitis, bacterial vaginosis, and trichomoniasis. Women also were asked about their douching behavior including whether they had practiced any douching in the past two months, their frequency of douching in the past two months, and the timing of the most recent episode of douching. For purposes of analyses, the douching frequency data were categorized into none, HS graduate 197 HS graduate 133 20, antibiotic use, and barrier contraception use, women of non-white race were not significantly more likely to acquire BV (OR 1.2, 95% CI 0.6-2.3).10 Similarly, in a cross-sectional study conducted among 100 women with and 100 without BV enrolled from an STD clinic in London, England, Rajamanoharan et al. found no significant relationship between race and BV after adjusting for use of vaginal antiseptics, history of BV, barrier contraception, and occupation.4 On the other hand, a recent cross-sectional study by Holzman et al., enrolling a larger number of women from health department, family planning, and university health clinics (496 nonpregnant women) showed that blacks with lower (