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American Journal of Epidemiology Advance Access published online on August 10, 2005
American Journal of Epidemiology, doi:10.1093/aje/kwi243
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American Journal of Epidemiology Copyright © 2005 by the Johns Hopkins Bloomberg School of Public Health All rights reserved
Received January 7, 2005
Accepted April 28, 2005

Article

A Cluster Analysis of Bacterial Vaginosis-associated Microflora and Pelvic Inflammatory Disease

Roberta B. Ness 1*, Kevin E. Kip 2, Sharon L. Hillier 1, David E. Soper 3, Carol A. Stamm 4, Richard L. Sweet 5, Peter Rice 6, and Holly E. Richter 7

1 Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA; Department of Obstetrics, Gynecology, and Reproductive Sciences, Magee-Womens Hospital and Magee-Womens Research Institute, Pittsburgh, PA
2 Department of Epidemiology, Graduate School of Public Health, University of Pittsburgh, Pittsburgh, PA
3 Department of Obstetrics and Gynecology, Medical University of South Carolina, Charleston, SC
4 Department of Obstetrics and Gynecology, Denver Health Medical Center, Denver, CO
5 Center for Women's Health, University of California at Davis, San Diego, CA
6 Division of Infectious Disease, Boston Medical Center, Maxwell Finland Laboratory, Boston, MA
7 Department of Obstetrics and Gynecology, University of Alabama School of Medicine, Birmingham, AL

* To whom correspondence should be addressed.
Roberta B. Ness, E-mail: repro{at}pitt.edu


  Abstract

Controversy surrounds the association between bacterial vaginosis (BV) and pelvic inflammatory disease (PID). Women (N = 1,140) were ascertained at five US centers, enrolled (1999-2001), and followed up for a median of 3 years. Serial vaginal swabs were obtained for Gram's stain and cultures. PID was defined as 1) histologic endometritis or 2) pelvic pain and tenderness plus oral temperature >38.8°C, leukorrhea or mucopus, erythrocyte sedimentation rate >15 mm/hour, white blood cell count >10,000, or gonococcal/chlamydial lower genital infection. Exploratory factor analysis identified two discrete clusters of genital microorganisms. The first correlated with BV by Gram's stain and consisted of the absence of hydrogen peroxide-producing lactobacillus, Gardnerella vaginalis, Mycoplasma hominis, anaerobic Gram-negative rods, and, to a lesser degree, Ureaplasma urealyticum. The second, unrelated to BV by Gram's stain, consisted of Enterococcus species and Escherichia coli. Being in the highest tertile in terms of growth of BV-associated microorganisms increased PID risk (adjusted rate ratio = 2.03, 95% confidence interval: 1.16, 3.53). Carriage of non-BV-associated microorganisms did not increase PID risk. Women with heavy growth of BV-associated microorganisms and a new sexual partner appeared to be at particularly high risk (adjusted rate ratio = 8.77, 95% confidence interval: 1.11, 69.2). When identified by microbial culture, a combination of BV-related microorganisms significantly elevated the risk of acquiring PID.

Keywords: chlamydia; gonorrhea; pelvic inflammatory disease; sexually transmitted disease; vaginitis.
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