Geraldine M. McQuillan

The prevalence of bacterial vaginosis in the United States, 2001-2004; associations with symptoms, sexual behaviors, and reproductive health

Objectives: Bacterial vaginosis (BV), a disturbance of vaginal microflora, is a common cause of vaginal symptoms and is associated with an increased risk of acquisition of sexually transmitted infections, HIV, and with adverse pregnancy outcomes. We determined prevalence and associations with BV among a representative sample of women of reproductive age in the United States. Study Design: Women aged 14–49 years participating in the National Health and Nutrition Examination Survey 2001–2004 were asked to submit a self-collected vaginal swab for Gram staining. BV, determined using Nugent’s score, was defined as a score of 7–10. Results: The prevalence of BV was 29.2% (95% confidence interval 27.2%–31.3%) corresponding to 21 million women with BV; only 15.7% of the women with BV reported vaginal symptoms. Prevalence was 51.4% among non-Hispanic blacks, 31.9% among Mexican Americans, and 23.2% among non-Hispanic whites (P <0.01 for each comparison). Although BV was also associated with poverty (P <0.01), smoking (P <0.05), increasing body mass index (&khgr;2P <0.0001 for trend), and having had a female sex partner (P <0.005), in the multivariate model, BV only remained positively associated with race/ethnicity, increasing lifetime sex partners (&khgr;2P <0.001 for trend), increasing douching frequency (&khgr;2P for trend <0.001), low educational attainment (P <0.01), and inversely associated with current use of oral contraceptive pills (P <0.005). Conclusion: BV is a common condition; 84% of women with BV did not report symptoms. Because BV increases the risk of acquiring sexually transmitted infections, BV could contribute to racial disparities in these infections.

Serologic Immunity to Diphtheria and Tetanus in the United States

Context Although immunization against diphtheria and tetanus is nearly universal during childhood, immunity wanes as people age. The prevalence of immunity in adults is unknown. Contribution According to the Third National Health and Nutrition Examination Survey (NHANES III), only 60% of the total adult population had serologic protection against diphtheria; 72% were protected against tetanus. By age 70, only 30% of adults had serologic immunity to either disease. Implications Booster immunization every 10 years is important to protect adults against diphtheria and tetanus. The Editors Routine immunization against tetanus and diphtheria has been standard practice in the United States since the late 1940s. To ensure protection against these two diseases, as well as pertussis, the Advisory Committee on Immunization Practices (ACIP) recommends administration of a primary series of diphtheria and tetanus toxoids and acellular pertussis vaccine in the first year of life, followed by doses of these vaccines at 15 to 18 months of age and 4 to 6 years of age. The ACIP then recommends administration of adult-formulation diphtheria and tetanus toxoids beginning at 11 to 12 years of age and every 10 years thereafter (1). Although diphtheria and tetanus occur only rarely in the United States, the recent outbreak of diphtheria in the former Soviet Union is a reminder that even a well-controlled infection can reemerge when population immunity is not maintained (2). In the United States, approximately 95% of children receive three or more doses of diphtheria and tetanus toxoids by 19 to 35 months of age (3), but adherence to the current recommendation for the decennial booster among adults is much lower (4). To document population immunity in the United States, we determined the prevalence of protective antibodies to diphtheria and tetanus by testing serum obtained from participants in the Third National Health and Nutrition Examination Survey (NHANES III). Methods Survey Design and Data Collection The NHANES III was conducted from 1988 to 1994 by the National Center for Health Statistics, U.S. Centers for Disease Control and Prevention. It provided national statistics on the health and nutritional status of the noninstitutionalized civilian U.S. population by conducting household interviews and a standardized physical examination (5). The survey research protocol was reviewed and approved by an institutional review board at the Centers for Disease Control and Prevention. The sampling was based on a complex, stratified, multistage, probability cluster sample design (5) that is representative of the U.S. population. Persons younger than 5 years of age, persons older than 59 years of age, black Americans, and Mexican-Americans were sampled at higher frequencies than were other persons. Race or ethnicity wasdefined by self-report as non-Hispanic white, non-Hispanic black, or Mexican-American. Persons who did not choose one of these categories were classified as other and were analyzed with the total population. The poverty-index ratio was calculated by dividing total family income by the poverty threshold index, adjusted for family size at year of interview. Residence in a county with a population equal to or greater than 1 million was defined as metropolitan residence. Residence in all other counties (including rural areas) was defined as nonmetropolitan. Data on years of education, marital status, occupation, and military service were analyzed for study participants 20 years of age or older. Participants were considered to have access to care if they indicated that they usually visited a particular clinic, health center, or physicians office when they were sick or for routine care. If a participant said that he or she usually saw one particular health professional or physician, he or she was categorized as having access to both a clinic and a physician. Laboratory Methods Serum samples were obtained once when each participant was examined. Diphtheria Antitoxin Antibody levels to diphtheria toxin were determined by a neutralization assay in Vero monkey kidney cells by using a modification of the procedure described by Miyamura and colleagues (6, 7). The serum samples from NHANES were run singly with 20% duplication. Diphtheria antitoxin titers were converted to IU/L after standardization with reference serum specimens provided by the Center for Biologics Evaluation and Research, U.S. Food and Drug Administration, by using a standard technique (8). The lowest level of detection for the diphtheria assay was 0.0038 IU/mL, and the upper limit of detection was 5.6 and 8.0 IU/mL on different runs of the assay. An antibody concentration of 0.10 IU/mL or greater was considered a fully protective level (9, 10). Tetanus Antitoxin Tetanus antitoxin was measured by using a solid- phase enzyme immunoassay (Immulon I, Dynatech, Chantilly, Virginia) with a lower limit of detection of 0.001 IU/mL. This method is described in detail elsewhere (11, 12). For all our analyses, protective levels of tetanus antitoxin were defined as greater than 0.15 IU/mL; the rationale for considering this cutoff protective is discussed elsewhere (11, 13). Response Rates All analyses were restricted to persons 6 years of age or older who had sufficient serum specimen for both assays. A total of 30 930 persons 6 years of age or older were selected for the study, and 23 527 (76%) were examined. Of those examined, 18 045 (77%) had a sufficient serum specimen for both tetanus and diphtheria testing. Persons 70 years of age or older had the lowest rates of available serum (69%). No differences by sex were observed, but response rates were lower for non-Hispanic blacks (74%) than for non-Hispanic whites and Mexican-Americans (78%). Careful evaluation using data from the home interview (91.6% completed the interview) detected no systematic selection bias due to nonresponse in the examination data. The results are therefore representative of the U.S. population. Statistical Analysis Prevalence estimates were weighted to represent the total U.S. population and to account for oversampling and nonresponse to the household interview and physical examination (14, 15). Standard errors were calculated by using SUDAAN (Research Triangle Institute, Research Triangle Park, North Carolina) (16), a family of statistical procedures for analysis of data from complex sample surveys. For comparisons between subgroups of NHANES III, data were age-adjusted to the 1980 U.S. population by using the direct method (17). To screen for possible predictors of seropositivity, differences in seroprevalence were evaluated without correction for multiple comparisons by examining the 95% CIs for the seroprevalence values generated by SUDAAN. P values were calculated by using a univariate t-statistic obtained from a general linear contrast procedure in SUDAAN. Results Immunity to Diphtheria Only 60.5% of the sample had protective levels of diphtheria antibody (Table). Mexican-Americans were 5% to 9% less likely than other racial or ethnic groups to have protective levels of antibody. The percentage of men with protective antibody to diphtheria decreased with increasing age, and only 30% of male participants 60 to 69 years of age were protected (Figure 1). Fewer women than men had protective levels of antibody, and the percentage of protected women also decreased with age (Figure 1). Table. Prevalence of Immunity to Diphtheria and Tetanus by Demographic Characteristics, Third National Health and Nutrition Examination Survey, 19881994 Figure 1. Age-specific prevalence of immunity to tetanus and diphtheria by sex, Third National Health and Nutrition Examination Survey, 19881994. When antibody levels were examined by race/ethnicity and age, a similar decrease in the proportion of protected persons was observed among non-Hispanic white persons and black persons until 49 years of age (Figure 2). Among black persons older than 50 years of age, the proportion of those with protective levels of antibody remained stable at approximately 40%. Mexican-Americans had a lower prevalence of protective antibody compared with non-Hispanic white persons and black persons for each 10-year age group from 20 to 49 years of age (P < 0.001). After 59 years of age, white persons had a lower prevalence of protective antibody levels than did non-Hispanic black persons and Mexican-Americans (P < 0.001). Figure 2. Age- and race/ethnicity-specific prevalence of immunity to diphtheria, Third National Health and Nutrition Examination Survey, 19881994. Immunity to Tetanus Seventy-two percent of the sample had protective levels of antibody to tetanus (Table). Mexican-Americans were 8% less likely than white or black persons to have protective levels of antibody (P < 0.001). The disparity between men and women with protective levels of antibody was greater for tetanus than for diphtheria: Seventeen percent more men than women had protective levels of antibody to tetanus (P < 0.001). The proportion of men with protective levels of antibody to tetanus did not decrease by age at the same rate as for diphtheria (Figure 1). At 70 years of age, 45% of men had protective antibody to tetanus. In contrast, the percentage of women with protective levels of tetanus antibody decreased rapidly after 40 years of age. By 70 years of age, only 21% of women had protective levels. As was seen with diphtheria antibody, protective levels of antibody to tetanus differed little by race/ethnicity until after 19 years of age (Figure 3). A smaller percentage (P 0.05) of Mexican-Americans in each 10-year group from 20 to 49 years of age had protective antibody. White persons 50 to 69 years of age were significantly more likely than black persons or Mexican-Americans to have protective levels of tetanus antibody. Figure 3. Age- and race/ethnicity-specific prevalence of immunity to tetanus, Third National Health and Nutrition Examination Survey, 19881994. Demog

National seroprevalence and trends in herpes simplex virus type 1 in the United States, 1976-1994.

Objectives: The objectives of this study were to estimate national seroprevalence of herpes simplex virus type 1 (HSV-1), describe trends in seroprevalence, and examine correlates of infection. Goal: The goal of this study was to measure the burden of HSV-1 infection in the U.S. population. Study: We tested serum samples for HSV-1 antibody and analyzed questionnaire data collected for the second and third National Health and Nutrition Surveys (NHANES II, 1976–80; NHANES III, 1988—94). Seroprevalence estimates were weighted to represent the total U.S. population. Results: At the time of NHANES III, two thirds (68%) of the U.S. population 12 years and older had HSV-1 antibody. Prevalence increased with age and varied by race/ethnicity; the majority of persons in all race/ethnic groups were HSV-1-seropositive by age 30. Overall, the national seroprevalence of HSV-1 decreased nonsignificantly by 2% in the years between NHANES II and III; decreases in HSV-1 seroprevalence in some population subgroups were balanced by increases in other groups. Conclusions: There was no overall change in the seroprevalence of HSV-1 in the U.S. population between NHANES II and III.

Racial and Ethnic Differences in the Seroprevalence of 6 Infectious Diseases in the United States: Data From NHANES III, 1988–1994

OBJECTIVES We examined racial/ethnic differences in the seroprevalence of selected infectious agents in analyses stratified according to risk categories to identify patterns and to determine whether demographic, socioeconomic, and behavioral characteristics explain these differences. METHODS We analyzed data from the third National Health and Nutrition Examination Survey, comparing differences among groups in regard to the prevalence of infection with hepatitis A, B, and C viruses, Toxoplasma gondii, Helicobacter pylori, and herpes simplex virus type 2. RESULTS Racial/ethnic differences were greater among those in the low-risk category. In the case of most infectious agents, odds associated with race/ethnicity were almost 2 times greater in that category than in the high-risk category. CONCLUSIONS Stratification and adjustment for socioeconomic factors reduced or eliminated racial/ethnic differences in the prevalence of infection in the high-risk but not the low-risk group, wherein race/ethnicity remained significant and might have been a surrogate for unmeasured risk factors.

Risk Factors for Human Herpesvirus 8 Infection among Adults in the United States and Evidence for Sexual Transmission

BACKGROUND Human herpesvirus 8 (HHV-8) causes Kaposi sarcoma. In the United States, transmission routes for HHV-8 are uncertain. METHODS The National Health and Nutrition Examination Survey III sampled individuals from the US general population (1988-1994). We used enzyme immunoassays (EIAs) to measure HHV-8 antibodies (K8.1 and open reading frame [ORF] 73 antigens) in 13,894 surveyed adults. HHV-8 seroprevalence was examined according to sexual history and viral coinfection markers. RESULTS Overall, seroprevalence was low when a highly specific cutoff was used (K8.1, 1.6%; ORF73, 1.5%) but was higher when a less-specific cutoff was used (K8.1, 7.1%; ORF73, 7.4%). When the more-specific approach was used, K8.1 seroprevalence was similar in men and women. Men who have sex with men (MSM) had a higher K8.1 seroprevalence (8.2%). Among other men, K8.1 seroprevalence was marginally associated with duration of heterosexual activity (P=.1) and was positively associated with the lifetime number of sex partners (P=.04) and with coinfections with hepatitis B virus (6.1% vs. 1.2% without coinfection; P<.001) and herpes simplex virus 2 (2.7% vs. 1.0%; P=.003). Among women, K8.1 seroprevalence was not significantly related to duration of sexual activity, the lifetime number of sex partners, or viral coinfections. The ORF73 EIA revealed similar but less clear-cut patterns. CONCLUSIONS Among men, HHV-8 transmission may occur through sexual activity, particularly sex with other men. No evidence was observed for heterosexual transmission to women.

Seroprevalence of Q fever in the United States, 2003-2004.

We performed serum testing for IgG antibodies against Coxiella burnetii (phase I and phase II) and analyzed questionnaire data from 4,437 adults > or = 20 years of age who participated in the National Health and Nutrition Examination Survey 2003-2004 survey cycle. National Q fever seroprevalence was determined by enzyme-linked immunosorbent assay and confirmed by using immunofluorescent antibody testing. Overall seroprevalence for Coxiella burnetii was 3.1% (95% confidence interval [CI] = 2.1-4.3%) among 4,437 adults > or = 20 years of age. Coxiella burnetii age-adjusted antibody prevalence was higher for men than for women (3.8%, 95% CI = 2.7-5.2% versus 2.5%, 95% CI = 1.5-3.7%, respectively, P < 0.05). Mexican Americans had a significantly higher antibody prevalence (7.4%, 95% CI = 6.6-8.3%) than either non-Hispanic whites (2.8%, 95% CI = 1.7-4.3%) or non-Hispanic blacks (1.3%, 95% CI = 0.6-2.5%) (P < 0.001). Multivariate analysis showed that the risk for Q fever antibody positivity increased with age and was higher among persons who were foreign-born, male, and living in poverty. These findings indicate that the national seroprevalence of Q fever in the United States is higher than expected on the basis of case numbers reported to the Centers for Disease Control and Prevention from state health departments. Potential differences in risk for exposure by race/ethnicity warrant further study.

The Relationship Between Periodontal Disease Attributes and Helicobacter pylori Infection Among Adults in the United States

OBJECTIVES We investigated the relationship between Helicobacter pylori infection and abnormal periodontal conditions. METHODS Data from the first phase of the third National Health and Nutrition Examination Survey were used. A total of 4504 participants aged 20 to 59 years who completed a periodontal examination and tested positive for H. pylori antibodies were examined. RESULTS Periodontal pockets with a depth of 5 mm or more were associated with increased odds of H. pylori seropositivity (odds ratio [OR] = 1.47; 95% confidence interval [CI] = 1.12, 1.94) after adjustment for sociodemographic factors. This association is comparable to the independent effects of poverty on H. pylori (OR = 1.54; 95% CI = 1.10, 2.16). CONCLUSIONS Poor periodontal health, characterized by advanced periodontal pockets, may be associated with H. pylori infection in adults, independent of poverty status.

Prevalence of HIV in the US household population: the National Health and Nutrition Examination Surveys, 1988 to 2002.

Summary: To examine trends in HIV prevalence in the US household population, serum or urine samples from 2 National Health and Nutrition Examinations Surveys (NHANES) (1988-1994 and 1999-2002), were tested for HIV antibody. In the 1999 to 2002 survey, data on risk behaviors, CD4 T lymphocytes, and antiretroviral therapy (ART) were also available. In the 1988 to 1994 survey, there were 59 positive individuals of 11,203 tested. In NHANES 1999 to 2002, there were 32 positive individuals of 5926 tested. The prevalence of HIV infection among those aged 18 to 39 years in NHANES 1988 to 1994 was 0.38% (95% confidence interval [CI]: 0.22-0.68) as compared with 0.37% (95% CI: 0.17 to 0.80) in 1999 to 2002. Prevalence did not change significantly between surveys in any race and/or ethnic or gender group among 18- to 39-year-old participants. HIV prevalence was 3.58% (95% CI: 1.88 to 6.71) among non-Hispanic blacks in the 40- to 49-year-old age group in 1999 to 2002, but the age range available in NHANES 1988 to 1994 was 18 to 59 years and does not allow direct comparison of prevalence. Cocaine use and the presence of herpes simplex virus-2 antibody were the only significant risk factors for HIV infection for non-Hispanic blacks. Fifty-eight percent of infected individuals not reporting ART had CD4 T-lymphocyte counts <200 cells/mm3 compared with 18.2% on therapy and 12.5% of participants newly informed of their HIV status.

Seroprevalence of Measles Antibody in the US Population, 1999–2004

BACKGROUND Endemic measles transmission was declared eliminated in the United States in 2000. To ensure that elimination can be maintained, high population immunity must be sustained and monitored. Testing for measles antibody was included in the National Health and Nutrition Examination Survey (NHANES), a nationally representative survey, conducted during 1999-2004. METHODS A measles-specific immunoassay was used to measure the seroprevalence of measles antibody in NHANES participants 6-49 years of age. For analysis, participants were grouped by birth cohort. RESULTS During 1999-2004, the rate of measles seropositivity in the population overall was 95.9% (95% confidence interval [CI], 95.1%-96.5%). The highest seroprevalence of measles antibody was in non-Hispanic blacks (98.6% [95% CI, 98.0%-99.1%]). Those born during 1967-1976 had significantly lower levels of measles antibody (92.4% [95% CI, 90.8%-93.9%]) than did the other birth cohorts. Independent predictors of measles seropositivity in the 1967-1976 birth cohort were non-Hispanic/black race/ethnicity, more than a high school education, having health insurance, and birth outside the United States. CONCLUSIONS Measles seropositivity was uniformly high in the US population during 1999-2004. Nearly all population subgroups had evidence of measles seropositivity levels greater than the estimated threshold necessary to sustain measles elimination. Non-Hispanic whites and Mexican Americans born during 1967-1976 had the lowest measles seropositivity levels and represent populations that might be at increased risk for measles disease if the virus were reintroduced into the United States.

Seroprevalence of HIV in the US Household Population Aged 18–49 Years: The National Health and Nutrition Examination Surveys, 1999–2006.

Objective:To monitor trends in HIV seroprevalence in the United States, HIV testing was included in the National Health and Nutrition Examination Survey (NHANES) conducted from 1999 to 2006. Methods:From 1999 to 2006, 11,928 participants aged 18-49 years were tested for HIV antibody. Prevalence estimates were weighted to account for oversampling and nonresponse. Results:There were 67 HIV antibody-reactive individuals for a seroprevalence of 0.5% [95% confidence interval (CI) 0.3-0.6]. In the only age subgroup directly comparable between surveys (18-39 years), HIV seroprevalence remained constant from NHANES III (1988-1994) to NHANES 1999-2002 and 2003-2006. In NHANES 1999-2006, non-Hispanic blacks had significantly higher HIV seroprevalence (2.0%, 95% CI 1.5-2.7) compared with individuals in all other race/ethnic groups combined. Seroprevalence was also higher in each race/ethnic group among men who have sex with men (9.4% 95% CI 5.0-17.1), among persons who had detectable antibody to herpes simplex type-two (1.9% 95% CI 1.4-2.8), among those who had 50 or more lifetime sex partners (3.4%, 95% CI 1.7-6.7), and among those who never married (0.8%, 95% CI 0.5-1.3). Conclusions:In this household-based population, seroprevalence did not significantly change from NHANES III to NHANES 1999-2006. Non-Hispanic blacks had significantly higher prevalence of infection compared with other race/ethnic groups. Male-to-male sex and the presence of HSV-2 antibody were the strongest predictors of HIV infection.