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Sexually Transmitted Diseases:
doi: 10.1097/OLQ.0b013e31815abaef
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Seroepidemiology of Human Papillomavirus Type 11 in the United States: Results From the Third National Health and Nutrition Examination Survey, 1991–1994

Hariri, Susan PhD*; Dunne, Eileen F. MD*; Sternberg, Maya PhD*; Unger, Elizabeth R. MD, PhD†; Meadows, Kristi S. BS†; Karem, Kevin L. PhD†; Markowitz, Lauri E. MD*

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From the *National Center for HIV/AIDS, Viral Hepatitis, STD, and TB Prevention, and †National Center for Zoonotic, Vector-Borne and Enteric Diseases, Coordinating Center for Infectious Diseases, Centers for Disease Control and Prevention, Atlanta, Georgia

Correspondence: Susan Hariri, PhD, Centers for Disease Control and Prevention, 1600 Clifton Road NE, MS E-02, Atlanta, GA 30333. E-mail: shariri@cdc.gov.

Disclaimer: The findings and conclusions in this report are those of the authors and do not necessarily represent the views of the funding agency.

Received for publication June 12, 2007, and accepted September 9, 2007.

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Abstract

Objectives: The national seroprevalence of the nononcogenic human papillomavirus (HPV) type 11, one of the types targeted by the quadrivalent HPV vaccine, has not been evaluated in the United States. The objectives of this study were to estimate the national seroprevalence and evaluate predictors of HPV-11 seropositivity.

Study Design: We tested serum samples for HPV-11 antibodies and analyzed questionnaire data from the second phase of the National Health and Nutrition Examination Survey III, 1991–1994. Seroprevalence estimates were weighted to represent the US population.

Results: Overall seroprevalence of HPV-11 infection was 4.7%. Seroprevalence was significantly higher among females (5.7%) than among males (3.6%). Independent predictors of HPV-11 seropositivity included sex, race/ethnicity, lifetime number of sex partners, education, and HPV-16 seropositivity.

Conclusion: This study represents the most comprehensive picture of HPV-11 infection in the United States to date, and provides baseline data on the prevalence of HPV-11 before availability of the quadrivalent HPV vaccine.

HUMAN PAPILLOMAVIRUSES (HPVs) are a heterogeneous group of nonenveloped DNA viruses that infect the skin and mucous membranes of human hosts. To date, at least 100 genetically distinct HPV types have been identified, over 40 of which infect the genital areas.1 HPV infection is ubiquitous, and genital HPV is the most common sexually transmitted infection in the United States.2,3 However, quantifying the prevalence of genital HPVs nationally has been difficult because the majority of HPV infections are asymptomatic4–6 and most infections clear within 2 years of infection.7,8 Although not all infected individuals develop detectable levels of antibodies to HPV, serologic measurements can be used to evaluate cumulative exposure to HPV at the population level.8,9

The global incidence and prevalence of oncogenic HPV types have been well described in several studies, mostly in the context of cervical cancer, over 70% of which is associated with HPV types 16 and 18,1,8,10 but also in seroprevalence studies, including a population-based investigation of HPV-16 seroprevalence in the United States.9,11–18 Less is known about the seroepidemiology of nononcogenic HPV types 6 and 11, which together are responsible for over 90% of anogenital warts worldwide.4–6,19–21 HPV types 6 and 11 are also detected in nearly all cases of recurrent respiratory papillomatosis (RRP), a rare but life-threatening disease,18,21–23 and are responsible for the majority of nononcogenic HPV-related morbidity and associated health care costs.24–28 Data on the proportional distribution of types 6 and 11 in genital warts as well as RRP are limited because many studies used methods that did not distinguish between these 2 closely related types that occur with high prevalence in both conditions. Data from a few investigations have demonstrated that HPV-11 accounts for 8–30% of genital warts worldwide.19,29–31 In the juvenile-onset form of RRP, in which vertical transmission from infected mother to child is the suspected mode of transmission,21–23,32 HPV-11 has been associated with a more aggressive clinical course.23

A prophylactic HPV vaccine directed against HPV types 6, 11, 16, and 18 has been shown in clinical trials to have high efficacy in females for prevention of infections and clinical outcomes due to HPV 6, 11, 16, and 18.33,34 This quadrivalent vaccine was approved by the FDA in June 2006 for use in young women between the ages of 9 and 26 years.33 If appropriately implemented, the current recommendation to routinely vaccinate 11- to 12-year-old adolescent girls35 could have a substantial impact on vaccine type HPV-related clinical outcomes.

The objective of this study was to determine the seroprevalence of HPV-11 infection in the general US population of ages 6 to 59 years. Additionally, the study aimed to describe patterns of HPV-11 seropositivity, and presumably infection, in various subpopulations and to characterize associated risk factors. Results were obtained from a national seroepidemiologic survey of HPV-11 infection performed on surplus serum samples from the second phase of the third National Health and Nutrition Examination Survey (NHANES III), conducted from 1991 to 1994.

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Materials and Methods

Study Population and Design

NHANES are cross-sectional national surveys conducted by the National Center for Health Statistics of the Centers for Disease Control and Prevention, conducted as period surveys until 1994 and redesigned as a continuous annual survey since 1999. NHANES are designed to provide national estimates on the health and nutritional status of the US civilian noninstitutionalized population. Consenting participants have household interviews and physical examinations and phlebotomy in mobile examination centers. The surveys use a stratified multistage probability cluster design to select a representative sample of the US civilian noninstitutionalized population aged 2 months or older in 50 states. NHANES III was conducted from 1988 to 1994 in two 3-year phases. Children aged ≤5, adults aged ≥60, Mexican Americans, and non-Hispanic African Americans were sampled at a higher rate compared to other demographic groups to allow sufficient sizes for analysis of the groups. Poverty index was calculated according to the US Census definition by dividing total family income by the poverty threshold after adjusting for family size at the time of interview. Persons residing in a county in a metropolitan area were classified as “urban” while all others were defined as “nonurban.” Limited sexual history information was asked of adolescents aged 15 to 16 years while respondents aged 17 to 59 years provided more detailed sexual behavior information. Use of alcohol, cocaine, and marijuana was asked of all participants ≥12 years. Response rates for 1988–1994 NHANES III were 86% for the household interview and 79% for the medical examination and have been described in detail elsewhere.36

The following analysis is limited to the second phase of NHANES III conducted from 1991 to 1994. Of the persons 6 to 59 years were selected to participate; 9542 were interviewed, 8933 (94%) of whom also received a health examination. Surplus serum samples were available for 8102 participants, which comprised 85% of the total interviewed and 91% of those examined.

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Laboratory Methods

We used an enzyme-linked immunosorbent assay (ELISA) to detect HPV-11 IgG antibodies in serum samples. Viruslike particles (VLPs) were produced by expression of an HPV-11 L1 recombinant baculovirus in insect cells (gift from Dr. Robert Rose, University of Rochester, NY).37 Purification of VLPs was performed as previously described.9 A direct VLP ELISA was performed with sera at 1:20 dilution, standardized and performed as described elsewhere.9,38 For quality control and evaluation, we screened anonymized human serum samples for reactivity to HPV 11 using 25% blocking of a mouse polyclonal antibody to HPV-11 VLP as indicator of positivity. These sera were then used as individual high positive and negative controls and also to prepare pools of high positive, low positive, and negative serum controls to standardize the ELISA. Five individual controls and 3 pooled controls were used on each plate. Quality control assessment included monitor of day-to-day and plate-to-plate variation using Levy-Jennings plots. Results for individual control serum samples that were run throughout the course of the NHANES III analysis were used in receiver operating characteristic analysis to determine the ELISA cutoff value for discrimination between positive and negative samples.

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Statistical Analysis

SUDAAN software version 9.0 was used for all statistical analyses to incorporate the sampling weights and account for the nonrandom cluster design in calculating the variance estimates based on a Taylor series approximation. All seroprevalence estimates were weighted to represent the total US civilian noninstitutionalized population and to account for oversampling and nonresponse to the household interview and physical examination. We estimated HPV-11 seroprevalence overall and by various demographic categories. Bivariate significance tests for association were based on a Wald χ2 statistic. The confidence intervals for the prevalence estimates were calculated on the basis of the log transformation with standard errors of the log prevalence calculated using the δ method.39 Critical values used for the confidence intervals were based on the t-distribution with the degrees of freedom as number of strata minus the number of primary sampling units, which in most cases was a total of 23 degrees of freedom. No adjustments for multiple comparisons were made to P values.

The association of age with HPV-11 was examined in bivariate logistic regression with age as a 6-level categorical variable (6–11, 12–19, 19–29, 30–39, 40–49, and 50–59). Plot of age category midpoints versus the β coefficients of that category from the models showed a nonlinear association in both sexes. We investigated the presence of an upward linear trend in females less than 39 years old and a downward linear trend among females older than 40 years, using age as a continuous variable in separate logistic regression models as suggested by the data. Likewise, we examined presence of an increasing linear trend in males up to 49 years. A trend was considered statistically significant if the β coefficient of age in the model was nonzero at P <0.05 using the Satterthwaite adjusted F test.

We used logistic regression analysis to identify independent predictors of HPV-11 seropositivity in participants 17 to 59 years old.40 Any variable with a statistically significant Wald χ2 statistic at P <= 0.10 on bivariate analysis was included in the initial models. Age was modeled as a continuous variable and evaluated for the possibility of a nonlinear association with HPV-11 seroprevalence. Using a backward elimination strategy, parameters determined to be statistically significant with the Satterthwaite adjusted F-test P <= 0.05 were retained in the main effects model. Data-based confounding was assessed for variables that were dropped in the backwards elimination steps. If a dropped variable was responsible for a change of ≥20% in the β parameter estimate of the main effects variables, the variable was retained in the model to adjust for confounding irrespective of statistical significance. Finally, all pairwise interactions between variables in the final model after assessing for confounding were evaluated. Pairwise interactions significant with a Satterthwaite adjusted F-test P <= 0.05 were retained.

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Results

Based on 8102 persons tested between 1991 and 1994, the overall seroprevalence of HPV-11 among persons 6 to 59 years in the United States was 4.7% (95% CI: 3.9–5.6). Seroprevalence was significantly higher in female (5.7%) than in male participants (3.6%) overall (P = 0.04) and remained higher in females across all age and race categories (Table 1). Overall, HPV-11 seroprevalence was highest among females in the 30- to 39-year age group (6.3%), whereas it peaked among males in the 40- to 49-year age group (5.7%). There was a significant increasing trend in seroprevalence for females 6 to 39 years and males 6 to 49 years followed by nonsignificant declines through age 59 in both males and females (Fig. 1). Seroprevalence also differed significantly by self-identified racial category. Overall, prevalence was highest among non-Hispanic African Americans (8.8%), more than double the prevalence in Mexican Americans (4.3%) and non-Hispanic whites (3.8%). A similar proportional trend was observed among racial categories when stratified by sex with African Americans having high rates of infection in both males and females. The prevalence of HPV-11 was much higher in African American females (12.6%) than African American males (4.5%). Geographic analysis of seropositivity did not reveal any regional differences. However, urban residents were significantly more likely to be seropositive (5.7%) than those living in nonurban areas (3.7%) nationwide, particularly among males. The overall seroprevalence of HPV-11 was significantly higher among people living below poverty level (6.6%) compared to those living at or above poverty (4.3%) and the trend remained the same when stratified by sex. HPV-16 seropositivity was also significantly associated with HPV-11 seropositivity and the pattern was the same in both males and females. Overall, a total of 171 participants tested positive for both infections, which represents 1.2% of the entire population (95% CI: 0.9–1.7), 1.7% of females (95% CI: 1.1–2.5), and 0.75% of males (95% CI: 0.4–1.3) (P = 0.02). Among those infected with HPV-11, 26.3% were also seropositive for HPV-16 (95% CI: 19.4–35.6).

Table 1
Table 1
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Fig. 1
Fig. 1
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Behavioral characteristics significantly associated with HPV-11 seropositivity included age at first sexual intercourse, lifetime number of sexual partners, and ever use of cocaine and marijuana (Table 2). Five male and 10 female respondents with no reported history of sexual intercourse were found to be HPV-11 seropositive. Almost all (n = 14) of these 15 individuals were also seropositive for another sexually transmitted infection, herpes simplex virus 2 (HSV-2). One female was of missing HSV-2 status and could not be evaluated. The seroepidemiology of HSV-2 in this population has been described in detail elsewhere.41

Table 2
Table 2
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In the multiple logistic regression model, statistically significant predictors of HPV-11 infection included female gender, African American race, increasing number of lifetime sexual partners, less than high school education, and HPV-16 coinfection (Table 3). Urban residence and drug use did not remain significant in the final model. Socioeconomic status as measured by living below or above the poverty level marginally confounded the association between HPV-11 and race, but the difference was not statistically significant and did not affect any of the estimates. Therefore, poverty level was not included in the model. We found no other confounding or effect modification, and thus no other variables were included in the model.

Table 3
Table 3
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Discussion

This study is the first to describe the seroprevalence and distribution of HPV-11 infection in the United States. Our results indicate that the odds of HPV-11 seropositivity were over 2 times higher among females compared to males. This observed sex difference is not surprising given inherent immunologic and anatomical differences between males and females that are well known to result in differential susceptibility to most sexually transmitted infections.42 Results of a study of genital warts among NHANES participants from 1999 to 2004 by Dinh et al. indicate that “women were three times more likely to report having a history of genital warts than men,” supporting our findings.43 Moreover, seroprevalences of other genital HPVs have also been reported to be significantly higher in females compared to males.9,44 In contrast to our findings, anogenital warts24,26 have been reported to have similar sex distributions. However, the results from this study are not directly comparable to the reported prevalence of anogenital warts, particularly data derived from genital warts claims submitted by privately insured patients who may not be representative of the general US population. Our results indicate that HPV-11 seroprevalence is much higher in both male and female non-Hispanic African Americans, a racial category that is likely underrepresented in the insurance claim data.

Although our data suggest that the prevalence of HPV-11 is only slightly lower among people who reported never having sex compared to those who reported ever having sex (4.4% vs. 5.5%, respectively), these results must be interpreted with caution. Only 15 respondents seropositive for HPV-11 reported never having had sex. This small number leads to an unstable and therefore uninterpretable estimate. Moreover, upon closer examination of the 15 respondents, we found that at least 14 were herpes simplex virus type 2 seropositive. Presence of 2 different sexually transmitted infections in this group may be an indication that the respondents either did not understand the sexual history questions or did not feel comfortable answering questions related to sexual history.

There was a significant trend for increasing HPV-11 seroprevalence up to 39 years of age in females and 49 years in males. Thereafter, HPV-11 appeared to decline although the downward trend was not found to be significant. This observed pattern suggests that the risk of HPV-11 infection begins as a person becomes sexually active and increases through the third decade in females and the fourth decade in males, after which it appears to gradually decline. Although we did not find significant decreases in seroprevalence in either males or females, the observed decrease may either represent a cohort effect such that older persons may have been less likely to be exposed to HPV-11 or a loss of antibodies to the virus over time.

As expected, we found the overall prevalence of HPV-11 (4.7%) to be lower than that previously reported for HPV-16 in the same population (13%).9 However, results of this study suggest that HPV-11 is a common sexually transmitted infection.

Other factors that were found to be independently associated with HPV-11 in the current study include nonwhite race (especially non-Hispanic African American race) and number of lifetime sex partners. About the latter, the data indicate that HPV-11 seroprevalence increases commensurate with increasing number of lifetime sex partners.

This study has some limitations. First, sexual behavior and other risk factors are self-reported and thus subject to reporting bias, including underreporting of risk factors. Second, use of serologic testing may underestimate infection with HPV-11 given the low rate of seroconversion after natural infection. In addition, while type-specific VLPs were used in the ELISA, cross-reactivity between closely related types, particularly HPV-6, cannot be excluded. Despite limitations, however, serology is currently the best approach to ascertaining exposure in the population. Finally, due to lack of HPV-6 VLPs required for testing specimens, we were unable to evaluate the seroprevalence of HPV-6 in this population.

The results of this study represent the most comprehensive picture of HPV-11 infection in the United States to date. Importantly, this study provides baseline data on the prevalence of HPV-11 before availability of a prophylactic vaccine against HPV 6, 11, 16, and 18, thereby allowing better assessment and evaluation of the impact of this vaccine on this common infection.

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