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\begin{document}

\title{Association of Sexual Behavior with HBV Infection Among Adults: Results
from the NHANES study}



\author[1]{Wei Zhao}%
\author[2]{Zhi-Qin Xie}%
\author[1]{Hong Gao}%
\author[1]{Lin Wu}%
\author[1]{Liang Zhao}%
\author[2]{Bin Feng}%
\author[1]{Yu-Qing Zhou}%
\affil[1]{Chongqing Emergency Medical Center}%
\affil[2]{Zhuzhou Central Hospital}%


\vspace{-1em}



  
  \date{June 13, 2024}


\begingroup
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\selectlanguage{english}
\begin{abstract}
\textbf{Background and Aims:} Although it is known that hepatitis B
virus (HBV) can be transmitted through sexual behavior, limited research
has been conducted on the specific types of sexual behavior that
facilitate transmission. The purpose of the research was to analyze the
association of sexual behavior with HBV infection in US adults.
\textbf{Method:} Four cycles (2009-2016) of National Health and
Nutrition Examination Surveys (NHANES) were collected, and 16569
participants were finally included. HBV infection was determined by a
positive HBV core antibody and participants were categorized into two
groups: ``yes'' and ``no'' group. Data pertaining to sexual behaviors
were gathered. The sexual identity group comprised individuals with no
sex, heterosexual, homosexual, bisexual, or unclear. The sexual type
group consisted of individuals with no sex, heterosexual vaginal sex,
heterosexual oral sex, heterosexual anal sex, heterosexual multiple
types, bisexual sex, male homosexual sex, female homosexual sex, or
unclear. Multivariable logistic regression was used to analyze the
association of sexual identity/type with HBV infection by adjusting
different covariates. \textbf{Results:} The present study comprised a
sample of 16,569 individuals between the ages of 18 and 69. Participants
with HBV infection were more likely to be 40-69 years predominant, men,
non-Hispanic Black. Additionally, these individuals were more likely to
have co-infections with HIV or HCV, engage in drug use or current
smoking, identify as homosexual or bisexual. After full adjustment, it
was found that homosexual men were associated with a higher risk of HBV
infection (odds ratio {[}OR{]}: 4.00, 95\% confidence interval {[}CI{]}:
2.09-7.64) compared to men without sexual behavior. Bisexual men (OR:
5.65, 95\% CI: 2.13-15) and men with heterosexual anal sex (OR: 4.52,
95\% CI: 1.12-18.2) were associated with a higher risk of HBV infection.
Notably, women engaging in any type of sexual behavior with men or women
did not have a significantly higher risk of HBV infection compared to
women without sexual behavior. \textbf{Conclusion:} The study showed
that homosexual men, bisexual men, and men with heterosexual anal sex
were found to be correlated with a higher risk of HBV infection. These
results may offer valuable insights for the pursuit of HBV elimination.%
\end{abstract}%



\sloppy


Association of Sexual Behavior with HBV Infection Among Adults: Results
from the NHANES study

Wei Zhao\textsuperscript{1+}, Zhi-Qin Xie\textsuperscript{2+}, Hong
Gao\textsuperscript{1}, Lin Wu\textsuperscript{1}, Liang
Zhao\textsuperscript{1}, Bin Feng\textsuperscript{2*}, Yu-Qing
Zhou\textsuperscript{1*}

\textsuperscript{1}Department of Hepatobiliary Surgery, Chongqing
Emergency Medical Center, Chongqing, China

\textsuperscript{2}Department of Hepatobiliary and Pancreatic Surgery,
Zhuzhou Hospital Affiliated to Xiangya School of Medicine, Central South
University, Zhuzhou City, Hunan Province, China

+These authors have contributed equally to this work and share first
authorship.

*Correspondence: Bin Feng, fengbin19720303@163.com; Yu-Qing Zhou,
zhouyuqing1977@hotmail.com

Abstract

\textbf{Background and Aims:} Although it is known that hepatitis B
virus (HBV) can be transmitted through sexual behavior, limited research
has been conducted on the specific types of sexual behavior that
facilitate transmission. The purpose of the research was to analyze the
association of sexual behavior with HBV infection in US adults.

\textbf{Method:} Four cycles (2009-2016) of National Health and
Nutrition Examination Surveys (NHANES) were collected, and 16569
participants were finally included. HBV infection was determined by a
positive HBV core antibody and participants were categorized into two
groups: ``yes'' and ``no'' group. Data pertaining to sexual behaviors
were gathered. The sexual identity group comprised individuals with no
sex, heterosexual, homosexual, bisexual, or unclear. The sexual type
group consisted of individuals with no sex, heterosexual vaginal sex,
heterosexual oral sex, heterosexual anal sex, heterosexual multiple
types, bisexual sex, male homosexual sex, female homosexual sex, or
unclear. Multivariable logistic regression was used to analyze the
association of sexual identity/type with HBV infection by adjusting
different covariates.

\textbf{Results:} The present study comprised a sample of 16,569
individuals between the ages of 18 and 69. Participants with HBV
infection were more likely to be 40-69 years predominant, men,
non-Hispanic Black. Additionally, these individuals were more likely to
have co-infections with HIV or HCV, engage in drug use or current
smoking, identify as homosexual or bisexual. After full adjustment, it
was found that homosexual men were associated with a higher risk of HBV
infection (odds ratio {[}OR{]}: 4.00, 95\% confidence interval {[}CI{]}:
2.09-7.64) compared to men without sexual behavior. Bisexual men (OR:
5.65, 95\% CI: 2.13-15) and men with heterosexual anal sex (OR: 4.52,
95\% CI: 1.12-18.2) were associated with a higher risk of HBV infection.
Notably, women engaging in any type of sexual behavior with men or women
did not have a significantly higher risk of HBV infection compared to
women without sexual behavior.

\textbf{Conclusion:} The study showed that homosexual men, bisexual men,
and men with heterosexual anal sex were found to be correlated with a
higher risk of HBV infection. These results may offer valuable insights
for the pursuit of HBV elimination.

Key words: sexual behavior, sexual identity, sexual type, hepatitis B
virus

\textbf{INTRODUCTION}

Chronic viral hepatitis B is a global affliction that imposes a
significant economic and medical burden on society. The persistence of
HBV infection in some individuals may result in chronic hepatitis B,
which can progress to cirrhosis and even liver
cancer\textsuperscript{{[}1{]}}. HBV and hepatitis C virus (HCV) are the
primary etiologic agents of liver cancer and overall mortality. Despite
the efforts of the US government to combat HBV, a considerable number of
individuals remain infected with the virus\textsuperscript{{[}2, 3{]}}.
Between 2001 and 2016, an estimated 7.6 million US adults aged 20-59
years were afflicted with HBV infection\textsuperscript{{[}4{]}}. The
challenge of eradicating HBV is formidable.

HBV, an infectious disease, can be transmitted through multiple routes.
The primary mode of transmission is from mother to neonate. Contaminated
blood products also pose a risk for HBV transmission. Furthermore, drug
use and sexual behavior are significant routes of
transmission\textsuperscript{{[}5{]}}.

Sexual behavior is a prevalent biological phenomenon in human beings,
serving various purposes such as the perpetuation of offspring,
expression of emotions, and others. Within society, the majority of
individuals identify as sexually heterosexual, while a sexual minority
exists, including those who identify as homosexual or
bisexual\textsuperscript{{[}6{]}}. Furthermore, individuals have
explored alternative forms of sexual activity, such as oral and anal
sex, as a means of avoiding vaginal sex, satisfying male pleasure, and
preventing unwanted pregnancy\textsuperscript{{[}7, 8{]}}. However,
sexual behavior may also result in the transmission of various diseases,
including HIV, HCV, HPV, and other sexually transmitted
infections\textsuperscript{{[}9-11{]}}, as well as certain cancers, such
as anal cancer and cervical cancer\textsuperscript{{[}7, 8, 12, 13{]}}.

The transmission of HBV through sexual activity has been firmly
established, particularly in the context of anal sex among homosexual
individuals\textsuperscript{{[}14-16{]}}. The European Union has
recognized men who have sex with men as a high-risk population for HBV
infection\textsuperscript{{[}17{]}}. However, limited research has been
conducted on the relationship between sexual identity/type and HBV
infection among homosexual, bisexual, and heterosexual individuals. It
was the first study to research the association between sexual behavior
and HBV infection among US adults, stratified by sexual identity/type.

\textbf{METHODS}

\textbf{Study Population}

The present study utilized data from the National Health and Nutrition
Examination Surveys (NHANES) spanning from 2009 to 2016. NHANES is a
nationally recognized center that examines demographic characteristics,
population health, and certain diseases, and provides publicly available
data. The investigation included a total of 40,439 participants;
however, due to age restrictions on certain questionnaires, individuals
under the age of 18 or over the age of 69 (N=19,791) were excluded.
Additionally, participants without complete responses to the sexual
behavior questionnaire regarding ''ever had vaginal, anal, oral sex''
(N=3,241) and those with missing data on anti-HBc examination (N=838)
were also excluded. Finally, 16,569 participants were included (Figure
1).

\textbf{Primary Exposure}

In the ``sexual behavior'' questionnaire, men were asked by'' ever had
vaginal sex with a woman'', ''ever had oral sex with a woman'', ''ever
had anal sex with a woman'', ''ever had any sex w/man: anal, oral'', and
women were asked by ''ever had vaginal sex with a man'', ''ever had oral
sex on a man'', ''ever had anal sex with a man'', ''ever had any kind of
sex w/woman''. Based on the sexual behavior of the population, we
categorized individuals into two groups: sexual identity and sexual
type. The sexual identity group comprised individuals with no sex,
heterosexual, homosexual, bisexual, or unclear. The sexual type group
consisted of individuals with no sex, heterosexual vaginal sex,
heterosexual oral sex, heterosexual anal sex, heterosexual multiple
types, bisexual sex, male homosexual sex, female homosexual sex, or
unclear.

\textbf{Outcomes}

As per the AASLD 2018 guidelines on hepatitis B, the presence of
positive HBV core antibody (anti-HBc) serves as an indicator of HBV
infection, including previous or present
infection\textsuperscript{{[}18{]}}. A detailed description for anti-HBc
detection has been reported in previous study\textsuperscript{{[}4{]}}.
Positive anti-HBc was classified under the ''yes'' group for HBV
infection, while negative anti-HBc was categorized under the ''no''
group.

\textbf{Covariates}

In the study, according to previous literature, several covariates were
included to adjust the models that described the association of sexual
behavior with HBV Infection. First, demographic characteristics
including age, gender, race/ethnicity, education, marital status,
poverty income ratio (PIR) were selected. The age group was classified
into three categories, namely 18-39, 40-59, 60-69 years. Race/ethnicity
was divided into five categories, including Mexican American, other
Hispanic, non-Hispanic White, non-Hispanic Black, and other Races,
comprising non-Hispanic multiracial. Education was classified into three
categories, namely less than high school, high school graduate, and more
than high school. The categorization of marital status comprised the
subsequent classifications: married, widowed/divorced/separated, never
married, and living with a partner\textsuperscript{{[}19{]}}. poverty
income ratio (PIR) was classified into \textless{}1.3, 1.3-1.8, and
\textgreater{}1.8\textsuperscript{{[}20{]}}. Body mass index (BMI) was
categorized as \textless{}25, 25-30, and [?]30. Smoking status was
classified as never smoking, former smoking, and current smoking.
Second, human immunodeficiency virus (HIV) infection, HCV infection, and
drug use were collected\textsuperscript{{[}6{]}}. All these variables
were categorized as ``yes'' and ``no'' group. Third, indicators of liver
function, including albumin (ALB), alanine aminotransferase (ALT),
aspartate aminotransferase (AST), alkaline phosphatase (ALP), gamma
glutamyl transferase (GGT), total bilirubin (TBIL), were included.

\textbf{Statistical Analysis}

Categorical variables were described as weighted percentages accompanied
by a 95\% confidence interval, and their comparison was computed
utilizing the chi-square test. Continuous variables were characterized
by their weighted mean \selectlanguage{ngerman}± standard deviation (SD), and their comparison
was calculated using a weighted linear regression model. The association
between sexual behavior and HBV infection was analyzed using
multivariable logistic regression models. The final model was adjusted
for age, race/ethnicity, education, marital status, PIR, HIV infection,
HCV infection, drug use, BMI, and smoking status. All statistical
analyses were conducted by Empowerstats 2.2 and STATA 17.0. The complex
survey design was represented using appropriate examination weights, and
statistical significance was determined at a level of p \textless{}
0.05.

\textbf{RESULTS}

\textbf{Characteristics of Participants}

A total of 16,569 participants were included in the study, with 50.09\%
(95\%CI: 49.08\%-51.1\%) being men and 49.91\% (95\%CI: 48.9\%-50.92\%)
being women, and an average age of 42.76 ± 14.57 years. \textbf{Table
1}summarizes all characteristics of the study stratified by HBV
infection (yes or no). The prevalence of HBV infection (including
previous or present infection) among US adults was approximately 4.04\%
(95\%CI: 3.72\%-4.38\%). The majority of outcomes exhibited
statistically significant differences when stratified by HBV infection.
Participants with HBV infection were more likely to be 40-69 years
predominant, men, non-Hispanic Black, with education less than high
school, with a poverty income ratio (PIR) \textless{}1.3. Additionally,
these individuals were more likely to have co-infections with HIV or
HCV, engage in drug use or current smoking, identify as homosexual or
bisexual, and exhibit elevated levels of ALT, AST, and GGT. The study
found that while no statistically significant difference was observed in
sexual behavior (yes or no) among individuals with HBV infection,
statistically significant differences were observed in sexual identity
and sexual type.

Furthermore, the characteristics of participants were compared and
stratified by sexual identity, as presented in \textbf{Table 5} . The
results indicated that the rates of HIV and HCV infection were
significantly higher among homosexual and bisexual individuals compared
to those without sexual behavior.

\textbf{Associations Between Sexual Identity and HBV Infection}

Sexual identity was classified into five groups,~including no sex
(3.94\%), heterosexual (88.43\%), homosexual (0.83\%), bisexual
(6.71\%), and unclear (0.09\%). In comparison to participants without
sexual behavior, the present study found that individuals who identified
as homosexual or bisexual had a significantly higher risk of HBV
infection across three models. Model 1 revealed that homosexual
individuals had an OR of 4.22 (95\%CI: 1.99-8.94) and bisexual
individuals had an OR of 1.73 (95\%CI: 1.15-2.59). Model 2 showed that
homosexual individuals had an OR of 5.75 (95\%CI: 2.63-12.55) and
bisexual individuals had an OR of 2.23 (95\%CI: 1.46-3.42). Model 3
demonstrated that homosexual individuals had an OR of 4.83 (95\%CI:
1.86-12.57) and bisexual individuals had an OR of 1.78 (95\%CI:
1.09-2.92). Notably, heterosexual individuals did not exhibit a
significant difference in HBV infection risk when compared to
participants without sexual behavior across all three models.

Upon stratification by gender, it was observed that among the men
population, individuals who identified as homosexual (OR=5.61, 95\%CI:
2.53-12.48) or bisexual (OR=4.32, 95\%CI: 2.51-7.44) exhibited a
increased risk of HBV infection in model 1, as compared to men without
sexual behavior. This trend persisted in models 2 and 3, where
homosexual (models 2: OR=7.96, 95\%CI: 3.51-18.05; models 3: OR=5.89,
95\%CI: 2.21-15.66) and bisexual (models 2: OR=4.45, 95\%CI: 2.48-7.99;
models 3: OR=4.2, 95\%CI: 2.2-8.03) individuals continued to demonstrate
a significantly elevated risk of HBV infection. Conversely, heterosexual
individuals did not exhibit a significant difference in HBV infection
risk as compared to men without sexual behavior across all three models.

However, in the women population, compared with women without sexual
behavior, whether heterosexual, or bisexual, no statistically
differences were observed across three models.

\textbf{Associations Between Sexual Type and HBV Infection}

According to the questionnaire, sexual type was classified into nine
groups, individuals with no sex (3.94\%), heterosexual vaginal sex
(10.23\%), heterosexual oral sex (0.59\%), heterosexual anal sex
(0.04\%), heterosexual multiple types (77.36\%), bisexual sex (6.71\%),
male homosexual sex (0.74\%), female homosexual sex (0.09\%), and
unclear (0.3\%).

In comparison to participants without sexual behavior, we found that
bisexual sex and male homosexual sex were found to be linked with an
increased likelihood of contracting HBV infection. Specifically, in
model 1, bisexual sex (OR=1.73, 95\%CI: 1.15-2.59) and male homosexual
sex (OR=4.82, 95\%CI: 2.25-10.31) were identified as having a higher
risk of HBV infection. In model 2, bisexual sex (OR=2.2, 95\%CI:
1.44-3.36) and male homosexual sex (OR=6.58, 95\%CI: 2.99-14.46) were
correlated with an increased risk of HBV infection. Similarly, in model
3, bisexual sex (OR=1.69, 95\%CI: 1.04-2.76) and male homosexual sex
(OR=5.23, 95\%CI: 1.95-13.99) were correlated with a higher risk of HBV
infection. Conversely, there were no significant differences observed in
heterosexual vaginal sex, heterosexual oral sex, heterosexual anal sex,
or heterosexual multiple types across the three models.

Upon stratification by gender, in the men population, comparing with men
without sexual behavior, heterosexual anal sex (OR=14.42, 95\%CI:
3.66-56.81), bisexual sex (OR=4.32, 95\%CI: 2.51-7.44) and male
homosexual sex (OR=5.61, 95\%CI: 2.53-12.48) exhibited an increased risk
of HBV infection in model 1. Heterosexual anal sex (OR=4.75, 95\%CI:
1.22-18.47), bisexual sex (OR=4.34, 95\%CI: 2.43-7.77) and male
homosexual sex (OR=7.75, 95\%CI: 3.43-17.52) were found to be linked
with an increased risk of HBV infection in model 2. Heterosexual anal
sex (OR=4.52, 95\%CI: 1.12-18.2), bisexual sex (OR=4.00, 95\%CI:
2.09-7.64) and male homosexual sex (OR=5.65, 95\%CI: 2.13-15) were found
to be linked with an increased risk of HBV infection in model 3. No
significant differences were observed in heterosexual vaginal sex,
heterosexual oral sex, or heterosexual multiple types across all three
models.

However, among the women population, compared with women without sexual
behavior, whether heterosexual vaginal sex, heterosexual oral sex,
heterosexual multiple types, bisexual sex, no statistically differences
were observed across three models.

\textbf{Associations Between Gender and HBV Infection}

Table 1 indicated a higher proportion of HBV infection in men compared
to women, while in model 1, 2, and 3 of table 4, women were found to
have a lower risk of HBV infection (OR=0.78, 95\%CI: 0.66-0.92; OR=0.71,
95\%CI: 0.6-0.85; OR=0.79, 95\%CI: 0.64-0.97).

\textbf{DISCUSSION}

In the sexual identity group, it was observed that individuals
identifying as bisexual or homosexual had a significantly higher
prevalence of HBV infection compared to those without any sexual
behavior. To account for the potential impact of gender, the data was
stratified by gender, revealing that bisexual and homosexual men had a
significantly higher prevalence of HBV infection compared to men without
any sexual behavior. However, no significant difference was observed
among women of all sexual identities. Further analysis was conducted by
grouping heterosexual individuals into heterosexual vaginal sex,
heterosexual oral sex, heterosexual anal sex, and heterosexual multiple
types. The incidence of HBV infection was found to be significantly
higher in men with heterosexual anal sex as compared to those without
sexual behavior, but no significant difference was observed in three
other groups. Bisexual men, homosexual men and men with heterosexual
anal sex may be focus populations for the elimination of HBV targets.

It is noteworthy that HBV infection has affected approximately 250
million individuals globally. HBV infection is one of the main causes of
liver cirrhosis and liver cancer, increasing the economic burden of the
people and the medical burden of the society. Despite the widespread
dissemination of HBV medical information and the existence of
professional organizations dedicated to the treatment of HBV
infection\textsuperscript{{[}1{]}}, there remains a significant portion
of the population who are unaware of their HBV infection status. This
lack of awareness poses challenges to follow-up treatment, increases
costs, and may even result in secondary
transmission\textsuperscript{{[}21{]}}. Therefore, it is imperative to
expand the dissemination of information regarding HBV screening,
transmission routes, vaccination, and the consequences of infection, in
order to raise awareness and promote prevention efforts.

Certain studies have suggested that sexual behavior is a significant
risk factor for the transmission of HBV\textsuperscript{{[}17, 22{]}},
and recent data from the United States indicates that approximately
one-third of acute HBV infections were associated with sexual behavior
during 2013-2018\textsuperscript{{[}23{]}}. Despite this, limited
research has been conducted on the relationship between sexual
type/identity and HBV infection.

Our findings indicate that men with heterosexual anal sex were 4.52
times more likely to contract HBV than men without sexual behavior.
However, no significant differences were observed in the risk of
contracting HBV through heterosexual vaginal sex, heterosexual oral sex,
or heterosexual multiple types of heterosexual sexual behavior. These
results suggested that heterosexual anal sex may be a particularly
high-risk factor for HBV infection. A literature also reported that
heterosexual anal sex contributed to the transmission of
HIV\textsuperscript{{[}24{]}}. Furthermore, the prevalence of HBV
infection was found to be 5.23 times higher in male homosexual sex and
1.69 times higher in bisexual sex compared to men without sexual
behavior. Homosexual and bisexual men were identified as being at a
greater risk of HCV and HIV infection, which is consistent with the
findings of a survey\textsuperscript{{[}25{]}}. A research also revealed
that the rate of HBV infection in individuals with HIV was 6.5 times
higher than in those without HIV\textsuperscript{{[}26{]}}. The
potential correlation between decreased counts and dysfunction of CD8+
and CD4+ T cells resulting from HIV infection and an increased
susceptibility to HBV infection has been suggested as a contributing
factor to the higher incidence of HBV co-infection among homosexual and
bisexual men\textsuperscript{{[}27, 28{]}}. In light of this,
preventative measures such as condom use and health screenings for
high-risk groups should be prioritized to mitigate transmission.

Nonetheless, the study found no statistically significant disparities
among women, regardless of their sexual identity or sexual type. In the
study, participants with HBV infection were more likely to be men
predominant. The authors, Robin Brown et al., attributed this gender
dimorphism to variations in sex hormone levels and immune factors, which
may account for the observed differences in HBV infection rates between
men and women\textsuperscript{{[}29, 30{]}}. Specifically, estrogen and
its interaction with estrogen receptors may have a suppressive impact on
HBV.

Furthermore, the prevalence of drug use was observed to be higher in the
HBV infection group compared to the non-HBV infection group, as reported
by Jaimie Z. Shing et al\textsuperscript{{[}4{]}}. The study revealed
that approximately 20\% of adults with a history of drug use were
infected with HBV, which was significantly higher than the proportion
observed in the general population. Drug use was identified as one of
the common modes of HBV transmission\textsuperscript{{[}5{]}}.
Additionally, previous research has demonstrated that the proportion of
smokers is higher in individuals with hepatitis B infection, which
aligns with our findings. Furthermore, smoking was correlated with an
increased risk of hepatitis B-related liver
cancer\textsuperscript{{[}31, 32{]}}.

To achieve the objective of the World Health Organization to eliminate
HBV by 2030, it was imperative to implement measures aimed at reducing
the transmission of HBV through sexual behavior
pathways\textsuperscript{{[}5{]}}. Furthermore, vaccination and regular
screening were deemed crucial.

However, our study was subject to certain limitations. The employment of
cross-sectional design in NHANES data enabled us to establish a
potential association between sexual behavior and HBV infection, but not
a causal relationship. Sexual behavior was from questionnaire, maybe
some bias existed. Furthermore, the absence of data on protective
measures, such as condom use, leading to the absence of this important
variable as covariates for the analysis.

\textbf{CONCLUISION}

In conclusion, the study findings indicated that homosexual men,
bisexual men, and men with heterosexual anal sex were found to be linked
with an increased risk of HBV infection. They should be the focus
populations for World Health Organization's goal of eliminating HBV by
2030.

\textbf{AUTHOR CONTRIBUTIONS}

WZ and Z-QX contributed to the conception and design, the acquisition,
analysis, interpretation of the data, the drafting of the article, or
critical revision for important intellectual content. HG, LW, LZ, and
H-ZZ collected data. BF and Y-QZ contributed to the conception and
design, the reviewing of the article, or critical revision for important
intellectual content. All authors approved the final version and agreed
to be accountable for all aspects of the work.

\textbf{ACKNOWLEDGMENTS}

We wish to thank colleagues of the National Health and Nutrition
Examination Survey (NHANES) program for their effort in data collection.

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Figure 1 A flowchart showing the selection of study participants.
NHANES, National Health and Nutrition Examination Survey.\selectlanguage{english}
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