https://orcid.org/0000-0002-1938-9365
ABSTRACT
This anonymous cross-sectional study aimed to investigate the relationships between HIV infection and mpox-related focus issues among Chinese men who have sex with men (MSM). This study involved in 27 MSM social organizations and was conducted from July 31 to August 4, 2023. Mpox vaccination hesitancy was defined as the proportion of participants who expressed unwillingness to receive self-funded and free vaccines. Logistic regression models were employed to estimate odds ratios (OR) and 95% confidence interval (95%CI). Of 7196 MSMs, the prevalence of mpox differed between people living with HIV (PLWH) (1.04%, 20/1920) and people living without HIV (PLWoH) (0.55%, 29/5276) (P = .037). However, after adjusting for all covariates, there was no significant association between HIV status and mpox (aOR = 1.17; 95%CI = 0.58, 2.39; P = .658). Furthermore, the crude rates of vaccination hesitation (PLWoH: 5.91%, PLWH: 4.11%; P = .004) and consultation hesitation (PLWoH: 16.22%, PLWH: 10.78%; P < .001) were both lower in the PLWH. Compared with PLWoH, PLWH had lower odds ratios of vaccination hesitation (aOR = 0.70; 95%CI = 0.53, 0.92; P = .011) and consultation hesitation (aOR = 0.74; 95%CI = 0.60, 0.90; P = .003) among MSM. The estimate of association between HIV status and consultation hesitation was even smaller among MSM who reported hepatitis C infection or uncertainty (aOR = 0.30; 95%CI = 0.15, 0.56), compared with those without hepatitis C (aOR = 0.73; 95%CI = 0.60, 0.89) (P for interaction = .037). MSM living with HIV in China demonstrated a greater willingness to accept mpox vaccination and medical consultation. In the future, it is recommended that medical institutions establish good medical environment to control the mpox epidemic, especially for PLWH.
KEYWORDS:
Introduction
Mpox (formerly known as monkeypox) virus infections usually occur in the African region and occasionally spread to the United Kingdom (UK) and the United States (US).Citation1–3 At the beginning of 2022, since the UK reported an imported mpox case from Nigeria, multiple countries began to report mpox cases.Citation4,Citation5 This multinational outbreak was quickly defined as the Public Health Emergency of International Concern (PHEIC) by the World Health Organization (WHO) on July 23, 2022.Citation6 By August 2, 2023, more than 88,000 confirmed mpox cases had been reported across 113 countries or territories.Citation7 In contrast to previous cases, the main infected population in this outbreak was men who have sex with men (MSM).Citation8,Citation9 Although there are three antiviral agents with activity against mpox, including cidofovir, brincidofovir, and tecovirimat,Citation10 the focus of human immunodeficiency virus (HIV) status in transmission and treatment of mpox occurred due to the similar risk population of mpox and HIV, immunosuppression of people living with HIV (PLWH), and stigma.Citation8,Citation11 Laurenson-Schafer et al. reported that 48% of mpox cases in the past year were PLWH (16961/35,329).Citation8 Furthermore, mpox cases living with HIV had a higher odds ratio of hospitalization.Citation8 However, there is a lack of recent national evidence on associations between HIV status and mpox virus infection.
On July 26, 2023, China subsequently announced the Mpox prevention and control program in order to control the spread of mpox, considering the nearly 500 confirmed cases of mpox across 23 provinces, autonomous regions and municipalities, as well as the size and activity of the MSM population in China.Citation12–14 Vaccination is considered as the effective way to curb infectious diseases.Citation15 Although there have been instances of infections or reinfections after vaccination, the clinical features and outcomes of them appear to be less severe.Citation16 Currently, in China, there is no access to the mpox vaccine, but its development is underway.Citation17 The rate of vaccination hesitation for other vaccines, particularly for influenza and human papilloma virus (HPV) is high among Chinese population.Citation18,Citation19 For instance, Wang et al. reported that the overall median rate of HPV vaccination refusal across China was 28.2%.Citation19 Vaccination hesitation is not conducive to the popularization of vaccination and may hinder efforts to end the mpox epidemic in the future. In our previous study, we analyzed the factors that influenced mpox vaccination in PLWH and PLWoH.Citation20 However, we did not analyze the association between HIV status and hesitation toward mpox vaccination. PLWH may face greater challenges in receiving the mpox vaccine due to concerns about the safety of the vaccine in immunocompromised populations.Citation21
In China, individuals who engaged in high-risky behavior or a related epidemiological history, suspected infections, or close contacts with infected individuals could seek consultation for mpox at an infectious disease specialist hospital or the dermatology department of a general hospital. People could test mpox at hospitals and Chinese Centers for Disease Control and Prevention (CDC). Up until now, due to the limited number of cases in each province, most of the cases were tested for free using nucleic acid detection at the CDC. The hesitation to seek medical consultation hinders the timely detection, isolation, and treatment for mpox cases, thereby increasing the challenge of finding the source of infection and cutting off the transmission. Considering privacy concerns, stigma, and limited access to medical settings, PLWH may hesitate to seek medical consultation for mpox.
Up to now, the association of HIV status with mpox-related focus issues, including mpox virus infection, mpox vaccination hesitation, and consultation hesitation for mpox were unknown among Chinese MSM. This study aimed to provide the latest relevant evidence to assist in formulating clinical and public health management policies, with the assistance of the 27 social organizations for MSM in China.
Materials and methods
Data source
Our participants were recruited from 27 MSM social organizations across 21 provinces, municipalities, and autonomous regions of China, between July 31 and August 4, 2023. The details were described in our previous study.Citation20 We recruited MSM who were at least 18 years old and reported engaging in sexual activities with at least one man in the past 12 months (including anal sex, oral sex, hand sex, hugging, touching, kissing, etc.) in mainland China. Participants provided informed consent. After excluding 342 MSM with unknown HIV status, we finally included 7196 MSM. The Ethics Committee of the Guizhou Center for Disease Control and Prevention (Q 2022–02) approved the study’s design, details, and procedures of the study.
Assessment of HIV status, mpox virus infection, mpox vaccination hesitation, and consultation hesitation for mpox
HIV status was assessed by asking one question: “Have you been diagnosed with HIV?.” Participants who answered “yes” were classified as PLWH, and those who answered “no” were classified as people living without HIV (PLWoH). Participants who selected the option of “uncertainty” were excluded from this study.
Our primary outcomes included mpox virus infection, mpox vaccination hesitation, and consultation hesitation for mpox. After informing participants about the symptoms of mpox and the diagnostic standard based on the Mpox prevention and control program,Citation13 we classified those who answered “diagnosed by a medical institution” as mpox virus infections. Mpox vaccination hesitancy was defined as the proportion of participants who answered “not willing to take self-funded and free vaccines” when asked whether they were willing to receive vaccines against mpox if available. Medical consultation hesitation for mpox was assessed by asking one question: “If you were infected with the mpox virus, which of the following measures would you prefer?.” The options included the “infectious disease specialist hospital,” “the dermatology department of a general hospital,” “related social organizations,” “the local CDC,” “self-medication,” “quarantine at home” and “no measures.” Participants who did not select the first two options were considered to have consultation hesitation.
Covariates
All information was collected by trained healthcare personnel through an electronic questionnaire. Covariates included age group (18 ~ 35 years, ≥36 years), occupation (employed, unemployed), ethnicity (Han, minorities), educational level (junior high school and below, high school, undergraduate, postgraduate, and above), residence (eastern region, western region, and central region), marital status (married, unmarried, widowed, or divorced), sexual orientation (homosexual, bisexual, and unsure), mpox-related knowledge (low, moderate, high), sexual diseases excluding HIV (syphilis, gonorrhea, condyloma acuminatum, genital herpes, and genital chlamydia trachomatis, etc.; yes, no), hepatitis C (yes, no, unsure), and level of sexual risky behavior (low, moderate, high).
Seven items, including sources of infection, possible routes of transmission, susceptible populations, clinical symptoms, vaccines, specific drugs, and preventive measures were used to assess mpox-related knowledge based on our previous studies.Citation22,Citation23 We assigned one point for each correct answer and then calculated the total score for mpox-related knowledge. Total scores ranged from 0 to 23, with higher scores indicating better knowledge. A score of zero represented low mpox-related knowledge, while a score of one to six represented moderate mpox-related knowledge. A score of seven or higher represented high mpox-related knowledge.Citation22,Citation23 Sexual risky behavior was determined based on three sexual behaviors: condomless anal intercourse, commercial sex, and group sex in the last month, as indicated by previous studies.Citation24,Citation25 We assigned a score of zero for option “no” and a score of one for all other responses for the last two behavior components. Regarding the behavior component of condomless anal intercourse, we allocated a score of one for individuals who reported engaging in this behavior “always” or “often,” while a score of zero was assigned to those who reported engaging in it “never” or “seldom.” High sexual risky behavior was indicated by the presence of all three factors, while low sexual risky behavior was indicated by the absence of any of the three behaviors, otherwise moderate sexual risky behavior.
Data analysis
Means ± standard deviations (SDs) and percentages were employed to describe continuous variables and categorical variables, respectively.
Univariate analysis was conducted using Chi-square test. Logistic regression models were conducted to estimate odds ratios (OR) and 95% confidence intervals (95% CI), while accounting for various adjustments to control for potential confounding factors. Model 1 was a univariate model. Model 2 accounted for adjustments in age group, occupation, ethnicity, educational level, residence, and marital status. Based on model 2, we additionally adjusted sexual orientation, mpox-related knowledge, sexual diseases excluding HIV, hepatitis C, sexual risky behavior, and other two outcomes in model 3. The statistical significance of an interaction was assessed by incorporating a product term in the model 3 during the stratified analysis. We measured the interaction of the product term.Citation26,Citation27 All analyses were conducted using R 4.2.0. A two-sided P value less than .05 was considered to be statistically significant.
Results
Population characteristics
displays the baseline characteristics of the participants. Of the 7163 MSM (32.25 ± 13.74 years), 44.44% of them lived in eastern China. More than half of them were younger than 35 years old (72.50%) and had a bachelor’s degree or higher (52.13%). The prevalence of mpox virus infection was 0.68% (49/7196). The rate of mpox vaccination hesitation and mpox consultation hesitation was 5.43% (391/7196) and 14.77% (391/7196), respectively ().
Table 1. Population characteristics by mpox status among men who have sex with men in China.
The prevalence of mpox virus infection, the rate of mpox vaccination hesitation and consultation hesitation were all higher among unemployed MSM, those with an educational level of junior high school and below, and those who were married (). In addition, MSM who identified as bisexual (1.10%), those who reported having other sexual diseases (2.72%), hepatitis C (15.38%), and engaging in high-risky sexual behavior (13.21%) had a higher prevalence of mpox virus infection. Furthermore, MSM who were aged 36 years or older (7.02%), those who identified as bisexual (6.61%), and those who had low mpox-related knowledge (13.04%) had a higher rate of vaccination hesitation. It was found that MSM who were aged 36 years or older (50.76%), minorities (19.48%), those residing in the western region (17.09%), those who had low mpox-related knowledge (84.27%), those who reported unknown hepatitis C (19.39%), and those who reported engaging high-risky sexual behavior (33.96%) had a higher rate of consultation hesitation ().
Associations of HIV status with mpox virus infection, mpox vaccination hesitation and consultation hesitation for mpox
The crude prevalence of mpox virus infection was higher in the PLWH (1.04%, 20/1920), compared with PLWoH (0.55%, 29/5276) (P = .037). Compared with PLWoH, PLWH had a higher odds ratio of mpox virus infection in both univariate model 1 and model 2. However, after controlling for all covariates, HIV status was not associated with mpox virus infection (aOR = 1.17; 95%CI = 0.58, 2.39; P = .658) (). There was no significant interaction observed among subgroups in relation to the associations between HIV status and mpox virus infection (Table S1).
Table 2. Associations of HIV status with mpox virus infection, mpox vaccination hesitation, and consultation hesitation for mpox.
The crude rate of mpox vaccination hesitation (PLWoH: 5.91%, 312/5276; PLWH: 4.11%, 79/1920; P = .004) and consultation hesitation for mpox (PLWoH: 16.22%, 856/5276; PLWH: 10.78%, 207/1920; P < .001) were both lower in the PLWH, compared with the PLWoH (). In the multivariable-adjusted analysis, after adjusting for all covariates, compared with PLWoH, PLWH had lower odds ratios of mpox vaccination hesitation (aOR = 0.70; 95%CI = 0.53, 0.92; P = .011) and consultation hesitation for mpox (aOR = 0.74; 95%CI = 0.60, 0.90; P = .003) (). Subgroup analysis showed that there was no significant interaction observed among subgroups in relation to the association between HIV status and mpox vaccination hesitation (Table S2). However, differences were observed within hepatitis C group regarding the relationship between HIV status and consultation hesitation for mpox (). The estimated association between HIV status and consultation hesitation for mpox was found to be smaller among MSM who reported hepatitis C infection or were unsure (aOR = 0.30; 95%CI = 0.15, 0.56), compared with those without hepatitis C (aOR = 0.73; 95%CI = 0.60, 0.89) (P for interaction = .037).
Figure 1. Subgroup analysis on associations between HIV status and consultation hesitation for mpox.
Discussion
To the best of our knowledge, this study is the first to provide insights into the association between HIV status and mpox-related focus issues among MSM in China. Of 7196 MSM, we observed a higher crude prevalence of mpox virus infection in PLWH, compared with PLWoH. In contrast, the crude rate of mpox vaccination hesitation and consultation hesitation for mpox were both lower in PLWH, compared with PLWoH. However, after adjusting for all covariates, HIV status was not associated with mpox virus infection. Importantly, compared with PLWoH, PLWH had lower odds ratios of mpox vaccination hesitation and consultation hesitation for mpox.
PLWH accounted for approximately 48% of the mpox cases in the multinational outbreak between Jan 1, 2022, and Jan 29, 2023.Citation8 HIV may increase the risk of hospitalization.Citation8 Therefore, comprehending the HIV epidemic and its relation with mpox-related issues is crucial in order to effectively mitigate mpox epidemic. We observed a crude prevalence of mpox virus infection in the PLWH, compared with the PLWoH. However, after adjusting for all covariates, this relation was not significant. We speculated that PLWH were more likely to engage risky sexual behavior, resulting in a higher prevalence of mpox virus infection. Therefore, after controlling for other factors such as risky sexual behavior, HIV status was not associated with mpox virus infection.
Previous research has indicated that Chinese healthcare professionals have a higher acceptance rate of mpox vaccine, compared with those residing in other non-endemic countries in 2022.Citation28 We supplemented the additional evidence regarding the differences in mpox vaccination hesitation among MSM with varying HIV status in China.Citation28 Contrary to speculation, our findings revealed that compared with PLWoH, PLWH had a lower odds ratio of mpox vaccination hesitation. Li et al. found that PLWH expressed support for mpox vaccination promotion among MSM.Citation29 Third-generation mpox vaccines were safer for use in immunocompromised populations.Citation21 The vaccine effectiveness of the third-generation smallpox vaccine (MVA-BN) against mpox was 87% for one-dose vaccination and 89% for two-dose vaccination.Citation30 The reduction of vaccination hesitancy among MSM living with can have significant benefits, such as promoting herd immunity and improving the capacity for public health emergency response in China. It was noted that development of the mpox vaccine should be continued with consideration for its applicability among PLWH. The requirement of two dose vaccines was still an impediment to rapid outbreak response.Citation21 Furthermore, our findings indicate that PLWH were more likely to accept medical consultation for mpox, particularly those who were coinfected with hepatitis C. Medical consultation hesitancy had detrimental effects on the timely management of cases and the detection of close contacts, which are crucial in controlling the transmission of mpox. The Chinese CDC reported only 89.2% of the 491 cases were identified through proactive medical consultation.Citation13 Approximately 69.2% of the participants agreed that media-related content about mpox contributed to the stigmatization of gay, bisexual, and other men who have sex with men in US.Citation31 It is also important to consider the sociological perspective when addressing the treatment of infectious diseases in order to protect individuals’ privacy. Protecting individuals’ privacy and mitigating social stigma are essential factors that promote a proactive approach to seeking medical consultation. In addition, our study revealed that MSM those who lived in western region had a higher rate of consultation hesitation. The regional disparities in mpox-related issues also evident in the US.Citation31,Citation32 Owens et al.Citation32 reported that rural MSM, in comparison with their urban counterparts, were less likely to report perceiving severe consequences acquiring mpox. The findings regarding regional disparities in mpox-related issues were crucial in formulating targeted interventions at the provincial level. Our study has demonstrated the necessity for hospitals to proactively prepare for prevention and control of mpox and establish a good medical environment in the future, particularly for PLWH.
The notable strength of this article was that it included a large sample size of over 7000 MSM in China. However, there were some limitations in our study. Firstly, it should be noted that the data regarding HIV status, other sexual diseases, hepatitis C, and mpox-related issues were obtained through self-reporting. This method of data collection may introduce a potential call bias. Furthermore, to ensure better comprehension among participants, we opted to use condyloma instead of HPV all-serotypes in the assessment of sexual diseases. It is noted that condyloma does not encompass all HPV-related infections or diseases. Therefore, we should investigate all HPV serotypes to thoroughly explore the relationship between other sexual diseases and mpox. In addition, it is important to acknowledge the high risk of social desirability bias that cannot be neglected because of stigma and privacy concerns. Secondly, our study did not account for other factors that may have influenced the association between HIV status and mpox virus infection, including the utilization of pre-exposure prophylaxis (PrEP) and smallpox vaccination. Thirdly, our study did not encompass the entire population of MSM in China, thus introducing a potential selection bias. However, due to the hidden nature of MSM population, the survey of MSM population based on 27 MSM social organizations can ensure the accessibility of the target population. Finally, it is important to highlight that the lack of access to the mpox vaccine in mainland China could potentially impact the rate of mpox vaccination hesitancy. Additionally, in accordance with the Mpox prevention and control program, we did not include self-assessment of mpox virus infections. However, self-assessment of infections may mean mpox infection of people who reported consultation hesitation. The actual rate of mpox virus infection may be underestimated.
In conclusion, our findings indicate that MSM living with HIV express a higher level of willingness to accept mpox vaccination and engage in medical consultation. In order to effectively curb the mpox epidemic, particularly among PLWH, it is imperative for medical institutions to establish a conducive medical environment in the future.
Ethics approval and consent to participate
The study’s design, details, and procedures were approved by the Ethics Committee of the Guizhou Center for Disease Control and Prevention (Q 2022–02). All participants had informed consent at the time of participation. The research has been performed in accordance with the Declaration of Helsinki.
Author contribution statement
MZ, GY, ML and JL conceptualized and designed the study, MD, MZ, YY, XQ, YZ, LM, RT, ZZ, FZ, SD and JY did data acquisition and data curation, MD did formal analysis, visualization and writing – original draft, JL, GY, ML and MZ did writing- reviewing and editing. All authors have seen and approved the submitted version of this manuscript.
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We appreciate the works by all authors for original data.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Data availability statement
Data are obtained according to corresponding author permission.
Supplementary material
Supplemental data for this article can be accessed on the publisher’s website at https://doi.org/10.1080/21645515.2023.2290788.
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References
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