Article Text
PDF
Abstract
Objective The available epidemiological and clinical evidence from the currently ongoing monkeypox (MPX) outbreak in non-endemic areas suggests an important factor of sexual transmission. However, limited information on the behaviour and experiences of individuals with an MPX infection has to date been provided. We aimed to describe the initial phase of the MPX outbreak in Belgium, and to provide a more in-depth description of sexual behaviour and transmission contexts.
Methods We used routine national surveillance data of 139 confirmed MPX cases with date of symptom onset until 19 June 2022, complemented with 12 semistructured interviews conducted with a subsample of these cases.
Results Sexualised environments, including large festivals and cruising venues for gay men, were the suspected exposure setting for the majority of the cases in the early outbreak phase. In-depth narratives of sexual behaviour support the hypothesis of MPX transmission through close physical contact during sex. Despite awareness of the ongoing MPX outbreak, low self-perceived risk of MPX acquisition and confusing initial signs and symptoms for other STIs or skin conditions delayed early detection of an MPX infection. In addition, we describe relevant contextual factors beyond individual behaviour, related to sexual networks, interpersonal interactions and health systems. Some of these factors may complicate early MPX detection and control efforts.
Conclusion Our results highlight the role of sexual contact and networks in the transmission of MPX during the early phase of the outbreak in Belgium. Risk communication messages should consistently and transparently state the predominant sexual transmission potential of MPX virus, and prevention and control measures must be adapted to reflect multilevel factors contributing to MPX transmission risk.
- Sexual Behavior
- QUALITATIVE RESEARCH
- Epidemiology
- Behavioral Sciences
Data availability statement
Data are available upon reasonable request. All relevant data supporting our findings are included in this published article. The complete dataset of conducted interviews is not made publicly available because they might contain information that could identify other persons, yet additional anonymised data are available from the corresponding author on reasonable request.
This article is made freely available to access and read on the journal website in accordance with BMJ’s website terms and conditions for the duration of the monkeypox emergency or until otherwise determined by BMJ. You may download and print the article for personal or non-commercial use provided all copyright notices and trademarks are retained. If you wish to reuse any or all of this article please use the request permissions link.
Statistics from Altmetric.com
WHAT IS ALREADY KNOWN ON THIS TOPIC
Monkeypox virus is known to spread among humans mainly through close physical contact. Clinical and epidemiological information from the ongoing global outbreak suggests that sexual contact might be a particularly efficient form of monkeypox transmission, yet we lack a contextualised understanding of transmission dynamics.
WHAT THIS STUDY ADDS
Combining routine Belgian surveillance data with a unique insight into the narratives of people who acquired monkeypox, our study confirms the high sexual transmission potential of monkeypox virus and reveals important interpersonal, network-level and health system factors contributing to efficient transmission contexts for monkeypox.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
Our study demonstrates the importance of risk communication and outbreak control measures that address the multilevel factors associated with monkeypox transmission.
Background
In the first half of May 2022, the UK reported several cases of laboratory-confirmed monkeypox (MPX) virus infection.1 Soon after, other countries in Europe, including Portugal, Italy and Belgium, reported similar cases, raising the alarm for potential widespread transmission of MPX.2–4
Not only the scale of this current outbreak is unprecedented, but also the geographical spread and the transmission mode. Historically, only few cases have occurred outside Central and Western Africa, mostly import related through infected animals or travellers and with limited secondary attack rates.5–12 However, as of 20 October 2022, 75 345 confirmed cases of MPX have been reported from 109 countries globally.13 People identifying as gay and bisexual men having sex with men (gbMSM) have been disproportionately affected.14 15 This raises questions about the role of sexual behaviour in the transmission of MPX. Apart from zoonotic transmission, human-to-human transmission in endemic countries is thought to occur through direct or indirect contact with skin lesions or bodily fluids, or via respiratory droplets during prolonged face-to-face contact.16 17 Although transmission during sexual contact has been speculated, it was never confirmed in these settings.18 In the current outbreak, however, patients predominantly presented with localised anogenital or oral lesions, suggesting transmission through local inoculation via close physical contact during sex.15 19 20 There is a need to unravel sexual behaviour histories and relevant contextual factors contributing to transmission risks, to better understand MPX transmission dynamics.
The first MPX case in Belgium was notified on 19 May 2022. On 21 October 2022, Belgium had become one of the most affected countries globally, reporting 67.61 cases per 1 million inhabitants.21 Cases clustered mainly in urban areas, especially in and around the city of Antwerp, with many initial cases reporting an epidemiological link to an international gay-oriented fetish festival that took place from 5 to 8 May 2022.22 In Belgium, all suspected MPX cases are referred to designated facilities for clinical assessment and laboratory confirmation within specialised infectious disease units.
The objective of this study was to describe the initial phase of the outbreak in Belgium and to provide a more in-depth description of sexual behaviour and transmission contexts.
Methods
Study design
We conducted a rapid cross-sectional, observational, mixed-methods study of laboratory-confirmed MPX cases with onset of symptoms between 10 May and 19 June 2022 in Belgium.
Data collection and analysis
This study was based on two distinct, yet inter-related, data sources: national routine surveillance data of confirmed MPX cases, and narrative data from semistructured interviews conducted with a subsample of these cases.
National routine surveillance
Probable and confirmed cases of MPX are mandatory notifiable to the three regional health authorities in Belgium. A confirmed case was defined as a person with an MPX virus-specific PCR assay positive result or an orthopoxvirus-specific PCR assay positive result, and symptom onset since 1 March 2022, as defined by the European Centre for Disease Prevention and Control.6 All cases are interviewed by the regional public health authorities to collect information on the most probable source of infection and to initiate contact tracing. The Belgian Institute for Public Health (Sciensano) is responsible for epidemiological follow-up, risk assessment and development of guidelines for healthcare workers. As part of the outbreak management procedures, a linelist is constructed with the information collected by the regional health authorities on demographic characteristics, diagnosis, clinical symptoms and possible exposure settings and transmission routes during the 21 days before symptom onset (presumed incubation period). We extracted MPX cases with date of symptom onset until 19 June (N=139) from this linelist to use as a basis for the epidemiological description of the initial weeks of the outbreak. Statistical analyses were performed with R (V.4.0.5).
Semistructured interviews with MPX-confirmed cases
To gain a contextualised understanding of the perspective and behaviour of those affected, we additionally conducted semistructured interviews with a subsample of the initial cases. Participants were all recruited between 24 May and 30 June 2022 at a large STI clinic in Antwerp, which reported the majority of cases. The attending physician asked patients’ informed consent to be contacted by a researcher for an interview at the time of clinical MPX diagnosis. Out of 62 patients, 47 provided consent to be contacted. Of these, a sample of 19 were contacted by the first author (JV) with the invitation to participate. Of these, 12 agreed to participate in this study. Initially, we conducted interviews with all consenting individuals who were available for an interview (ie, convenience sampling). In a later stage, participants were more purposely selected, guided by emergent findings after preliminary analysis of the first interview data and as per the iterative nature of qualitative research. Notably, people with atypical clinical manifestations or symptoms (eg, skin lesions outside the anogenital area, a single isolated skin lesion with or without general symptoms) or particularly information-rich cases based on clinical judgement of the attending physician (eg, a clear epidemiological link, no self-reported history of sexual contact) were intentionally recruited to allow for maximum variation.
Interviews were held via telephone or online, using Zoom, and lasted between 30 and 60 min. All interviews were conducted by a social science researcher with a medical background and trained in qualitative research, guided by a questionnaire containing both open-ended and closed-ended questions (see online supplemental material 1). Questions related to sociodemographic background, social and sexual behaviour during the 3 weeks before symptom onset, epidemiological linkages related to MPX (eg, contact with known MPX cases), and health-seeking behaviour and risk perception related to MPX. Interviews were not recorded to foster a feeling of trust, yet answers were documented in the questionnaire and detailed notes were taken instead.
Supplemental material
The first author (JV) analysed the interview data by creating a data matrix of questionnaire responses using a spreadsheet manager (MS Excel V.2108), supplemented with thematic coding of the researcher’s notes and free-text data using the Framework Method.23
Results
General description of the initial outbreak
The first case of confirmed MPX in Belgium developed symptoms on 10 May. Afterwards, numbers steadily increased, from 3 cases during the first week to 58 cases during the sixth week of the epidemic, as shown in the epidemic curve (see figure 1). This epidemic curve also shows the probable exposure settings. While 31 (61%) cases indicated a gay-oriented festival as being the probable source of infection in the first 4 weeks, this decreased and was only reported by 10 (11%) cases in weeks 5 and 6.
Epidemic curve monkeypox cases per week in Belgium, by date of symptom onset and by most probable exposure setting.
All cases (N=139) were men, with a median age of 38 years (youngest 20, oldest 62 years old). The majority self-identified as gay or bisexual men (95%) (see table 1).
Sociodemographic, clinical and epidemiological characteristics of the initial 139 confirmed cases in the Belgian MPX outbreak based on routine surveillance data
Almost all cases reported skin lesions, the majority of which had anogenital lesions (78%). Eight cases (6%) were hospitalised: six to control pain, one because home isolation was not possible and one for unknown reasons.
Eight cases (aged between 29 and 62 years old) self-reported a history of smallpox vaccination. The HIV status was known for 124 patients, among whom 40 were HIV positive.
Travel history was available for 131 cases, 52 (40%) of whom reported travelling outside Belgium during the presumed incubation period, which was set at 21 days prior to symptom onset. Of all notified cases, 28 (20%) reported contact with a confirmed MPX case during the presumed incubation period.
Exposure settings, interactions and conducive contexts for MPX transmission
Among the notified cases, 39 (28%) mentioned participation in a gay-oriented festival where they had sexual contact, and 2 persons (1%) reported participation in a gay-oriented festival without having had sexual contact on-site during the presumed incubation period. Mainly four different festivals were reported: a fetish festival for gbMSM in Belgium (attended by 18 cases), two Pride festivals in Spain (attended, respectively, by 12 and 4 cases) and one Pride festival in Belgium (attended by 11 cases). In addition to the routine surveillance data, we conducted semistructured interviews with a subsample of 12 MPX cases (see table 2). The narratives of these interviews (summarised through quotation excerpts in table 3) supported the potential role of gay-oriented festivals in MPX transmission, with four participants having attended at least one of these events with anonymous sexual contacts on-site (see online supplemental material 2). In addition, four other interviewees demonstrated an indirect link to these events, through sexual contact with one or more partners who recently attended these events.
Supplemental material
Sociodemographic, clinical and behavioural characteristics of interview participants
Overview of the main themes and subthemes identified in the narratives of semistructured interviews, supported by illustrative quotes
Other cruising venues for gbMSM (eg, saunas, gay bars) were reported as the most probable exposure setting by 25 (18%) notified cases. Qualitative data revealed how the anonymous nature of sexual contacts in these venues often complicated backward and forward contact tracing efforts.
Suspected modes of transmission
Sexual contact was self-reported as the most probable mode of transmission, among 83% of the notified cases (table 1). No distinction between different types of sexual contact could be made, as such more granular data were not collected through routine surveillance. Also, all but one interviewee self-perceived having acquired the infection from a sexual partner. However, only two interviewees were able to label a specific sexual encounter as the likely source of MPX acquisition. Both cases had observed a perianal pustular rash on the buttocks of a particular sex partner during penetrative anal sex. Partner notification was not possible for either as the partners were anonymous contacts. When inquiring about noticeable signs and symptoms of possible MPX infection among their sex partners, the other interviewees highlighted a number of impediments to the acquisition of this information, such as darkrooms and the cruising nature of sexual contacts (see table 3).
When comparing a more detailed history of behaviour of interviewees during the presumed incubation period with the manifestation of skin lesions, we generally observed a compatibility between reported sexual behaviour and possible inoculation sites (see online supplemental material 2). Often, multiple sex acts could be documented during the same encounter, combining penetrative oral and anal sex, interspersed with kissing contacts. In such cases, most participants reported anogenital lesions, often combined with skin lesions on other body parts where close physical contact occurred. In three cases, no anogenital lesions could be detected despite reportedly engaging in condomless anal and/or oral penetrative sex.
Four cases from the routine surveillance reported close physical contact other than during sex as the most likely transmission mode. We interviewed one of these cases, which revealed non-sexual transmission via close physical contact or fomites as a possible transmission route. This person did not report any history of sexual contact during the past few months. Yet, he reportedly hugged and kissed, and later shared bathing towels, with contacts identifying as gbMSM attending several cruising venues during a short stay at his place. One of these contacts later reported testing positive for MPX.
Health-seeking behaviour and risk perception
Routine surveillance data show a time interval between symptom onset and clinical diagnosis of up to 21 days (median of 6 days). Analysis of qualitative data provided additional insights into the reasons for diagnostic delay.
Many participants reported not recognising signs and symptoms as suspect of MPX when they first emerged, despite reportedly having heard of MPX circulating in gbMSM communities in Belgium and Europe through several media reports. Inadequate representation of the diversity of the extent and nature of skin lesions through media reports was mentioned as a reason. Skin lesions in the anogenital area were frequently linked to a possible STI, for which care was sought in primary care or specialist sexual health services. In two cases, treatment was first initiated for a presumed STI, such as a herpes simplex or secondary syphilis infection, before either patient or provider considered a possible MPX infection.
A low self-perceived MPX risk was linked to notions of MPX being a rare disease in the general population, a low number of sexual partners and consistent condom use, which constituted a perception of safe sex in relation to MPX (see table 3). In three cases, the presence of atypical symptoms (eg, a single lesion or very discrete skin lesions) caused participants to confuse lesions for other possible skin conditions, such as insect bites or eczema. The gradual appearance of additional skin lesions, or the pattern of skin lesions with general symptoms after having had sexual contact with men, ultimately urged participants to seek care that led to a clinical MPX diagnosis.
Discussion
Our findings support the role of sexual contact in the early spread of MPX during the current outbreak in Belgium. Yet, as suggested in previous reports, our surveillance data show a shift in the probable source of infection from (international) festivals and gatherings to smaller, yet also sexualised, events and cruising venues.24
This description of the initial cases in Belgium confirms other reports from European countries, indicating that MPX is predominantly spreading in sexual networks of gbMSM. Although our observations do not provide any conclusive evidence in terms of established sexual transmission routes, they support earlier raised hypotheses of MPX transmission through sexual contact. A more detailed inquiry into sexual activities through 12 semistructured interviews revealed frequent and multiple skin-to-skin and skin-to-mucosa exposures over the 3 weeks before symptom onset. These exposures present different opportunities for MPX transmission, depending on the presence of active virus in skin lesions and bodily fluids of an MPX-infected sexual partner. Recent studies have detected high viral loads in samples from skin lesions, anal swabs, saliva or oropharyngeal swabs of infected patients, and MPX DNA as well as replication-competent virus has also been detected in semen3 25–27 (own observations). Virus that is shed from these sites can be readily transmitted when it comes into contact with mucosal membranes, as during sexual contact. Previous outbreaks in Central and West Africa predominantly occurred after zoonotic spillover from the animal reservoir. Subsequent human-to-human transmission is known to occur through direct skin-to-skin contact or via the respiratory route, but transmission rates were generally found to be low with limited secondary spread.7 Sexual contact, on the other hand, might be more efficient in transmitting MPX due to the intense contact with mucosal membranes. This enhanced mode of transmission in combination with spread through dense sexual networks, therefore, may allow for sustained transmission within the population.
Although our research strongly focuses on individual behaviour, its role in MPX transmission should be understood within facilitating contexts comprised of multilevel factors. In the context of the current outbreak, our interview data provide more insight into interpersonal and community-level factors. A first finding is the interconnectedness of sexual networks among gbMSM, with linkages to a specific event (ie, international gay-oriented fetish festival) that took place in Belgium early in the epidemic.28 We described both direct (ie, sexual contact at the event) and indirect (ie, sexual contact with partners who attended the event) connections to this event. Dense sexual networks—across international boundaries—imply that the chance to encounter an MPX-infected sexual partner is higher in communities of gbMSM compared with the general population.29 Communicating this message is relevant, as we found evidence of low self-perceived MPX risk being linked to notions of low prevalence of MPX in the general population, or a low number of sexual partners, masking the elevation in risk caused by network-level factors. These processes of sensemaking were shown to impact health-seeking behaviour and prevented early diagnosis of an MPX infection in some cases. In addition, we also described factors related to the settings and interactions among gbMSM. The cruising nature of exposure settings, for instance, may facilitate anonymous interaction, with a frequent absence of contact information for contact tracing and partner notification. Lastly, interactions with the health system also emerged from our qualitative data, with primary care providers confusing MPX symptoms for other STIs. Healthcare providers—especially those attending to gbMSM—should maintain a high index of suspicion for MPX, especially among male clients presenting with anogenital skin lesions with or without general symptoms.
Our findings have several implications for effective outbreak control. First, a transparent and consistent communication on the sexual transmission of MPX is warranted, as risk communication is key to enable affected communities to take informed decisions to protect their health.30 Even though human-to-human MPX transmission could theoretically occur through any close physical contact, all epidemiological, clinical and behavioural reports indicate that non-sexual MPX transmission in the current outbreak is rare. Information campaigns should be broad, yet primarily appeal to communities of gbMSM, as they currently remain most affected by the MPX virus. The risk of stigmatisation should be carefully considered and messages should be prepared in collaboration with affected communities and all relevant stakeholders, including venue managers of locations with cruising opportunities.31 Moreover, the narratives of interviewees stress the importance of media reports, which should be inclusive towards the broad range in representations of a possible MPX infection to allow early recognition of (atypical) MPX-associated symptoms. Lastly, our data highlight the challenges of contact tracing for anonymous encounters. Therefore, there is a need for a rapid expansion of pre-exposure vaccine accessibility globally and innovative approaches for anonymous partner notification, for instance, through functional additions to the messaging systems of online dating apps, which many users would be in favour of.32
There are several limitations to our study. Sensitive information on sexual behaviour might not always be reliably disclosed to public health agencies. We have countered this effect to some extent through conducting interviews with a subsample, by an experienced qualitative researcher skilled in creating a safe and non-judgemental environment. However, social desirability bias cannot be fully excluded. Second, four persons reported only heterosexual contact during the 21-day period before symptom onset, yet no further information could be obtained from these persons to reliably assess the most probable mode of transmission. Lastly, hypotheses inspired by these qualitative data need confirmation through larger quantitative follow-up studies.
Conclusion
In-depth behavioural data from this study highlight the role of sexual contact and sexual networks in the transmission of MPX during the early phase of the outbreak in Belgium. Risk communication should consistently and transparently state the predominant sexual transmission potential of MPX. Prevention and control measures must be adapted to reflect the multilevel factors impacting on MPX transmission, including supporting anonymous partner notification and attention for atypical clinical presentations.
Abstract translation
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.Data availability statement
Data are available upon reasonable request. All relevant data supporting our findings are included in this published article. The complete dataset of conducted interviews is not made publicly available because they might contain information that could identify other persons, yet additional anonymised data are available from the corresponding author on reasonable request.
Ethics statements
Patient consent for publication
Ethics approval
The planning, conduct and reporting of this study were in line with the Declaration of Helsinki, as revised in 2013. Monkeypox is a notifiable disease in Belgium. The Belgian Institute for Health (Sciensano), in cooperation with the Belgian regional health authorities, has legal permission to process patient information for both routine and outbreak surveillance without patients’ explicit consent. The conduct of semistructured interviews was done as part of the routine outbreak investigation activities of the Institute of Tropical Medicine (ITM) in Antwerp, Belgium, and approved by the Institutional Review Board of the ITM (ref. 1596/22). All interview participants provided verbal informed consent.
Acknowledgments
We would like to thank all interviewed participants for their time, cooperation and efforts. IB and LL are members of the Institute of Tropical Medicine’s Outbreak Research Team, which is financially supported by the Department of Economy, Science, and Innovation of the Flemish government. VL is a fellow of the European Centre for Disease Prevention and Control (ECDC) Fellowship Programme, supported financially by the ECDC.
References
Supplementary materials
Supplementary Data
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Footnotes
JV and VL are joint first authors.
Handling editor Anna Maria Geretti
Twitter @JefVanhamel, @VLaisnez, @rommah
JV and VL contributed equally.
Contributors JV, VL, LL, IB, KV, AL, WVB and BV contributed to the conceptualisation of the study. LL, IB, NB-R, TV, CK and KV were involved in clinical management of the cases. JV, ML and BV designed the interview questionnaire. JV conducted the 12 interviews. NH, OL and RM interviewed cases as part of regional public health authorities. VL, AL and WVB analysed the routine surveillance data. JV and VL prepared the first draft of the manuscript. All authors were involved in the interpretation of the data and in writing and reviewing the final version of the manuscript. All authors approved of the final version. BV is the guarantor for this manuscript.
Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Disclaimer The views and opinions expressed herein do not state or reflect those of the ECDC. The ECDC is not responsible for the data and information collation and analysis and cannot be held liable for conclusions or opinions drawn.
Competing interests None declared.
Provenance and peer review Not commissioned; externally peer reviewed.
Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.