Longitudinal mpox virus surface sampling in an outpatient setting

We read with interest the report from Mellon et al. regarding air sampling for mpox (formerly monkeypox) virus (MPXV) in an outpatient setting and the need for additional data to assess the risk to healthcare workers (HCWs) [[1]Mellon G. Rubenstein E. Antoine M. Ferré V.M. Gabassi A. Molina J.-M. et al.Air detection of monkeypox virus in a dedicated outpatient clinic room for monkeypox infection diagnosis.J Infect. 2022; (22)00750-2: S0163-S4453Google Scholar]. In August 2022, we performed longitudinal surface sampling at a large sexual health clinic in London, UK, to investigate environmental contamination of a typical outpatient setting where patients with mpox are assessed. During the four-week period of observation at the clinic, 85 patients were seen and subsequently diagnosed with mpox based on samples collected during their visit (number of patients confirmed positive seen in 7 days' prior sampling: week 1: 31 cases; week 2: 26 cases; week 3: 22 cases; week 4: 6 cases). Weekly sampling was performed in the same observation room using Copan UTM swabs (Copan, Brescia, Italy) with quantitative polymerase chain reaction (qPCR) analysis performed as previously described [[2]Gould S. Atkinson B. Onianwa O. Spencer A. Furneaux J. Grieves J. et al.Air and surface sampling for monkeypox virus in a UK hospital: an observational study.Lancet Microbe. 2022; 3: e904-e911Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar]. Samples were collected from the same eight locations each week: HCW desk, HCW keyboard, patient chair armrest, floor beneath patient chair, desk between patient and HCW, wall next to examination table (approximately where the patient head will be facing during examination), floor beneath examination table, and the door handle to exit the examination room. qPCR analysis of the 32 samples collected (eight samples collected weekly for four weeks) resulted in only three MPXV-positive samples all with crossing threshold (CT) values near the limit of detection for the assay, indicating occasional low-level contamination of the sampled environment. All three positive samples were collected from the floor of the examination room (Figure 1); viral isolation using previously described methods detected replicating virus in one sample collected from the floor beneath the examination table (week 2), confirming the presence of infection-competent MPXV in this sample [[2]Gould S. Atkinson B. Onianwa O. Spencer A. Furneaux J. Grieves J. et al.Air and surface sampling for monkeypox virus in a UK hospital: an observational study.Lancet Microbe. 2022; 3: e904-e911Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar]. Two of the three positive samples were identified in the same location on consecutive weeks, raising the possibility of duplicate identification. Though our data cannot exclude this possibility, surfaces were thoroughly cleaned using disinfectant wipes (Spill Wipes, Clinell; GAMA Healthcare, Hemel Hempstead, UK) and the floor cleaned with chlorine solution (Chlor-clean; Guest Medical, Edenbridge, UK) after each examination of a suspected mpox case, in addition to routine cleaning performed at the end of every working day. Despite a significant potential for mpox transmission in healthcare settings, few cases of mpox have been reported in HCWs, with just five cases recorded by the World Health Organization as occupational exposures in Europe through January 2023 [[3]World Health Organization/European Centre for Disease Prevention and ControlJoint ECDC–WHO Regional Office for Europe Mpox Surveillance Bulletin: 4. January 2023; (Available at:) ([last accessed January 2023])https://www.who.int/europe/publications/m/item/joint-ecdc-who-regional-office-for-europe-mpox-surveillance-bulletin–04-january-2023Google Scholar]. Infection prevention and control (IPC) measures including the use of personal protective equipment (PPE) may explain, in part, the very small number of occupationally associated infections reported. The PPE recommended for typical UK outpatient consultations (gloves, fluid-repellent surgical mask, apron, and eye protection if splash risk) is simpler than the recommended PPE for UK HCWs caring for patients with mpox admitted to hospital (gloves, fit-tested FFP3 respirator, long-sleeved fluid-repellent gown, eye protection) [[4]UK Health Security Agency. Principles for mpox control in the UK: 4 nations consensus statement. 2022. Available at: https://www.gov.uk/government/publications/principles-for-monkeypox-control-in-the-uk-4-nations-consensus-statement/principles-for-monkeypox-control-in-the-uk-4-nations-consensus-statement [last accessed January 2023].Google Scholar]. However, the amount of environmental contamination and opportunities for exposure to virus are expected to be greater and more cumulative for inpatient settings compared to outpatient settings [[1]Mellon G. Rubenstein E. Antoine M. Ferré V.M. Gabassi A. Molina J.-M. et al.Air detection of monkeypox virus in a dedicated outpatient clinic room for monkeypox infection diagnosis.J Infect. 2022; (22)00750-2: S0163-S4453Google Scholar,[2]Gould S. Atkinson B. Onianwa O. Spencer A. Furneaux J. Grieves J. et al.Air and surface sampling for monkeypox virus in a UK hospital: an observational study.Lancet Microbe. 2022; 3: e904-e911Abstract Full Text Full Text PDF PubMed Scopus (17) Google Scholar,[5]Nörz D. Brehm T.T. Tang H.T. Grewe I. Hermanussen L. Matthews H. et al.Clinical characteristics and comparison of longitudinal qPCR results from different specimen types in a cohort of ambulatory and hospitalized patients infected with monkeypox virus.J Clin Virol. 2022; 155: 105254Crossref PubMed Scopus (17) Google Scholar,[6]Hernaez B. Muñoz-Gómez A. Sanchiz A. Orviz E. Valls-Carbo A. Sagastagoitia I. et al.Monitoring monkeypox virus in saliva and air samples in Spain: a cross-sectional study.Lancet Microbe. 2023; 4: e21-e28Abstract Full Text Full Text PDF PubMed Scopus (12) Google Scholar]. The two previous studies in outpatient settings both focused on air sampling and both studies identified positive qPCR samples, although neither identified infectious virus. Our data confirm that environmental contamination of surfaces occurs in outpatient settings and can contain infectious virus. This contamination may occur due to several mechanisms including from respiratory droplets or via dislodgement of viral particles on patient clothing which are removed for patient examination. It is likely that the contact PPE recommended in outpatient settings (in combination with frequent room cleaning) is proportionate to mitigate the risk from fomite transmission within the environment; however, the detection of MPXV in air samples from previous studies does raise concerns. At present, infectious virus has not been detected in air samples and the risk of establishing human mpox infection via the respiratory route is unknown. The absence of numerous cases in HCWs working in outpatient settings suggests that either (i) infectious virus in respiratory secretions is rarely present at sufficient titre to establish infection, (ii) respiratory transmission of Clade IIb MPXV is not an optimal route of transmission, or (iii) that surgical/FFP2 masks are sufficient to mitigate the residual risks of (i) and (ii). We have shown that surface contamination occurs in an outpatient setting and, although it was minimal in the environment sampled, infection-competent MPXV could be detected. It is likely that several factors contribute to the low level of contamination observed, including minimal time spent in this locality and the frequency of cleaning. Such focused surface deposition of virus would not be expected if there had been aerosolization of virus. Thus in future studies, and where feasible, combined surface and air sampling may provide additional insights. It is feasible that the contamination observed could present an infection risk in specific situations; however, UK PPE recommendations combined with frequent standard cleaning procedures appear sufficient to mitigate onward transmission risk in outpatient settings. IPC recommendations should be kept under review as more data emerge regarding infectious virus in respiratory secretions and the risk of respiratory transmission of MPXV. The investigations performed were a component of the urgent public health investigation performed as part of UKHSA's public health incident response to cases of a high-consequence infectious disease in the UK. UKHSA is the national health security agency for England and an executive agency of the UK Government's Department of Health and Social Care. The study protocol was subject to internal review by the Research Ethics and Governance Group, which is the UKHSA Research Ethics Committee, and was granted full approval. The authors wish to acknowledge the support of S. Summers, K. Emery, and R. Davies for assistance with cell culture. Conceptualization and methodology: B.A., S.G., T.F., A.M.B., J.D., D.A., G.W.; investigation: B.A., S.P., G.W; formal analysis: B.A., A.S., O.O., J.F., I.N., J.G.; writing – original draft: B.A., A.M.B., J.D., G.W.; writing – review and editing: all authors. This report contains work supported by UKHSA Grant-in-Aid. The contents of this paper, including any opinions and/or conclusions expressed, are those of the authors alone and do not necessarily reflect UK Health Security Agency policy. This work was funded by UKHSA Grant in Aid funding and the NIHR Health Protection Research Unit in Emerging and Zoonotic Infections. The funding source had no involvement in study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the article for publication. J.D. is supported by the Moh Foundation.