Best practice of gastrointestinal endoscopy during Mpox upsurge: an Indonesian Society for Digestive Endoscopy recommendation
Article information
, Ahmad Fariz Malvi Zamzam Zein,2,*, Raisa Wibowo1, Achmad Fauzi1, Abdul Aziz Rani1, Marcellus Simadibrata1, Dadang Makmun1, Murdani Abdullah1, Ari Fahrial Syam1, Muhammad Miftahussurur3, Agasjtya Wisjnu Wardhana4, Amanda Pitarini Utari1, Andi Muhammad Luthfi Parewangi5, Arles Arles6, Arnelis Arnelis7, Bradley Jimmy Waleleng8, Bogi Pratomo Wibowo9, Fauzi Yusuf10, Hasan Maulahela1, Hery Djagat Purnomo11, I Dewa Nyoman Wibawa12, Ignatia Sinta Murti13, Indra Marki14, Kaka Renaldi1, Masrul Lubis15, Muhammad Begawan Bestari16, Muhammad Firhat Idrus1, Pieter Saragih17, Putut Bayupurnama18, Ruswhandi Ruswhandi19, Saskia Aziza Nursyirwan1, Suyata Suyata20, Titong Sugihartono3, Triyanta Yuli Pramana21, Virly Nanda Muzellina1, Yustar Mulyadi22, on behalf of the Indonesian Society for Digestive EndoscopyAbstract
The emergence of Mpox as a significant zoonotic viral threat presents new challenges in gastrointestinal endoscopy. This article outlines the risk of Mpox transmission during gastrointestinal endoscopy, particularly through respiratory droplets and contact with the mucosal surfaces. Gastrointestinal endoscopy may also facilitate transmission by fomites, as the Mpox virus can persist on medical instruments and surfaces for long periods. Nosocomial Mpox transmission is a significant concern in both endemic and non-endemic regions. This highlights the necessity for enhanced infection control measures in gastrointestinal endoscopy, including pre-endoscopic assessment, proper use of personal protective equipment, and rigorous post-procedural disinfection. Additionally, vaccination of healthcare workers frequently exposed to high-risk situations is emphasized. Ongoing surveillance and monitoring of healthcare workers are key components in minimizing the transmission risk. Although no direct cases of Mpox transmission via gastrointestinal endoscopy have been reported, these recommendations mitigate the potential risks associated with such procedures and necessitate strict adherence to infection control protocols. By adhering to these protocols and adapting to current practices, gastrointestinal endoscopy can be safely performed during the Mpox upsurge, ensuring the protection of both patients and healthcare workers.
INTRODUCTION
Gastrointestinal endoscopy (GIE) is an essential diagnostic and therapeutic procedure for the treatment of various gastrointestinal, liver, and pancreatobiliary diseases. However, the recent upsurge in Mpox poses significant challenges to healthcare workers (HCWs) who perform these procedures, owing to the risk of transmission via mucosal surfaces and respiratory droplets. The Indonesian Society for Digestive Endoscopy (ISDE) recognizes the need for updated protocols to enhance safety during GIE during the Mpox upsurge.
Mpox is caused by the monkeypox virus (MPXV), a member of the Orthopoxvirus genus, and is a zoonotic disease primarily transmitted through close contact with skin lesions, respiratory droplets, and contaminated objects.1 The number of reported cases from 123 countries reached 106,310 patients by August 31, 2024.2 On August 14, 2024, the World Health Organization declared Mpox as a public health emergency of international concern. The Ministry of Health, Republic of Indonesia, reported 88 confirmed cases in Indonesia as of August 31, 2024.
Gastroenterologists are exceptionally prone to Mpox infection owing to close exposure to the mucosal surfaces of the oral cavity, larynx, pharynx, and GI tract during GIEs. Given that GIE is classified as an aerosol-generating procedure (AGP),3 transmission risks are further heightened. This paper outlines the ISDE recommendations for safe GIE practices during the Mpox upsurge.
ADDRESSING THE RISK IN GASTROINTESTINAL ENDOSCOPY
There are direct routes of human-to-human transmission of Mpox, such as percutaneous, mucosal, and respiratory exposure. Percutaneous exposure facilitates close-contact transmission, including skin-to-skin contact, particularly in broken skin. Mucosal exposure enables direct exposure of the mucous membranes, including the mouth, vagina, and rectum. Respiratory exposure occurs via respiratory droplets produced by sneezing, coughing, and other similar actions. Indirect routes of human-to-human transmission may result from contaminated items, such as patient-used garments or linens, and household sharing. Furthermore, nosocomial Mpox transmission remains a major issue in both endemic and non-endemic countries.4-6
To date, no report has identified Mpox cases with GIE transmission, and the risk of exposure during GIE is unknown, although HCWs performing GIE carry potential risks of Mpox transmission. The potential risk of Mpox transmission involves direct contact with lesions, aerosol droplets, or contaminated equipment (endoscopes and accessories) during GIE. Moreover, GIE may facilitate transmission by fomites, including countertops, computer keyboards, and screens, as MPXV can persist on contaminated medical instruments and surfaces for extended periods.7 Some professional societies have classified both the upper and lower GIE as AGP, considering them at least an uncertain risk. The transmission of MPXV through aerosolization of respiratory secretions during GIE is a pivotal concern for HCWs in endoscopy units. Hence, GIE poses a considerable risk in the era of the Mpox upsurge.8
A mitigation strategy for GIE during the Mpox upsurge is provided to enhance the principle of patient-HCW safety. It encompasses pivotal aspects of GIE, including pre-endoscopic assessment, risk stratification, infection control and prevention in endoscopy units, and post-endoscopic control. Amidst limited studies investigating GIE during the Mpox upsurge, preparedness for performing GIE in both endemic and non-endemic countries is ultimate.
PRE-ENDOSCOPIC ASSESSMENT
To mitigate the risk of Mpox transmission, a thorough pre-endoscopic assessment is essential. All the patients are screened for Mpox symptoms and exposure history before undergoing GIE. It helps identify at-risk individuals and ensures that appropriate precautions are taken to protect patients and HCWs.1
The pre-endoscopic assessment includes a complete travel history documentation of 21 days prior to GIE, considering the Mpox incubation period. Close contacts and potential exposure to confirmed or suspected Mpox cases are thoroughly investigated by recording skin-to-skin contact, sharing of personal items, and living in the same household. Screening for common symptoms such as fever, headache, lymphadenopathy, and malaise is mandatory, with special emphasis on the presentation of new-onset rash or lesions, particularly in the genital and perianal areas.9 However, some patients present with atypical symptoms, including mucosal involvement presenting with non-specific features that resemble other conditions. Oropharyngeal manifestations include oral or tonsillar ulcers, epiglottitis, and pharyngitis, which may cause odynophagia and dysphagia. Mucosal involvement in the anorectal region leads to ulcerations or proctitis, resulting in pain, bleeding, tenesmus, or diarrhea. Although less common, conjunctival mucosal involvement also occurs, potentially causing keratitis and vision loss.10,11
Suspected cases should undergo a clinical examination consisting of a skin examination, focusing on areas where rashes or lesions are commonly found (e.g., face, hands, feet, and genital areas), lymph node assessment, and palpation of swollen lymph nodes located in the cervical, axillary, and inguinal regions. Subsequent laboratory testing is ordered if deemed necessary.9 Viral polymerase chain reaction (PCR) testing is indicated if the patient presents with a suspicious rash or a history of exposure (Fig. 1).1
Patient assessment protocol before gastrointestinal endoscopy in suspected Mpox cases.
RISK STRATIFICATION OF GIE
GIE is commonly classified as urgent, semi-urgent, or elective. However, for practical purposes, we propose classifying these procedures as urgent or elective, without adding semi-urgent GIE. Table 1 provides an overview of GIE procedures that distinguish between the two categories. Urgent GIE is a life-saving procedure for gastrointestinal emergencies such as hemostatic endoscopy for upper and lower gastrointestinal bleeding, endoscopic retrograde cholangiopancreatography for acute cholangitis, foreign body extraction, and endoscopic nutritional access placement. Elective GIE includes endoscopic mucosal resection, endoscopic submucosal dissection, diagnostic esophagogastroduodenoscopy, colonoscopy, enteroscopy, and endoscopic ultrasound.12
List of indications for urgent and elective endoscopy
A complete pre-endoscopic assessment provides data on patient risk stratification and the nature of GIE urgency, which will subsequently determine patient management. Risk stratification divides patients into three categories: high, moderate, and low risk. The high-risk group includes patients with confirmed exposure, typical Mpox-related symptoms, and a positive PCR test for Mpox. A moderate-risk group is defined as patients with a history of exposure but no typical or atypical Mpox-related symptoms. The low-risk group is defined as patients with neither the investigated exposure nor symptoms. The risk stratifications outlined above are shown in Table 2.
Risk stratification categories for pre-endoscopic assessment
Therefore, it is important to select patients based on risk stratification. Neither elective nor urgent GIEs are restricted to low-risk patients with standard precautions. Postponing elective GIEs should be considered in moderate-risk patients until a definitive diagnosis is made. A proper course of action for high-risk patients would defer elective GIEs and initiate isolation and standard treatment for Mpox. Urgent GIEs should be implemented in both high- and moderate-risk patients. It must be performed with proper standards of infection prevention measures and appropriate personal protective equipment (PPE).8 PPE plays a vital role in minimizing exposure during procedures. It is recommended that HCWs wear full PPE, including N95 respirators, face shields, eye protectors, gowns, and gloves. This comprehensive gear protects against respiratory droplets and potential contact with contaminated surfaces, thereby reducing the risk of transmission (Fig. 2).
Healthcare worker equipped with full personal protective equipment, wearing disposable gown, N95 respirator, goggles, gloves, and surgical cap.
Elective GIEs in patients at high and moderate risk should be managed using a comprehensive and safe approach. Elective GIEs should be postponed until the patient is no longer infectious, typically after all lesions have crusted over or fallen off, or a fresh layer of skin has formed. For low-risk patients, planned GIEs may continue, and adherence to standard infection prevention measures should be ensured.9
Urgent GIEs among moderate- and high-risk Mpox patients should be performed with proper standards of infection control and prevention measures. The prerequisites are an endoscopy room, appropriate PPE, and limited number of personnel.3 The endoscopy suite must be equipped with high-efficiency particulate air (HEPA) filtration systems and maintained with good ventilation to lower airborne particle concentration. Whenever possible, single-use disposable accessories can further reduce the risk of contamination. Limiting the number of individuals present during GIE is another effective measure. Reducing personnel to only those essential for GIE limits the potential exposure of additional staff to the virus.1 The flowchart in Figure 3 provides a simplified representation of the risk stratification process and GIE indications, guiding the decision-making for elective or urgent procedures based on patient risk levels.
Algorithm of decision making in performing gastrointestinal endoscopy (GIE) during Mpox upsurge.
Categorization of GIE as an AGP, requires some concerns to be addressed. The risk of aerosol generation in the upper GIE can be significantly reduced by avoiding or identifying alternatives to throat sprays. Further studies have shown that performing trans-nasal endoscopy may reduce aerosol generation. Some events contribute to aerosol generation during lower GIE, including rectal extubation and intubation, and application of abdominal pressure.13
INFECTION CONTROL AND PREVENTION IN ENDOSCOPY UNIT
Training and education are fundamental for HCWs who perform GIE. They must be regularly updated on Mpox transmission and infection control practices. Keeping the team informed of the latest guidelines and safety protocols ensures that all staff members understand the risks and necessary precautions to prevent transmission. Comprehensive implementation of these measures can significantly reduce the risk of Mpox transmission during GIE, ensuring a safer environment for both patients and HCWs.1
Environmental control measures include equipping endoscopy suites with HEPA filters, maintaining adequate ventilation, disinfecting all surfaces using hospital-approved disinfectants, and limiting personnel in the procedure room to merely essential staff. During endoscopic procedures, all surfaces that come into contact with patients must be disinfected using hospital-approved disinfectants such as bleach or hydrogen peroxide-based products with antiviral activity. Submerging endoscopes and other reusable instruments in 0.02% glutaraldehyde for 10 minutes has been proven to be effective in inactivating Mpox.14 Additionally, soiled laundry should be handled gently to avoid disturbing any infectious particles, and medical waste can be managed following standard protocols. While standard cleaning and disinfection of endoscopes remains effective, there is a potential risk of aerosolization during the process, necessitating strict safety measures to protect staff from Mpox infection.
Meister et al.15 recommended the wet cleaning of rooms to prevent the resuspension of viral particles, which reduces the risk of airborne transmission. Rigorous cleaning of the room and equipment with alcohol- or aldehyde-based disinfectants following each procedure are necessary. Once disinfectants impair the lipid envelope, the virus loses its ability to infect. Alcohol- and aldehyde-based disinfectants are particularly effective in inactivating Mpox on stainless steel. Disinfection of surfaces contaminated with Mpox with 75% ethanol for at least 1 minute reduces Mpox titers by 4.25 log10.15,16
The risk of spreading is heightened by the use of contaminated instruments or surfaces, underscoring the importance of rigorous decontamination practices. Furthermore, fomite transmission is a significant concern because the virus can persist on contaminated medical instruments and surfaces for extended periods. Thorough sterilization of all equipment and environmental surfaces after each procedure is crucial.14
POST-ENDOSCOPIC PROTOCOLS
The exposure risk level among HCWs involved in GIE should be evaluated based on Center for Disease Control and Prevention (CDC) risk assessment for MPXV exposure in healthcare settings. The assessment covers the level of protection against contact exposure with skin lesions, bodily fluids, contaminated materials, dried lesion exudates, or crusts, and the correct and consistent use of PPE. Furthermore, HCWs frequently exposed to high-risk situations for Mpox transmission in their clinical duties are advised to receive a pre-exposure vaccination prior to initiating any procedures. The JYNNEOS vaccine, made from the strain Modified Vaccinia Ankara-Bavarian Nordic (MVA-BN), is recommended by both the United Kingdom Health Security Agency and the United States Food and Drug Administration for individuals aged 18 and above, with two doses administered 4 weeks apart.10 The vaccine can be administered either subcutaneously at a dose of 0.5 mL or intradermally at a dose of 0.1 mL.9 This two-dose regimen induces immunogenicity, generating antibody levels considered protective against smallpox, and by inference, against Mpox as well.10
In Indonesia, the MVA-BN vaccine, provided by the Ministry of Health, is recommended primarily for high-risk groups, including men who have sex with men, individuals with multiple sexual partners, those recently in contact with confirmed Mpox cases, and HCWs or lab personnel directly handling Mpox cases.17 However, this vaccine is intended only to prevent the development of symptoms or lessen the severity of the illness. Thus, growing concerns exist regarding HCWs performing AGPs, such as GIE, who may also be at an increased risk of Mpox exposure due to the potential for airborne transmission.
Recent studies have identified the presence of Mpox virus DNA in aerosols and droplets, highlighting the potential for respiratory transmission in healthcare settings, even when patients wear masks. Although viable viruses are not recovered from aerosol samples in all cases, the detection of viral DNA in 64% of air samples raises concerns about the risk of airborne spread in confined spaces, especially during AGPs.18 While HCWs equipped with full PPE engaged in these procedures are not traditionally classified as high-risk, the nature of endoscopic procedures, involving contact with oral or respiratory secretions, raises the possibility of transmission through contaminated surfaces or aerosols. The CDC underscores the importance of proper PPE use in reducing transmission risk. However, improper PPE use or removal can significantly increase vulnerability. Given the heightened exposure risk in such clinical settings, we recommend extending the Mpox vaccination to HCWs performing AGPs as a preventive measure, in addition to ensuring strict adherence to PPE protocols.7
The Mpox vaccine can be administered as post-exposure prophylaxis (PEP) to individuals with confirmed or presumed exposure to the Mpox virus. As with PEP, the vaccine should ideally be administered within four days of exposure. However, vaccination between 4 and 14 days post-exposure may still offer some protective benefit.19 After 14 days of exposure, HCWs should weigh the benefits of vaccination against potential risks, particularly in cases of immunosuppression or previous allergic reactions. Individuals with an ongoing risk of Mpox exposure should be offered vaccination regardless of prior exposure or the time elapsed since exposure, provided they do not develop symptoms. Vaccination after the onset of symptoms, following an Mpox diagnosis, or after recovery from the disease is unlikely to provide any benefit.
Monitoring of HCW should continue through integrated surveillance. Passive approaches might include educating and requesting HCW to self-report signs or symptoms of disease to occupational health,20 while active approaches might include telephone and video calls to HCW for symptom and temperature check-ins, or in-person presentations to occupational health for regular assessments. In general, the type of monitoring employed often reflects the risk of transmission, with more active monitoring approaches used for higher risk of exposures, including check-ins on tolerability and adherence to PEP. Self-monitoring approaches are usually sufficient for exposure, with a lower risk of transmission. Even higher risk of exposures may be appropriate for a self-monitoring strategy if occupational health services or public health authorities determine that it is appropriate. Ultimately, the person’s exposure risk level, reliability in reporting symptoms that might develop, number of persons needing monitoring, time since exposure, receipt of PEP, and available resources are factors that determine the type of monitoring used.21
CONCLUSIONS
Ensuring the safety of both HCWs and patients during GIE amidst the ongoing Mpox upsurge requires a multi-faceted approach. This includes a comprehensive pre-endoscopic assessment, risk-based stratification, strict infection control protocols, and post-procedural monitoring. Additionally, the vaccination of at-risk HCWs and adherence to the latest Mpox guidelines are critical. When applied consistently, these measures significantly reduce the risk of Mpox transmission, safeguarding both the HCWs and patients during critical GIE.
Notes
Conflicts of Interest
The authors have no potential conflicts of interest.
Funding
None.
Author Contributions
Conceptualization: RRP, AFMZZ, RW, AF; Investigation: all authors; Supervision: all authors; Project administration: RRP, AFMZZ, RW; Resources: RRP, AFMZZ, RW; Writing–original draft: RRP, AFMZZ, RW; Writing–review & editing: all authors.