The rapidly evolving coronavirus disease 2019 (COVID-19) pandemic caused by SARS-COV-2 continues to pose unprecedented challenges to global medical communities and it has changed the way medicine is practiced globally. Due to its alarmingly high transmission rate, even among asymptomatic patients [1,2], it is essential for healthcare personnel to be extremely cautious during all patient interactions, especially when aerosol-generating procedures (AGPs) are performed.

COVID-19 can manifest with various gastrointestinal symptoms; therefore, gastroenterologists are particularly at risk of inadvertent exposure [3-5]. All endoscopic procedures should be considered AGPs, and the relevant precautions should be enforced [6-11]. Gastrointestinal societies have published recommendations on personal protective equipment (PPE) and case selection for safe endoscopy during the COVID-19 pandemic [7,8,12-15].

Like other medical societies, the Thai Association for Gastrointestinal Endoscopy (TAGE) strives to provide a safe platform for its members–endoscopists, endoscopy nurses, technical assistants, and all other endoscopy personnel–to deliver safe and effective patient care. TAGE recently published its recommendations on endoscopic practice during the COVID-19 pandemic, focusing on the required PPE, case selection, and scope cleaning process [13].

However, there are discrepancies in resource supply and institutional capability, which questions whether such recommendations can be implemented in real-world practice. This study aimed to evaluate the practicality of the gastrointestinal society recommendations, as perceived by endoscopy unit staff, using a questionnaire-based survey. The secondary aim was to assess the perceptions of safety related to endoscopic procedures performed during the COVID-19 pandemic among endoscopy personnel.

An international survey was conducted. A web-based online questionnaire consisting of 24 questions was developed to evaluate the perceptions of endoscopy personnel on the TAGE recommendations during the COVID-19 pandemic. The content of the survey was validated by a panel of experts (Supplementary Material 1). The population of interest included endoscopists (gastroenterologists and surgeons), endoscopy nurses, and technical assistants. All participants had to sign a written consent electronically for the survey. The study was approved by the Institutional Review Board of Chulalongkorn University.

The survey was sent to all board-certified physician endoscopists, registered endoscopy nurses, and fellows-in-training according to the TAGE National Membership Office database. In addition, the TAGE recommendations were published on social media platforms (Fig. 1). The survey was sent to Facebook^® (Facebook, Inc., Menlo Park, CA, USA) users who shared the recommendations and were identified as endoscopy staff according to their public profile. Relevant credentials and demographic data such as job position, level of training, level of care provided at the employing institution, working experience, and volume of endoscopy cases were included in the questionnaire and systematically analyzed.

TAGE recommended (a) PPEs based on patient risk stratification and (b) prioritizing endoscopic procedures as emergent, urgent, and elective for case selection, which were consistent with recommendations from the Asian-Pacific Society of Digestive Endoscopy, Society of American Gastrointestinal and Endoscopic Surgeons, and Center of Disease Control on COVID-19 statements (Fig. 1) [7,16]. To minimize inadvertent droplets or aerosol splash from channel irrigation, TAGE recommended three additional steps during the pre-cleaning process, as shown in Fig. 1 [17].

Personal demographics and work-related data from the survey respondents were collected. All responses were anonymous. The questionnaire focused on three main aspects of the recommendations: (1) PPE during endoscopy, (2) case selection to be performed during the pandemic, and (3) scope cleaning process (Supplementary Material 1). The level of agreement, perceived practicality, and ability to implement each recommendation were assessed using a Likert scale ranging from 1 to 5.

The web link of the questionnaire was distributed via email, Line^® (Line Corporation, Tokyo, Japan), and Facebook^® messenger applications. Two reminders were sent to all recipients at weekly intervals to increase the response rate.

Respondents would be considered from a low prevalent country if there were only “sporadic cases” according to the WHO categorization or a “cluster of cases” that did not exceed 10,000 accumulated cases per million population. High prevalence countries were defined as those with “community spread” or >10,000 accumulated cases per million population [18].

Univariate and bivariate analyses were also performed. Descriptive statistics were used to present continuous, ordinal, and categorical data. Mann-Whitney U and Kruskal Wallis tests were used for Likert-scale ordinal data, while chi-squared and Fisher’s exact tests were used for categorical data. Ordinal logistic regression analysis was performed to identify the relationships among the variables. If there was a statistically significant difference between the analyzed groups, a posthoc analysis was performed using the Mann-Whitney U test. All statistical analyses were performed using SPSS Statistics for Windows, Version 22.0 (IBM Corp., Armonk, NY, USA).

The survey was distributed to all 339 TAGE members, 488 members of the Endoscopy Nurse Society of Thailand (ENST), and 71 gastroenterology fellows-in-training in Thailand. A total of 927 Facebook^® users who shared published TAGE recommendations were screened. The survey was sent to 392 users who were found to be healthcare personnel in endoscopy units outside Thailand.

Of the 1290 surveys sent, 330 endoscopic personnel from 15 countries responded, accounting for a response rate of 25.6%. Using 1290 as the targeted population frame with a 95% confidence interval for Cochrane’s sample size formula, the corresponding correction formula yielded a 4.66% margin of error [19]. The demographic data of respondents are described in Table 1.

When asked about PPE recommendations for endoscopy (Fig. 1), 94.5% (312/330) agreed with the TAGE recommendations. In contrast with an overwhelming agreement, the practicality and applicability of the recommendations were lower (χ²=40.2; p=0.001 and χ²=25.8; p=0.047, respectively). Only 59.4% of the respondents believed that their endoscopy units were capable of adopting the TAGE recommendations, and 15.1% reported encountering some degree of difficulty in implementing them (Fig. 2). Ordinal regression analysis showed that a higher number of COVID-19 patients being treated in the hospital was associated with a higher agreement with the PPE recommendations (Wald χ² (1)=5.81; p=0.016). PPE shortage and lack of administrative support were ranked as the top two main obstacles to implementing the recommendations (52% and 31%, respectively). To overcome the PPE shortage problem, most endoscopic personnel found the “doit-yourself” PPE and reusing the equipment to be the most beneficial (36.7% and 23.9%).

Regarding the case selection, 95.5% (n=315) agreed with the TAGE recommendations; however, only 70.9% and 67.3% of the respondents stated that the recommendations were practical and the implementation was easy (Fig. 2) (χ²=115.3; p<0.001 and χ²=22.6; p=0.032, respectively). Less than half (45.2%) of the respondents reported not performing elective endoscopy during the study period. The top two reasons for non-compliance were “physician preference” and inability to reschedule”.

Less than half of the respondents (46.1%) felt “moderately safe” working in an endoscopy unit during the COVID-19 pandemic period whereas 21.5% felt a “little safe” or “not safe at all” or unsafe. The main reason for “unsafe” working conditions (80%) was inadequate PPE provided to the endoscopy personnel.

The sense of safety of the respondents in the endoscopy unit significantly differed during the pandemic with age (χ²=15.3; p=0.004) and the level of experience of the endoscopy personnel (χ²=17.6; p=0.001) (Fig. 3). After adjusting for age, multivariate ordinal regression analysis showed that greater experience was associated with better perceptions of safety (Wald χ² (1) =13.7; p=0.008). In the subgroup analysis of trainee responses (n=32), there was no statistically significant difference in agreement, perceived practicality, or applicability of the recommendations. However, the trainees reported feeling less safe, compared with the attending physicians (n=246) (U=3,778; p=0.04), as shown in Figure 3.

Looking at the various professional roles of the respondents, there were no statistically significant differences between the responses of the endoscopists (n=278) and the endoscopy nurses (n=44) related to their agreement with and the perceived practicality of the recommendations on PPE and case selection (U=5,226; p=0.065 and U=5,998; p=0.83 and U=5,599; p=0.305 and U=5,911; p=0.70, respectively). Physician endoscopists had more difficulty implementing PPE recommendations than endoscopy nurses (17% vs. 4.6%, U=4,732; p=0.011). There was no statistically significant difference in safety perception by the physicians and endoscopy nurses (U=4,026; p=0.43). When asked about scope cleaning protocols during the COVID-19 pandemic, the endoscopists were more likely to respond as “I do not know” than the endoscopy nurses (U=4,276; p=0.001).

Although there were no differences in the agreement with and perceived practicality and applicability of the recommendations among the different levels of hospitals, respondents from private hospitals were more likely to perceive the recommendations for case selection to be less practical than those from governmental hospitals (U=6,478; p=0.015). After adjusting for hospital size, ordinal regression analysis showed that the odds of respondents in private practices considering recommendations on case selection to be non-practical was 7.4 (95% confidence interval, 2.8-4.9) times that of those from non-private practices (Wald χ² (1)=6.17; p=0.013), as shown in Fig. 4. The number of endoscopic procedures performed in COVID-19 patients was associated with the agreement with the case selection recommendations (χ²=15.1; p=0.002).

Respondents from countries with a high prevalence of COVID-19 (n=150) had significantly less agreement with the PPE recommendations (U=11,570; p=0.008) and were less likely to perceive the recommendations to be practical or easily applicable, compared to low prevalent countries (n=180) (U=10,444; p<0.001 and U=8,585, p<0.001, respectively). Similarly, it was also more difficult to implement the recommendations on case selection and scope reprocessing in highly prevalent countries (U=9,992; p<0.001 and U=10,320, p<0.001, respectively). They also felt less safe working in endoscopy units (U=11,062; p=0.003). The associations between each parameter and the agreement with and the practicality and applicability of the recommendations are summarized in Tables 2 and 3.

As COVID-19 continues to ravage the world, endoscopy units are now adapting to the “new normal” of medical practice. Our study has demonstrated that although the recommendations of gastrointestinal societies are generally accepted, their practicality and applicability are still questioned, especially in resource-limited and/or highly prevalent areas. Coverall suit, N95 masks, and leg covers were reported as the most deficient equipment, with 37% of the respondents stating that do-it-yourself equipment and reusing the mask were the most helpful in overcoming the PPE shortage problem [20-24]. At the time of this study, there has been no study validating the efficacy of one reuse method over another. Studies investigating the most cost-effective methods for reusing such equipment are needed for resource-limited medical communities.

Even though the majority of the respondents reported being able to implement the recommendations, almost half (46%) responded neutrally to a question on safety while working in an endoscopy unit. The sense of safety did not differ with gender, professional role, institutional level, number of COVID-19 cases in the hospital, or case load of endoscopic procedures for COVID-19 patients; it differed with age, working experience, training status, and the prevalence of COVID-19 in the country. Despite the higher mortality risk associated with COVID-19 infections [25], respondents in the older age groups still felt safer working during the pandemic. These results demonstrate that the imperturbability of seasoned endoscopists and nurses comes with experience. They also support the TAGE recommendation of assigning more experienced endoscopists to perform endoscopy for patients with COVID-19.

The lower sense of safety of the trainees, compared with their attending counterparts, is a critical observation that should be urgently addressed. Trainees, in spite of their limited experience, constitute a fundamental workforce in the hospital and may inevitably be allocated to the frontline amidst overwhelming medical demand. As opposed to attending physicians, trainees are more vulnerable to coercion and generally receive less training for mass-casualty events [26,27]. Therefore, operational management should involve fellows in the development of emergency plans to strike a balance between high-quality patient care and the personal safety of trainees [28]. It is also important to note that despite the high prevalence of COVID-19 in the countries of the respondents, only 26.3% had performed endoscopy in COVID-19 patients. This finding suggests that emergent endoscopy among these patients is not common.

The TAGE recommendation to postpone all elective cases has an inevitable economic impact on endoscopic practices. The significant disagreement on its practicality among respondents in private practice and governmental counterparts underscored the financial implications of these recommendations. Although there are no strict guidelines on when to resume general practice, the timing should be individualized according to the recommendations of local health authorities while exercising good clinical judgment.

In general, the TAGE recommendations are similar to those by other societies with only a few exceptions, as described in Table 4. Regarding scope reprocessing, although the TAGE recommendations were in agreement with those by the European Society of Gastrointestinal Endoscopy and the American Society of Gastrointestinal Endoscopy on virucidal efficacy of standard scope cleaning, TAGE experts were more concerned about accidental splashing or aerosolization during the pre-cleaning process while wiping, blowing air, flushing scope channels, or unplugging valves. As a result, an additional protocol aiming to protect reprocessing personnel was recommended; this was the use of alcohol wipes on the control knobs and the exterior of the endoscope with Peracetic acid immersion as the next step, considering its fast and broad virucidal and sporicidal activities [29]. However, the adoption of this practice was controversial due to concerns about their proteinaceous fixative properties on the endoscope surface [30]. Therefore, these additional agents should only be used for pre-cleaning steps before standard high-level disinfection.

This study benefited from a relatively large group of multinational respondents. By reaching out to those directly involved in endoscopy management during the COVID-19 pandemic and those who shared the published recommendations via social media platforms, the obtained responses were more likely to reflect the real-world adoption of the recommendations. Given that this was a large multinational survey, the differences in the demographic characteristics of the respondents were inevitable. Despite these differences, the respondents overwhelmingly agreed with nearly all aspects of the recommendations, suggesting that the perceptions of the importance of PPE, the case selection protocol, and the scope cleaning process adjustment during the COVID-19 pandemic were universal among healthcare personnel regardless of their geographical location, level of training, or available resources. However, the perceptions of the practicality and applicability of each recommendation differed with the local COVID-19 prevalence as the pivotal determining factor. Our findings emphasize that the guidelines of societies may not satisfy the “one size fits all” principle. They also demonstrate the crucial need for each endoscopy unit to adapt its practice pattern according to the local prevalence.

Our study was also subject to inherent limitations of a survey study that included recall and selection bias. Due to the international design of the study and the changing prevalence of COVID-19 in each country, the responses obtained may be subject to change over time. In addition, as further evidence on the aerosolization risk of endoscopy emerges, the official recommendations on optimal PPE and reprocessing methods for endoscopic procedures may be modified.

We conclude that using appropriate PPE and implementing optimal case selection for endoscopic practice during the COVID-19 pandemic remains a challenge, especially among less experienced endoscopists in highly prevalent countries, although the response of the respondents indicated a general agreement with the recommendations. TAGE recommendations, similar to other guidelines, should be taken only as general guidance, rather than as a compulsory standard. The personal sense of safety of endoscopy personnel is imperative in the management of an endoscopy unit during the pandemic. The optimal response to such an unprecedented public health crisis necessitates knowledge, preparedness, and multidisciplinary coordination to ensure proper resource availability and allocation.