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Barriers for Resuming Endoscopy Services in Egypt during COVID-19: A Multicenter Survey, Assignments of Medicine

An original article presenting the findings of a multicenter survey conducted in Egypt to identify the barriers for resuming endoscopy services during the COVID-19 pandemic. The study highlights the current practice in Egyptian endoscopy units and discusses the challenges faced in different regions of Egypt. The survey involved contributions from various authors and departments of internal medicine, hepatology, gastroenterology, and tropical medicine from several universities in Egypt and Germany.

What you will learn

  • What percentage of endoscopy centers in Egypt have provided special rooms for confirmed or suspected COVID-19 cases?
  • How have different regions in Egypt been affected by the shortage of specialists in endoscopy units?
  • What are the main barriers for resuming endoscopy services in Egypt during the COVID-19 pandemic?

Typology: Assignments

2020/2021

Uploaded on 07/27/2021

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Name of Journal: World Journal of Gastroenterology
Manuscript NO: 60090
Manuscript Type: ORIGINAL ARTICLE
Observational Study
Barriers for resuming endoscopy service in the context of COVID-19
pandemic: A multicenter survey from Egypt
Elshaarawy O et al. Resuming endoscopy during COVID-19 pandemic
Omar Elshaarawy, Sameh Aldesoky Lashen, Nahed A Makhlouf, Doaa
Abdeltawab, Mariam Salah Zaghloul, Rasha M Ahmed, Hayam Fathy, Shimaa
Afifi, Muhammad Abdel-Gawad, Eman Abdelsameea, Sherief Abd-Elsalam,
Salem Youssef Mohamed, Mohammed Tag-Adeen, Mina Tharwat, Ahmed
Alzamzamy, Ahmed Nasr Bekhit, Alshaimaa M Eid, Abeer Awad, Mohammad
Aamr, Waleed A Abd El Dayem, Mohamed-Naguib Wifi, Mohamed Alboraie
Omar Elshaarawy, Eman Abdelsameea, Department of Hepatology,
Gastroenterology and Liver Transplantation, National Liver Institute,
Menoufia University, Shebine Elkom 32511, Egypt
Omar Elshaarawy, Department of Internal Medicine and Center of Alcohol
Research and Liver Diseases, Salem Medical Center, Heidelberg University,
Heidelberg 69121, Germany
Sameh Aldesoky Lashen, Department of Internal Medicine, Faculty of
Medicine, University of Alexandria, Alexandria 21521, Egypt
Nahed A Makhlouf, Doaa Abdeltawab, Department of Tropical Medicine
and Gastroenterology, Faculty of Medicine, Assiut University, Assiut 71515,
Egypt
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Name of Journal: World Journal of Gastroenterology Manuscript NO: 60090 Manuscript Type: ORIGINAL ARTICLE Observational Study Barriers for resuming endoscopy service in the context of COVID- pandemic: A multicenter survey from Egypt Elshaarawy O et al. Resuming endoscopy during COVID-19 pandemic Omar Elshaarawy, Sameh Aldesoky Lashen, Nahed A Makhlouf, Doaa Abdeltawab, Mariam Salah Zaghloul, Rasha M Ahmed, Hayam Fathy, Shimaa Afifi, Muhammad Abdel-Gawad, Eman Abdelsameea, Sherief Abd-Elsalam, Salem Youssef Mohamed, Mohammed Tag-Adeen, Mina Tharwat, Ahmed Alzamzamy, Ahmed Nasr Bekhit, Alshaimaa M Eid, Abeer Awad, Mohammad Aamr, Waleed A Abd El Dayem, Mohamed-Naguib Wifi, Mohamed Alboraie Omar Elshaarawy, Eman Abdelsameea, Department of Hepatology, Gastroenterology and Liver Transplantation, National Liver Institute, Menoufia University, Shebine Elkom 32511, Egypt Omar Elshaarawy, Department of Internal Medicine and Center of Alcohol Research and Liver Diseases, Salem Medical Center, Heidelberg University, Heidelberg 69121, Germany Sameh Aldesoky Lashen, Department of Internal Medicine, Faculty of Medicine, University of Alexandria, Alexandria 21521, Egypt Nahed A Makhlouf, Doaa Abdeltawab, Department of Tropical Medicine and Gastroenterology, Faculty of Medicine, Assiut University, Assiut 71515, Egypt

Mariam Salah Zaghloul, Department of Hepatology, Gastroentrology and Infectious Diseases, Kafrelsheikh University, Faculty of Medicine, Kafrelsheikh 33565, Egypt Rasha M Ahmed, Hayam Fathy, Department of Internal Medicine, Faculty of Medicine, Assiut University, Assiut 71515, Egypt Shimaa Afifi, National Hepatology and Tropical Medicine Research Institute, Cairo 11638, Egypt Muhammad Abdel-Gawad, Department of Hepatology, Gastroenterology and Infectious Diseases, Faculty of Medicine, Al-Azhar University, Assiut 71524, Egypt Sherief Abd-Elsalam, Department of Tropical Medicine and Infectious Diseases, Faculty of Medicine, Tanta University, Tanta 31527, Egypt Salem Youssef Mohamed, Department of Internal Medicine, Gastroenterology and Hepatology Unit, Faculty of Medicine, Zagazig University, Zagazig 44519, Egypt Mohammed Tag-Adeen, Department of Internal Medicine, Gastroenterology Unit, Qena Faculty of Medicine, South Valley University, Qena 83523, Egypt Mina Tharwat, Department of Tropical Medicine and Gastroenterology, Faculty of Medicine, Aswan University, Aswan 81528, Egypt Ahmed Alzamzamy, Department of Gastroenterology and Hepatology, Military Medical Academy, Cairo 11771, Egypt

Al-Azhar University, ElMokhayam El Daem St., Nasr City, Cairo 11562, Egypt. alboraie@azhar.edu.eg Received: October 14, 2020 Revised: November 3, 2020 Accepted: Published online:

Abstract BACKGROUND The current coronavirus disease 2019 (COVID-19) pandemic has affected routine endoscopy service across the gastroenterology community. This led to the suspension of service provision for elective cases. AIM To assess the potential barriers for resuming the endoscopy service in Egypt. METHODS A national online survey, four domains, was disseminated over a period of 4 wk in August 2020. The primary outcome of the survey was to determine the impact of the COVID-19 pandemic on the endoscopy service and barriers to the full resumption of a disabled center (s). RESULTS A hundred and thirteen Egyptian endoscopy centers participated in the survey. The waiting list was increased by ≥ 50% in 44.9% of areas with clusters of COVID-19 cases ( n = 49) and in 35.5% of areas with sporadic cases ( n = 62). Thirty nine (34.8%) centers suffered from staff shortage, which was considered a barrier against service resumption by 86.4% of centers in per-protocol analysis. In multivariate analysis, the burden of cases in the unit locality, staff shortage/recovery and the availability of separate designated rooms for COVID-19 cases could markedly affect the resumption of endoscopy practice ( P = 0.029, < 0.001 and 0.02, respectively) and Odd’s ratio (0.15, 1.8 and 0.16, respectively). CONCLUSION The COVID-19 pandemic has led to restrictions in endoscopic volumes. The staff shortage/recovery and the availability of COVID-19 designed rooms are the most important barriers against recovery. Increasing working hours and

INTRODUCTION

In December 2019, a novel an enveloped RNA Beta coronavirus caused an outbreak called severe acute respiratory syndrome coronavirus 2 (SARS-CoV-

  1. -resulted in coronavirus disease 2019 (COVID-19) began in Wuhan[1,2]. The virus rapidly spread throughout the country, then throughout the whole world, and was declared a global pandemic by the World Health Organization in March 2020[3]. As of September 23, 2020, it has infected over 31 million people worldwide and caused more than 965000 deaths[3,4]. The clinical gastrointestinal manifestations are present and less severe when compared with SARS[1,5,6]. Early reports from Wuhan stated that around 10% of COVID-19 cases had diarrhea and nausea, 1 to 2 d before the beginning of respiratory symptoms[6], and some cases may be missed if screening was applied only to those with respiratory symptoms. It is widely believed that SARS-CoV-2 spreads via droplets and contact (especially if within one meter of distance), but there is evidence that airborne spread is also possible during aerosol-generating procedures (AGPs)[2]. In addition, new emerging evidence that SARS-CoV-2 can be found in the feces of patients, giving the possibility of fecal–oral route transmission[7,8]. This can be explained by the excessive expression of angiotensin-converting enzyme 2 protein, a receptor for SARS-CoV-2 required for cell entry in the epithelial layer of the gastrointestinal tract[9]. Being highly infective, SARS-CoV-2 put the healthcare workers (HCWs) in clinical departments performing endoscopy in great challenges during this pandemic as being highly susceptible to getting the infection[10]. Endoscopy could be considered a high-risk procedure as pulmonary and gastric secretions, as well as fecal material, may contain high viral loads. So, infection to HCWs occurs either due to direct contact with the infected patients or to the lack or improper use of the personal protective equipment[11]. In fact, several studies have discussed infection prevention and control measures that must be implemented to increase patient safety,

prevent nosocomial outbreaks, protect HCWs, and ensure the rational use of limited personal protective equipment (PPE)[11,12]. Several endoscopy societies and expert groups have offered recommendations and position statements for endoscopy during the COVID- 19 pandemic[11,13-16]. Several GI society guidelines recommended ceasing elective procedures during the pandemic to decrease the risk of infection[17- 19]. Different recommendations/guidelines have been recently released to ensure the smooth reopening of endoscopy units and resuming elective procedures[17]. Whether or not endoscopy units in different parts of the world are ready to resume service based on these recommendations is not fully known. This study is a multicenter study to discuss the barriers of resuming endoscopic maneuvers in different centers and governorates in Egypt as the coronavirus infection rate has remarkably decreased and there are international calls for resuming all the activities with caution and different precautions, and to assess whether the endoscopic service has returned to its near normal standard level. MATERIALS AND METHODS Methods We designed an online survey that was based on four domains (see Supplementary Figure 1). The first domain included the demographic data as regards the governorate, the type of health care facility, and the type(s) of endoscopy service(s) provided. The second domain was for the status of the COVID-19 pandemic and its impact on the endoscopy service(s). The third domain was directed to the readiness of the health care facility for dealing with COVID-19 cases (infrastructure, working staff, PPEs, case stratification, etc. ), and the fourth domain was about the ability of the facility to resume the endoscopy service(s) and the different barriers which preclude service resumption. The whole survey included 20 main questions. all the questions

didn’t give a full response, so they were excluded from the analysis. Most respondents ( n = 67, 59.3%) were from high-volume endoscopy units either University or teaching facility general hospitals providing emergency endoscopy. Cairo and Giza regions have participated with 30 (26.5%) centers, Lower Egypt (Alexandria, Beheira, Sharqia, Qalyubia, Damietta, and Ismailia) and Upper Egypt (Assiut, Fayoum, Sohag, Qena, Aswan and Luxor) have participated through 34 (30.1%) centers, and Delta region (Menoufia, Kafr el-sheik , Gharbia, and Dakahlia) have participated through 13 (11.5%) centers. COVID-19 designated facilities were present among 48 (42.5%) centers (Figure 1). Patient selection and classification On the day of planned endoscopic procedure patients were checked for being suspected cases of COVID-19 in 95 (84.1%) of centers. The process of selection and screening was based on symptoms among 90 centers (79.6%), temperature check among 82 centers (72.6%), non-contrast multi spiral computed tomography (MSCT) chest among 50 centers (44.2%), polymerase chain reaction (PCR) testing among 11 centers (9.7%), and antibody testing among 3 centers (2.7%). Impact of the current status of the pandemic on the waiting lists Endoscopy practice was almost resuming or resumed in about 70% of the centers Figure 2C. In general, there was an expansion of the waiting lists all over the country. The Quantification of the expansion is shown in Figure 2B. We found significant variation in the waiting lists according to the distribution of COVID-19 pandemic status among different centers. In areas with clusters of cases ( n = 49), the waiting lists increased by 0%-25% in 14.29%, 26%-50% in 32.65%, 51%-75% in 34.69%, 76%-100% in 10.2%, and by more than 100% in 8.17% of these centers. While in areas with sporadic cases ( n = 62), 45.16% of the centers had their waiting list increased by 0%- 25%, however, in 19.35% and 20.9% of the centers the list increased by

26%-50%, and 51%-75%, respectively. In about 14.59% of the centers, the waiting list increased by more than 75%, meanwhile, areas with no new cases ( n = 2), 50% of centers had their list increased by only 0%-25% (FET = 19.1, P = 0.005). Shortage in staff During the COVID-19 outbreak, endoscopy staff has been deployed to COVID-19 designated wards and hospitals. In addition, a significant number of healthcare providers were infected. Shortage of endoscopy staff was present among 39 (34.8%) of centers (Figure 2D). Specialists shortage was present in 88 (77.9%) of centers, nursing staff shortage in 90 (79.6%) of centers, and trainees shortage in 110 (97.3%) of centers. This shortage was considered as a barrier against resuming endoscopy service among 38 (33.6% in intention to treat analysis, 86.4% in per-protocol analysis; 69 centers didn’t answer). The shortage in specialists was more pronounced in Delta and lower Egypt than upper Egypt and Cairo and Giza (61.5% and 91.3% vs. 64.7% and 83.3% respectively, P = 0.019). However, the shortage of nursing staff and trainees were not significantly different among different centers, P = 0.93 and P = 0.24 respectively). Only 41 units (35%) had to increase the working hours to compensate for this shortage. Seventy-six units (67.3%) recovered their staff either from sick leave or COVID-19 wards. Pre-procedural precautions applied by different Centers during the COVID-19 pandemic During the current COVID-19 epidemic in Egypt, 72 (63.7%) of endoscopy centers have provided suitable waiting area for appropriate social distancing precautions, 65 (57.5%) of centers could provide an adequate number of recovery rooms to keep the social distancing strategy to the optimum, and 40 (35.4%) of centers have increased their working hours to accommodate the extra-burden of increased cases volume; at the same time, 77 (68.1%) of

resumption of endoscopic services commensurate with facilities and pandemic situations of each country[14,17-19]. To our knowledge, whether or not endoscopy centers in Egypt are ready to resume elective services has not been studied. Accordingly, the results of the current survey represent the current status of resuming routine endoscopic services in Egypt and determine the barriers of resuming such services. Our results showed that 70% of different centers all over Egypt have resumed routine endoscopic services as is illustrated in Figure 2C. This is in parallel to the current situation of early recovery phases of the pandemic and the decline in the number of new COVID-19 cases in Egypt and other countries worldwide[3]. Waiting lists of elective endoscopy practice is one of the challenges of full capacity resumption of endoscopic services and according to the British Society of Gastroenterology guidance in the early recovery stages, triage mechanisms are needed to prioritize patients scheduling according to the indications[20]. The highest percentages of waiting lists expansion are observed in areas with clusters of COVID-19 cases which indicate the awareness of senior decision-makers of endoscopy centers in Egypt with the importance of triaging and prioritization of patients scheduling in the light of clinical need with the available capacity. Also, this reflects their compliance with GI endoscopy societies' guidance. In addition, this observation complies with the current SARS-CoV-2 pandemic situation in Egypt, as there is a decreasing in the number of areas with new cases allowing endoscopy centers to restore their full capacity as soon as possible. Regarding the shortage in endoscopy staff, 34.5% of the centers reported a significant shortage of staff during the SARS-CoV-2 pandemic in nursing staff (79.6%) and specialists (77.9%). This is related to two factors; one was the reallocation for staff and medical equipment to the surge in demand to manage suspected and confirmed COVID-19 cases and the other was some of them get infected caused by frequent exposure to infected patients. The shortage in specialists was more pronounced in Delta and Lower Egypt

geographically which may be related to the geographic distribution of a large number of confirmed COVID-19 cases and isolation hospitals that need more medical staff. This shortage in endoscopy staff is considered as a barrier against resuming endoscopy service among 38 centers in the current study (33.6% in intention to treat analysis where n = 113, 86.4% in the per-protocol analysis where n = 44). Regarding patient selection before endoscopy, a large number of participating centers (84.1%) screened their patients. The most common method used was symptoms-based screening for COVID- risk stratification (79.6%) of the centers and fewer centers used PCR testing (9.7%). Similarly, Alboraie et al [21]^ reported that most worldwide centers (93.9%) screened patients for possible COVID-19 disease prior to the procedure and 54 centers (33.13%) used PCR testing. However, asymptomatic infected patients are a known source for transmission[2,22], accordingly, this type of screening is not sufficient to guide for COVID-19 risk stratification. A recent study from China used both symptoms-based screening and PCR in their patient screening, reported no cases of endoscopy-related nosocomial COVID-19 disease transmission in 1361 cases[23]. Regarding pre-procedural precautions and endoscopy centers designation, our results show that most participating centers so far follow the different international GI endoscopy societies guidelines[14,17-19]^ including appropriate social distancing precautions or increase working hours to accommodate the extra-burden of increased cases volume. More than two-thirds of our centers have adopted a selection strategy to select the endoscopist and the assisting team based on the presence of a suspected/confirmed COVID-19 case. Also, Alboraie et al [21]^ stated that the majority (78.5%) of the centers considered dedicated teams for the delivery of endoscopic services after the onset of the pandemic. To reduce the risk of infection spread most of the international society's recommendations are in agreement with the existence of a restricted

ARTICLE HIGHLIGHTS

Research background An outbreak of coronavirus disease 2019 (COVID-19) has hit the world and disturbed whole healthcare system, including endoscopic practices which are a very risky procedures in terms of exposure to infection. Research motivation Smooth resumption of routine endoscopic service has to be guaranteed as well as decreasing the burden of exposing patients and endoscopy staff to infection during endoscopic procedures. Many strategies have to be implemented in endoscopy units, however, these strategies face many barriers as shortage of personal protective equipment, working staff and post procedure tracing of infection and follow-up of patients. Research objectives This survey study was designed to evaluate feasibility and difficulty of resumption of routine endosopic service in the context of COVID- pandemic. Research methods We conducted a survey study that included 20 questions to be answered by the head of endoscopy units in 113 units from all over Egypt. Research results One hundred and thirteen centers participated in the study from all over Egypt. Due to halting the routine endoscopic services during the pandemic, the waiting lists were doubled in most of the centers. Third of the centers suffered of shortage of endoscopy staff. The lack of dedicated endoscopy rooms for infected patients and the staff shortage were the main barriers to resume routine services smoothly.

Research conclusions We recommend increasing working hours and dividing endoscopy staff into teams to overcome the shortage of endoscopy staff. Also, follow up of patients for two weeks after endoscopic procedures to detect any possible transmission of infection in endoscopy centers as this strategy may help in tracing the source of nosocomial transmission. Research perspectives For smooth resumption of endoscopic service between two waves of the current pandemic, several strategies have to be applied in a uniform manner in all endoscopy units. Our study showed how different centers acted differently during this pandemic in terms of their plan to safely getting routine endoscopy service on track. Future studies should propose modalities to guarantee uniform application of determined strategies that overcome the current barriers. REFERENCES 1 Xie J , Tong Z, Guan X, Du B, Qiu H. Clinical Characteristics of Patients Who Died of Coronavirus Disease 2019 in China. JAMA Netw Open 2020; 3 : e205619 [PMID: 32275319 DOI: 10.1001/jamanetworkopen.2020.5619] 2 Huang C , Wang Y, Li X, Ren L, Zhao J, Hu Y, Zhang L, Fan G, Xu J, Gu X, Cheng Z, Yu T, Xia J, Wei Y, Wu W, Xie X, Yin W, Li H, Liu M, Xiao Y, Gao H, Guo L, Xie J, Wang G, Jiang R, Gao Z, Jin Q, Wang J, Cao B. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 2020; 395 : 497-506 [PMID: 31986264 DOI: 10.1016/S0140-6736(20)30183-5] 3 Coronavirus Disease (COVID-19) Situation Reports [Internet]. [cited 2020 Sep 23]. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation- reports

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  1. American Society for Gastrointestinal Endoscopy: guidance for trainees during the COVID-19 pandemic. Gastrointest Endosc 2020; 92 : 748- [PMID: 32485214 DOI: 10.1016/j.gie.2020.05.032] 18 Chiu PWY , Ng SC, Inoue H, Reddy DN, Ling Hu E, Cho JY, Ho LK, Hewett DG, Chiu HM, Rerknimitr R, Wang HP, Ho SH, Seo DW, Goh KL, Tajiri H, Kitano S, Chan FKL. Practice of endoscopy during COVID-19 pandemic: position statements of the Asian Pacific Society for Digestive Endoscopy (APSDE- COVID statements). Gut 2020; 69 : 991-996 [PMID: 32241897 DOI: 10.1136/gutjnl-2020-321185]

19 Gralnek IM , Hassan C, Beilenhoff U, Antonelli G, Ebigbo A, Pellisè M, Arvanitakis M, Bhandari P, Bisschops R, Van Hooft JE, Kaminski MF, Triantafyllou K, Webster G, Pohl H, Dunkley I, Fehrke B, Gazic M, Gjergek T, Maasen S, Waagenes W, de Pater M, Ponchon T, Siersema PD, Messmann H, Dinis-Ribeiro M. ESGE and ESGENA Position Statement on gastrointestinal endoscopy and the COVID-19 pandemic. Endoscopy 2020; 52 : 483- [PMID: 32303090 DOI: 10.1055/a-1155-6229] 20 The British Society of Gastroenterology [Internet]. BSG Guidance on recommencing GI Endoscopy in the deceleration & early recovery phases of the COVID-19 pandemic | [cited 2020 Sep 23]. Available from: https://www.bsg.org.uk/covid-19-advice/bsg-guidance-on-recommencing-gi- endoscopy-in-the-deceleration-early-recovery-phases-of-the-covid-19- pandemic/ 21 Alboraie M , Piscoya A, Tran QT, Mendelsohn RB, Butt AS, Lenz L, Alavinejad P, Emara MH, Samlani Z, Altonbary A, Monged A, Lemmers A, Sudovykh I, Ho DQD, Ghazanfar S, Kamau E, Iqbal S, Tan DMY, Liao WC, Vignesh S; “The Global Endo-COVID working group”. The global impact of COVID-19 on gastrointestinal endoscopy units: An international survey of endoscopists. Arab J Gastroenterol 2020; 21 : 156-161 [PMID: 32912748 DOI: 10.1016/j.ajg.2020.08.008] 22 Hoehl S , Rabenau H, Berger A, Kortenbusch M, Cinatl J, Bojkova D, Behrens P, Böddinghaus B, Götsch U, Naujoks F, Neumann P, Schork J, Tiarks- Jungk P, Walczok A, Eickmann M, Vehreschild MJGT, Kann G, Wolf T, Gottschalk R, Ciesek S. Evidence of SARS-CoV-2 Infection in Returning Travelers from Wuhan, China. N Engl J Med 2020; 382 : 1278-1280 [PMID: 32069388 DOI: 10.1056/NEJMc2001899] 23 Lindsley WG , Martin SB Jr, Thewlis RE, Sarkisian K, Nwoko JO, Mead KR, Noti JD. Effects of Ultraviolet Germicidal Irradiation (UVGI) on N95 Respirator Filtration Performance and Structural Integrity. J Occup Environ Hyg 2015; 12 : 509-517 [PMID: 25806411 DOI: 10.1080/15459624.2015.1018518]