COVID-19 screening before gastrointestinal procedures

In March 2020, the World Health Organization declared coronavirus 2019 (COVID-19) a global pandemic. We aimed to assess the ability of COVID-19 screening to detect preprocedural infection at the gastrointestinal units. One hundred and three patients indicated for gastrointestinal tract interventional procedures were included. All patients surveyed for COVID-19-related symptoms and COVID-19 rapid IgM/IgG antibodies. Symptomatic and COVID-19 antibody-positive patients further tested for COVID-19 reverse transcriptase by polymerase chain reaction (RT-PCR). All patients contacted, 14 days after the procedure and asked about the possible development of COVID-19. All health care workers (HCWs) (n=18) were screened weekly for COVID-19-related symptoms. The mean age was 46.11 ± 17.16 years of them 58.25% were males. 2.9% patients had COVID-19-related symptoms and 97.1% were asymptomatic. All symptomatic patients tested positive for COVID-19 IgM antibody and RT-PCR. Among asymptomatic patients 23% had positive COVID-19 antibodies, of them 56.5%patients had positive RT-PCR. One HCW developed COVID-19 during the study. None of the included patients developed new onset of COVID-19 infection, two weeks after the procedure. COVID-19 antibody test may be a reasonable preprocedural screening method for low-income countries and COVID-19 RT-PCR screening for symptomatic patients and those with positive COVID-19 antibody test.

Worldwide, this pandemic has had a significant impact on gastrointestinal practices, with an approximately 83% reduction in endoscopic procedures [4]. Similar overall reductions in endoscopic procedures have been seen in Italy in nationwide multicentric studies as well as in Pakistan [5,6]. Gastroenterology staff may be at an increased risk for acquiring COVID-19 because the virus is detectable in the GIT [7], and endoscopy is an aerosol-generating procedur e [8].. Recommendations have been issued to guide personal protective equipment (PPE) use [9] and the triage of procedural urgency [10]. There are many positive impacts of preprocedure testing for COVID-19, such as categorization of patient risk, the use of appropriate PPE, and decreasing the spread of the virus to patients and HCWs.
Ideally, all patients having gastrointestinal procedures would be required to undergo testing to confirm or

Open Access
Egyptian Liver Journal *Correspondence: Ahmedmaher.206@azhar.edu.eg 1 Department of Internal Medicine, Al-Azhar University, Nasr City, Cairo 11884, Egypt Full list of author information is available at the end of the article exclude active viral infection by reverse transcriptase polymerase chain reaction (RT-PCR). There is currently no national policy for preprocedural screening of patients during the COVID-19 pandemic in Egypt. Due to the current limited supply of available testing kits along with the cost involved, we used a combination of COVID-19 symptoms and COVID-19 rapid IgM/IgG antibody levels for prescreening of patients who had indications for gastrointestinal procedures.

Methods
We aimed to assess the ability of COVID-19 screening tools using patients' symptoms and preprocedure COVID-19 antibody test to detect preprocedural infection and to prevent nosocomial COVID-19 at gastroenterology units.
This prospective cross-sectional study was conducted at Al Hussein University Hospital, Cairo, Egypt, between April 1 and August 1, 2020. The study was approved by the ethical committee of Faculty of Medicine, Al-Azhar University, Cairo, Egypt (Med._147Med.Research. COVID-19 Screening Before Gastrointestinal Procedures. _00000175). Informed consent was obtained from all individual participants included in the study. Among 144 patients who underwent gastrointestinal procedures, 41 patients were not tested for COVID-19 antibodies and excluded from the study. Finally, 103 patients surveyed for COVID-19 symptoms and COVID-19 rapid IgM/IgG antibodies were included.
All patients who had indications for diagnostic and/ or therapeutic gastrointestinal procedures (n=103) underwent prescreening for COVID-19 symptoms. In addition, the occurrence of postprocedure COVID-19 infection was assessed among the included patients and medical staff members working in the gastrointestinal unit (n=18) to assess the efficiency of the proposed prescreening method. Patients who were not tested for COVID-19 antibodies were excluded.

Postprocedure screening for COVID-19
All patients were contacted (by phone) 14 days after the procedure and asked about the possible development of COVID-19 symptoms [11,12]. The postprocedural diagnosis of COVID-19 infection was based on a new onset of fever ≥ 38°C and two or more new symptoms: cough, sore throat, dyspnea, anosmia, loss of taste, and diarrhea [13]. Patients with suspected symptoms of COVID-19 were referred to COVID-19 treatment centers.
All HCWs (n=18) were screened weekly for COVID-19-related symptoms. In the setting of a highly suspected COVID-19 [13], the clinical diagnosis was further confirmed by COVID-19 rapid IgM/IgG antibodies and the COVID-19 RT-PCR. Infected HCWs discharged from duty and referred for treatment.

COVID-19 detection by rapid IgM/IgG
SARS-CoV-2 antibodies were detected by a COVID-19 IgM/IgG antibody rapid diagnostic test (SGTi-flex COVID-19 IgM/IgG, Sugentech, South Korea). It is a qualitative immunoassay for the rapid detection of both anti-SARS-CoV-2-IgM and anti-SARS-CoV-2-IgG in the venous blood or plasma with a sensitivity of 92.43% and a specificity of 99.15%, as reported by the manufacturer. The results were analyzed visually after 15-20 min.

COVID-19 detection by RT-PCR
Nasopharyngeal swabs were collected for COVID-19 RT-PCR testing as described previously [14]. Briefly, probes were annealed to three target sequences specific to COVID-19: ORF1ab, nucleocapsid (N), and spike (S) primers/probes for bacteriophage MS2. Two of the three genes and the MS2 (positive control) had to be positive for a diagnosis of COVID-19.
Indications of urgent (8-24 h) endoscopic procedures included upper GIT bleeding, food bolus impaction, lower GIT bleeding (hemodynamically unstable), acute intestinal obstruction, cholangitis with sepsis/septic shock, and biliary leakage. Urgent percutaneous transhepatic drainage (PTD) was indicated in cholangitis with sepsis/septic shock and biliary leakage. Semiurgent (24 h to 7 weeks) endoscopic procedures were indicated in the following situations: gastric cancer diagnosis, acute-onset dysphagia, lower GIT bleeding (hemodynamically stable), partial intestinal obstruction, new-onset bloody diarrhea with negative cultures, inflammatory bowel disease flare, choledocholithiasis with/without cholangitis, biliary pancreatitis with/without cholangitis, concerns for pancreatic cancer or cholangiocarcinoma, and small-bowel bleeding. Semiurgent indications for radiofrequency ablation (RFA) and transarterial chemoembolization (TACE) included active hepatocellular carcinoma (HCC). Semiurgent liver biopsy was performed for patients with ongoing hepatitis and for those with potentially malignant liver lesions. Semiurgent pigtail insertion and PTD were indicated in patients with active hydatid cysts, choledocholithiasis with or without cholangitis, and biliary pancreatitis with or without cholangitis.
Elective (≥ 8 weeks) endoscopic procedures were performed for the following indications: ampullary adenoma, isolated weight loss, heartburn, dyspepsia/ noncardiac chest pain, established dysphagia, Barrett's esophagus, esophageal varices evaluation or follow-up banding, iron-deficiency anemia, percutaneous endoscopic gastrostomy (PEG) tube placement, chronic diarrhea, colorectal cancer screening, ulcerative colitis with dysplasia, biliary stent replacement, concerns for submucosal mass, double duct sign without a discrete mass, concerns for neuroendocrine tumor, pancreatic cyst evaluation, and small-bowel tumor. Elective pigtail insertion was performed in patients with symptomatic simple liver cysts.

Precautions to prevent infection during gastrointestinal procedures
Based on the COVID-19 RT-PCR results of the included patients, HCWs likely followed the recommended precautions to protect against infection. If patients were negative on COVID-19 RT-PCR, HCWs wore a hair net, surgical mask, face shield, single-use gown, and single pair of gloves. If patients were positive on COVID-19 RT-PCR, the HCWs wore a hair net, N-95 or FFP, 2/3 surgical mask, face shield and goggles, full-sleeve gown, a double layer of gloves, and shoe covers. All rooms were non-negative-pressure and were disinfected at the end of each procedure. All patients wore surgical masks (except during procedures).

Statistical analysis
Data were analyzed using the statistical package for social sciences, version 20.0 (SPSS Inc., Chicago, Illinois, USA). Quantitative data are expressed as the mean ± standard deviation (SD). Qualitative data are expressed as frequencies and percentages.

Results
Among 144 patients who underwent gastrointestinal procedures, 41 patients were not tested for COVID-19 antibodies and excluded from the study. Finally, 103 patients surveyed for COVID-19 symptoms and COVID-19 rapid IgM/IgG antibodies were included. The mean age of the included patients was 46.11 ± 17.16 years, and there were 60 (58.25%) males and 43 (42.75%) females (Table 1)
The frequency of diabetes mellitus and elevated CRP levels were significantly higher among asymptomatic patients who were positive for COVID-19 antibodies (P < 0.05) ( Table 2).

Discussion
In the current study, we first surveyed all patients for COVID-19 symptoms and COVID-19 rapid IgM/IgG antibodies. Patients with COVID-19-related symptoms and/or positive antibodies were further subjected to RT-PCR testing. The preprocedural frequency of COVID-19 antibodies among the included patients was 25.3% (26/103), and the majority 88.5% (23/26) of COVID-19 antibody positive patients were asymptomatic. RT-PCR was detected in all (n=3) symptomatic patients and in 61.5% of COVID-19 antibody-positive patients. There is no postprocedure infection in all enrolled patients, based on symptoms screening. Symptom-based screening alone is not helpful in selecting patients prior to GIT procedures during the COVID-19 pandemic [15].. Not only was the positive predictive value of COVID-19 symptoms low (2.46%), but positive RT-PCR tests were also detected in asymptomatic patients prior to the procedures [15]. In support of these findings, 13% of asymptomatic patients had COVID-19, as detected by RT-PCR in our study. These data highlighted the importance of RT-PCR in the prescreening of patients prior to GIT procedures. However, universal RT-PCR testing prior to GIT procedures is not without limitations. One concern is the accuracy of the currently available assays [16,17]. In addition, RT-PCR testing is time consuming and may not be a suitable prescreening test for urgent and semiurgent procedures. Indeed, a 15.3 to 16.6% increase in colorectal cancer deaths, likely related to delays in diagnosis during the pandemic, was reported [18]. Moreover, RT-PCR is an expensive test and may not be affordable in a country with limited resources, such as Egypt. Although it cannot replace preprocedural RT-CR universal screening, preprocedural RT-PCR screening in symptomatic and/or COVID-19 antibodypositive patients may be more economical for lowincome countries.
Polymerase chain reaction testing is the gold standard in COVID-19 diagnosis, yet the uncertainty of its accuracy should not be ignored. This suggests that the preprocedural clinical evaluation of COVID-19 based on symptoms, risk factors, and disease prevalence is of paramount importance. All symptomatic patients (n=3) in the current study had COVID-19, as confirmed by RT-PCR. In contrast, Bowyer et al. had 119 symptomatic patients who underwent endoscopic evaluation had negative RT-PCR results prior to endoscopy [15]. This discrepancy may be related to the fact that all symptomatic patients in our study had highly suggestive COVID-19 symptoms (fever ≥ 38°C); on the other hand, many patients in the Bowyer et al. study presented with known GI symptoms. The accuracy of COVID-19 antibody tests in prescreening for COVID- 19 has not yet been validated. COVID-19 antibody was detected in 1.9% of Spanish patients screened before endoscopy [11]. The frequency of COVID-19 antibodies among Egyptian HCWs ranged from 12.2 to 18.2%, of which 33.3-35% had positive COVID-19 RT-PCR results [14,19]. A higher rate of COVID-19 antibodies (25.3%) in patients was detected in our study, which may be explained by the variable prevalence of COVID-19 in different countries as well as the variable sensitivity of the kits used. Notably, 61.5% of COVID-19 antibody-positive patients had positive RT-PCR results.
The incidence of preprocedural COVID-19 among patients undergoing GIT procedures is variable. In a multicenter, retrospective, Italian survey, the preprocedural rate of RT-PCR among patients undergoing ERCP was 2.7% [20]. Lower rates of 0.8%, 0.14%, and 0.96% were reported in Winnebago [15], California [21], and New York City [22], respectively. The high rate (15.5%) of COVID-19 in our patients may reflect the high prevalence of COVID-19 during the period of the study in Egypt.
The rate of COVID-19 among HCWs at GIT facilities ranged from 4.3 to 15.8% [20,23]. A similar rate (13.5%) was confirmed by RT-PCR among Egyptian HCWs at the GIT facility [19]. The lower rate (5.5%) in our study may be explained by the fact that RT-PCR was used in symptomatic health care workers only. Indeed, COVID-19 was detected in 16.1% of asymptomatic HCWs in the GIT department [19] and the emergency department (14.3%) using RT-PCR [14].
The advantages of our study are that we conducted the study during the peak of the 1st wave of the COVID-19 pandemic in Egypt, used a simple combination of clinical and serological tests to detect patients with a high risk for COVID-19, and tested them with RT-PCR. The limitations of our study include the single center study, a small sample size, and the lack of all patients tested COVID-19 with RT-PCR.

Conclusion
Preprocedural COVID-19 RT-PCR screening in symptomatic patients and/or COVID-19 antibody-positive patients is recommended prior to gastrointestinal procedures. The absence of postprocedure symptomatic COVID-19 in our study might be an indication that the screening methods and PPE used are adequate preventive tools in low-income countries.