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      Snowballing transmission of COVID-19 (SARS-CoV-2) through wastewater: Any sustainable preventive measures to curtail the scourge in low-income countries?

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          Abstract

          In this communication, we proposed sustainable preventive measures that may be adopted by the low-income countries to forestall the potential outbreak and transmission of COVID-19 (coronavirus disease 2019) through wastewater. Most low-income countries have poor sanitation and wastewater management policies, which create potential risks of COVID 19 spread. Hence, the proposed measures include decentralization of wastewater treatment facilities, community-wide monitoring and testing of SARS-CoV-2 in wastewater samples, improved sanitation, developing point-of-use devices for wastewater decontamination, and more focused policy interventions. Therefore, this paper adds useful insights into the monitoring and management of ongoing COVID-19 outbreak in low-income countries.

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          Highlights

          • The potential risks of COVID-19 in wastewater are highlighted.

          • Wastewaters from hospitals, quarantine centers, etc. dedicated to COVID-19 treatments may contain SARS-CoV-2 RNA particles.

          • Preventive measures to tackle the potential risks of SARS-CoV-2 transmission in wastewater are proposed.

          • Chlorination, ozonation, and UV radiations are useful in SARS-CoV-2 deactivation in water.

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          Most cited references52

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          First Case of 2019 Novel Coronavirus in the United States

          Summary An outbreak of novel coronavirus (2019-nCoV) that began in Wuhan, China, has spread rapidly, with cases now confirmed in multiple countries. We report the first case of 2019-nCoV infection confirmed in the United States and describe the identification, diagnosis, clinical course, and management of the case, including the patient’s initial mild symptoms at presentation with progression to pneumonia on day 9 of illness. This case highlights the importance of close coordination between clinicians and public health authorities at the local, state, and federal levels, as well as the need for rapid dissemination of clinical information related to the care of patients with this emerging infection.
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            Detection of SARS-CoV-2 in Different Types of Clinical Specimens

            This study describes results of PCR and viral RNA testing for SARS-CoV-2 in bronchoalveolar fluid, sputum, feces, blood, and urine specimens from patients with COVID-19 infection in China to identify possible means of non-respiratory transmission.
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              Evidence for Gastrointestinal Infection of SARS-CoV-2

              Since the novel coronavirus (SARS-CoV-2) was identified in Wuhan, China, at the end of 2019, the virus has spread to 32 countries, infecting more than 80,000 people and causing more than 2600 deaths globally. The viral infection causes a series of respiratory illnesses, including severe respiratory syndrome, indicating that the virus most likely infects respiratory epithelial cells and spreads mainly via respiratory tract from human to human. However, viral target cells and organs have not been fully determined, impeding our understanding of the pathogenesis of the viral infection and viral transmission routes. According to a recent case report, SARS-CoV-2 RNA was detected in a stool specimen, 1 raising the question of viral gastrointestinal infection and a fecal-oral transmission route. It has been proven that SARS-CoV-2 uses angiotensin-converting enzyme (ACE) 2 as a viral receptor for entry process. 2 ACE2 messenger RNA is highly expressed and stabilized by B0AT1 in gastrointestinal system, 3 , 4 providing a prerequisite for SARS-CoV-2 infection. To further investigate the clinical significance of SARS-CoV-2 RNA in feces, we examined the viral RNA in feces from 71 patients with SARS-CoV-2 infection during their hospitalizations. The viral RNA and viral nucleocapsid protein were examined in gastrointestinal tissues from 1 of the patients. Methods From February 1 to 14, 2020, clinical specimens, including serum, nasopharyngeal, and oropharyngeal swabs; urine; stool; and tissues from 73 hospitalized patients infected with SARS-CoV-2 were obtained in accordance with China Disease Control and Prevention guidelines and tested for SARS-CoV-2 RNA by using the China Disease Control and Prevention–standardized quantitative polymerase chain reaction assay. 5 Clinical characteristics of the 73 patients are shown in Supplementary Table 1. The esophageal, gastric, duodenal, and rectal tissues were obtained from 1 of the patients by using endoscopy. The patient’s clinical information is described in the Supplementary Case Clinical Information and Supplementary Table 2. Histologic staining (H&E) as well as viral receptor ACE2 and viral nucleocapsid staining were performed as described in the Supplementary Methods. The images of fluorescent staining were obtained by using laser scanning confocal microscopy (LSM880, Carl Zeiss MicroImaging, Oberkochen, Germany) and are shown in Figure 1 . This study was approved by the Ethics Committee of The Fifth Affiliated Hospital, Sun Yat-sen University, and all patients signed informed consent forms. Figure 1 Images of histologic and immunofluorescent staining of gastrointestinal tissues. Shown are images of histologic and immunofluorescent staining of esophagus, stomach, duodenum, and rectum. The scale bar in the histologic image represents 100 μm. The scale bar in the immunofluorescent image represents 20 μm. Results From February 1 to 14, 2020, among all of the 73 hospitalized patients infected with SARS-CoV-2, 39 (53.42%), including 25 male and 14 female patients, tested positive for SARS-CoV-2 RNA in stool, as shown in Supplementary Table 1. The age of patients with positive results for SARS-CoV-2 RNA in stool ranged from 10 months to 78 years old. The duration time of positive stool results ranged from 1 to 12 days. Furthermore, 17 (23.29%) patients continued to have positive results in stool after showing negative results in respiratory samples. Gastrointestinal endoscopy was performed on a patient as described in the Supplementary Case Clinical Information. As shown in Figure 1, the mucous epithelium of esophagus, stomach, duodenum, and rectum showed no significant damage with H&E staining. Infiltrate of occasional lymphocytes was observed in esophageal squamous epithelium. In lamina propria of the stomach, duodenum, and rectum, numerous infiltrating plasma cells and lymphocytes with interstitial edema were seen. Importantly, viral host receptor ACE2 stained positive mainly in the cytoplasm of gastrointestinal epithelial cells (Figure 1). We observed that ACE2 is rarely expressed in esophageal epithelium but is abundantly distributed in the cilia of the glandular epithelia. Staining of viral nucleocapsid protein was visualized in the cytoplasm of gastric, duodenal, and rectum glandular epithelial cell, but not in esophageal epithelium. The positive staining of ACE2 and SARS-CoV-2 was also observed in gastrointestinal epithelium from other patients who tested positive for SARS-CoV-2 RNA in feces (data not shown). Discussion In this article, we provide evidence for gastrointestinal infection of SARS-CoV-2 and its possible fecal-oral transmission route. Because viruses spread from infected to uninfected cells, 6 viral-specific target cells or organs are determinants of viral transmission routes. Receptor-mediated viral entry into a host cell is the first step of viral infection. Our immunofluorescent data showed that ACE2 protein, which has been proven to be a cell receptor for SARS-CoV-2, is abundantly expressed in the glandular cells of gastric, duodenal, and rectal epithelia, supporting the entry of SARS-CoV-2 into the host cells. ACE2 staining is rarely seen in esophageal mucosa, probably because the esophageal epithelium is mainly composed of squamous epithelial cells, which express less ACE2 than glandular epithelial cells. Our results of SARS-CoV-2 RNA detection and intracellular staining of viral nucleocapsid protein in gastric, duodenal, and rectal epithelia demonstrate that SARS-CoV-2 infects these gastrointestinal glandular epithelial cells. Although viral RNA was also detected in esophageal mucous tissue, absence of viral nucleocapsid protein staining in esophageal mucosa indicates low viral infection in esophageal mucosa. After viral entry, virus-specific RNA and proteins are synthesized in the cytoplasm to assemble new virions, 7 which can be released to the gastrointestinal tract. The continuous positive detection of viral RNA from feces suggests that the infectious virions are secreted from the virus-infected gastrointestinal cells. Recently, we and others have isolated infectious SARS-CoV-2 from stool (unpublished data), confirming the release of the infectious virions to the gastrointestinal tract. Therefore, fecal-oral transmission could be an additional route for viral spread. Prevention of fecal-oral transmission should be taken into consideration to control the spread of the virus. Our results highlight the clinical significance of testing viral RNA in feces by real-time reverse transcriptase polymerase chain reaction (rRT-PCR) because infectious virions released from the gastrointestinal tract can be monitored by the test. According to the current Centers for Disease Control and Prevention guidance for the disposition of patients with SARS-CoV-2, the decision to discontinue transmission-based precautions for hospitalized patients with SARS-CoV-2 is based on negative results rRT-PCR testing for SARS-CoV-2 from at least 2 sequential respiratory tract specimens collected ≥24 hours apart. 8 However, in more than 20% of patients with SARS-CoV-2, we observed that the test result for viral RNA remained positive in feces, even after test results for viral RNA in the respiratory tract converted to negative, indicating that the viral gastrointestinal infection and potential fecal-oral transmission can last even after viral clearance in the respiratory tract. Therefore, we strongly recommend that rRT-PCR testing for SARS-CoV-2 from feces should be performed routinely in patients with SARS-CoV-2 and that transmission-based precautions for hospitalized patients with SARS-CoV-2 should continue if feces test results are positive by rRT-PCR testing.
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                Author and article information

                Contributors
                Journal
                Sci Total Environ
                Sci. Total Environ
                The Science of the Total Environment
                Elsevier B.V.
                0048-9697
                1879-1026
                2 July 2020
                10 November 2020
                2 July 2020
                : 742
                : 140680
                Affiliations
                [a ]Department of Agricultural Civil Engineering, Kyungpook National University, Daegu, Republic of Korea
                [b ]Department of Agricultural and Biosystems Engineering, University of Ilorin, PMB 1515 Ilorin, Nigeria
                [c ]Department of Civil and Environmental Engineering, Federal University of Technology, PMB 704 Akure, Nigeria
                [d ]Key Laboratory of Environmental Biotechnology, Research Centre for Eco-Environmental Sciences, Chinese Academy of Sciences, Beijing 100085, China
                [e ]Kwara State Ministry of Health, Ilorin, Kwara State, Nigeria
                [f ]Department of Chemical Engineering, University of Ilorin, PMB 1515 Ilorin, Nigeria
                [g ]Institute of Agricultural Science & Technology, Kyungpook National University, Daegu, Republic of Korea
                Author notes
                [* ]Correspondence to: Bashir Adelodun, Department of Agricultural Civil Engineering, Kyungpook National University, Daegu, Republic of Korea. Department of Agricultural and Biosystems Engineering, University of Ilorin, PMB 1515 Ilorin, Nigeria. adelodun.b@ 123456unilorin.edu.ng
                [** ]Correspondence to: Kyung-Sook Choi, Department of Agricultural Civil Engineering, Kyungpook National University, Daegu, Republic of Korea. Institute of Agricultural Science & Technology, Kyungpook National University, Daegu, Republic of Korea. ks.choi@ 123456knu.ac.kr
                Article
                S0048-9697(20)34202-9 140680
                10.1016/j.scitotenv.2020.140680
                7329667
                32629273
                28f45240-7161-4c96-98c3-187ec02f2a37
                © 2020 Elsevier B.V. All rights reserved.

                Since January 2020 Elsevier has created a COVID-19 resource centre with free information in English and Mandarin on the novel coronavirus COVID-19. The COVID-19 resource centre is hosted on Elsevier Connect, the company's public news and information website. Elsevier hereby grants permission to make all its COVID-19-related research that is available on the COVID-19 resource centre - including this research content - immediately available in PubMed Central and other publicly funded repositories, such as the WHO COVID database with rights for unrestricted research re-use and analyses in any form or by any means with acknowledgement of the original source. These permissions are granted for free by Elsevier for as long as the COVID-19 resource centre remains active.

                History
                : 12 May 2020
                : 29 June 2020
                : 30 June 2020
                Categories
                Article

                General environmental science
                covid-19,coronavirus transmission,low-income countries,sars-cov-2,wastewater reuse

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