SARS-CoV-2–Positive Sputum and Feces After Conversion of Pharyngeal Samples in Patients With COVID-19

Abstract

Letters30 March 2020SARS-CoV-2–Positive Sputum and Feces After Conversion of Pharyngeal Samples in Patients With COVID-19FREEChen Chen, PhD, Guiju Gao, MD, Yanli Xu, MD, Lin Pu, MD, Qi Wang, MD, Liming Wang, PhD, Wenling Wang, PhD, Yangzi Song, MS, Meiling Chen, MS, Linghang Wang, MD, PhD, Fengting Yu, MS, Siyuan Yang, MS, Yunxia Tang, PhD, Li Zhao, PhD, Huijuan Wang, PhD, Yajie Wang, PhD, Hui Zeng, MD, PhD, and Fujie Zhang, MD, PhDChen Chen, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Guiju Gao, MDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Yanli Xu, MDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Lin Pu, MDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Qi Wang, MDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Liming Wang, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Wenling Wang, PhDNHC Key Laboratory, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China (W.W., L.Z., H.W.), Yangzi Song, MSBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Meiling Chen, MSBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Linghang Wang, MD, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Fengting Yu, MSBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Siyuan Yang, MSBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Yunxia Tang, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Li Zhao, PhDNHC Key Laboratory, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China (W.W., L.Z., H.W.), Huijuan Wang, PhDNHC Key Laboratory, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China (W.W., L.Z., H.W.), Yajie Wang, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), Hui Zeng, MD, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.), and Fujie Zhang, MD, PhDBeijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., F.Z.)Author, Article, and Disclosure Informationhttps://doi.org/10.7326/M20-0991 SectionsAboutVisual AbstractPDF ToolsAdd to favoritesDownload CitationsTrack CitationsPermissions ShareFacebookTwitterLinkedInRedditEmail Background: The outbreak of coronavirus disease 2019 (COVID-19) has become a global public health problem. In the absence of a specific therapy or vaccine, timely diagnosis and the establishment of a sufficient isolation period for infected individuals are critical to containment efforts. Real-time quantitative fluorescence polymerase chain reaction (RT-qPCR) testing of respiratory specimens for SARS-CoV-2 RNA is currently used for case diagnosis and to guide the duration of patient isolation or hospital discharge (1). Specimens that are positive on RT-qPCR have, however, also been reported from blood (2), feces (3), and urine (4). Whether testing of multiple body sites is important when considering patient isolation has not been thoroughly studied.Objective: To assess the results of RT-qPCR for SARS-CoV-2 RNA of sputum and fecal samples from a group of patients after conversion of their pharyngeal samples from positive to negative.Methods and Findings: We retrospectively identified a convenience sample of patients admitted to Beijing Ditan Hospital, Capital Medical University, with a diagnosis of COVID-19 and paired RT-qPCR testing of pharyngeal swabs with either sputum or feces samples. A diagnosis of COVID-19 required at least 2 RT-qPCR–positive pharyngeal swabs, and patients underwent treatments as well as initial and follow-up testing of pharyngeal, sputum, or fecal samples at the discretion of treating clinicians. Hospital discharge required meeting 4 criteria: afebrile for more than 3 days, resolution of respiratory symptoms, substantial improvement of chest computed tomographic findings, and 2 consecutive negative RT-qPCR tests for SARS-CoV-2 in respiratory samples obtained at least 24 hours apart (1). We report the findings of patients with at least 1 initial or follow-up RT-qPCR positive sputum or fecal sample obtained within 24 hours of a follow-up negative RT-qPCR pharyngeal sample. The RT-qPCR assay targeted the open reading frame 1ab (ORF1ab) region and nucleoprotein (N) gene with a negative control. A cycle threshold value of 37 or less was interpreted as positive for SARS-CoV-2, according to Chinese national guidelines.Among 133 patients admitted with COVID-19 from 20 January to 27 February 2020, we identified 22 with an initial or follow-up positive sputum or fecal sample paired with a follow-up negative pharyngeal sample. Of these patients, 18 were aged 15 to 65 years, and 4 were children; 14 were male; and 11 had a history of either travel to or exposure to an individual returning from Hubei Province in the past month. Fever was the most common initial onset symptom. Five patients had at least 1 preexisting medical condition (Table). All patients met criteria and were discharged from the hospital.Table. Characteristics of 22 Patients With Confirmed COVID-19 Who Had a Positive RT-qPCR Result for SARS-CoV-2 in Fecal and/or Sputum Samples After a Negative RT-qPCR Result on Pharyngeal SwabWe collected 545 specimens from 22 patients, including 209 pharyngeal swabs, 262 sputum samples, and 74 feces samples (Figure). In these patients, sputum and feces remained positive for SARS-CoV-2 on RT-qPCR up to 39 and 13 days, respectively, after the obtained pharyngeal samples were negative.Figure. Results of nucleic acid testing in 22 patients with confirmed COVID-19 infection, by timing of symptom onset.Infection was confirmed by RT-qPCR assay of pharyngeal swabs, sputum samples, and feces samples. Day 0 is the day of symptom onset for each patient. Patient 2 had RT-qPCR positive sputum samples after negative pharyngeal samples (although not paired within 24 hours); he was discharged from the hospital on the basis of sequential negative samples. N = negative; NA = not available; P = positive; RT-qPCR = real-time quantitative fluorescence polymerase chain reaction. Download figure Download PowerPoint Discussion: Pharyngeal swabs are widely used to determine the appropriateness of a patient's discharge from the hospital and whether isolation continues to be required. We observed 22 patients who had positive RT-qPCR results for SARS-CoV-2 in the sputum or feces after pharyngeal swabs became negative. These findings raise concern about whether patients with negative pharyngeal swabs are truly virus-free, or sampling of additional body sites is needed. It is important to emphasize, however, that it is not known whether the positive RT-qPCR results for SARS-CoV-2 observed here indicate that a patient continues to pose a risk for infection to others. Related, positive throat samples (after negative samples) after hospital discharge have been reported (5).Limitations of our study are that it is based on a convenience sample and that serial samples were not obtained from each patient on a defined schedule. These results warrant further study, including the systematic and simultaneous collection of samples from multiple body sites and evaluation of infectious risk.References1. China National Health Commission. Chinese Clinical Guidance For COVID-19 Pneumonia Diagnosis and Treatment. 7th ed. 4 March 2020. Accessed at http://kjfy.meetingchina.org/msite/news/show/cn/3337.html on 22 March 2020. Google Scholar2. Huang C, Wang Y, Li X, et al. 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 CrossrefMedlineGoogle Scholar3. Wang W, Xu Y, Gao R, et al. Detection of SARS-CoV-2 in different types of clinical specimens. JAMA. 2020. [PMID: 32159775] doi:10.1001/jama.2020.3786 CrossrefMedlineGoogle Scholar4. Wang L, Li X, Chen H, et al. SARS-CoV-2 infection does not significantly cause acute renal injury: an analysis of 116 hospitalized patients with COVID-19 in a single hospital, Wuhan, China. medRxiv. 27 February 2020. Accessed at www.medrxiv.org/content/10.1101/2020.02.19.20025288v1 on 24 March 2020. Google Scholar5. Lan L, Xu D, Ye G, et al. Positive RT-PCR test results in patients recovered from COVID-19. JAMA. 2020. [PMID: 32105304] doi:10.1001/jama.2020.2783 CrossrefMedlineGoogle Scholar Comments 0 Comments Sign In to Submit A Comment Neelesh GuptaUniversity of South Alabama Medical Center, Mobile, AL, USA1 April 2020 What about transmission Good to peruse this erudite study. The infectivity of sputum is of concern if the infection is air-borne like tuberculosis, and infectivity of stool is of concern only if the COVID-19 virus is not destroyed by gastric juices. Could authors shed light on these important issues. Disclosures: Nil Richard M Fleming, PhD, MD, JD (FHHI-OI-Camelot); Matthew R Fleming, BS, NRP (FHHI-OI-Camelot); Tapan K Chaudhuri, MD (Eastern Virginia Medical School)FHHI-OI-Camelot; Eastern Virginia Medical School31 March 2020 CoVid-19 Pneumonia Deaths - Exactly as defined - It's time to get serious about this! The deaths associated with CoVid-19 are exactly as we have previously defined and warned about [1].The inflammatory reaction precipitated by viruses - worsening coronary artery disease (CAD), cancer, and other chronic inflammatory diseases - was originally laid out in the mid-1990s, published in a Cardiology Textbook in 1999 [2] and later detailed on 20/20 [3] in 2004.The inflammatory changes, which occur within tissue can and must be measured to determine the severity of CoVid-19 pneumonia (CVP). FMTVDM must also be used if we are to measure the success or failure of proposed treatments for CVP [4-6] - directing individual patient treatment; saving time, money, resources and lives.You need only ask yourself if guessing is good enough [7] or should we be measuring treatment outcomes? Simply ask yourself, what would you want if the patient with CVP on a ventilator in a hospital were your friend or someone you loved?References:1. Fleming RM, Fleming MR, Chaudhuri TK. Hope and knowledge, after all, is very contagious – more contagious than this virus. 18 March 2020. BMJ 2020;368:m1087. https://www.bmj.com/content/368/bmj.m1087/rr 2. Fleming RM. Chapter 64. The Pathogenesis of Vascular Disease. Textbook of Angiology. John C. Chang Editor, Springer-Verlag New York, NY. 1999, pp. 787-798. doi:10.1007/978-1-4612-1190-7_64. 3. "Hidden Heart Disease. Could a simple, inexpensive test save your life?" 20/20 - ABC Network with Barbara Walters and Dr. Timothy Johnson 16 April 2004. https://www.youtube.com/watch?v=Hvb_Ced7KyA&t=22s 4. The Fleming Method for Tissue and Vascular Differentiation and Metabolism (FMTVDM) using same state single or sequential quantification comparisons. Patent Number 9566037. Issued 02/14/2017. 5. Mahase Elisabeth. Covid-19: what treatments are being investigated? BMJ 2020; 368:m1252 6. Sayburn Anna. Covid-19: trials of four potential treatments to generate "robust data" of what works BMJ 2020; 368 :m1206 7. Fleming RM, Fleming MR, Dooley WC, Chaudhuri TK. Invited Editorial. The Importance of Differentiating Between Qualitative, Semi-Quantitative and Quantitative Imaging – Close Only Counts in Horseshoes. Eur J Nucl Med Mol Imaging. 2020;47(4):753-755. DOI:10.1007/s00259-019-04668-y. Published online 17 January 2020 https://link.springer.com/article/10.1007/s00259-019- 04668-y https://rdcu.be/b22Dd Disclosures: FMTVDM issued to first author. Sheila Nguyen, MD(1), Srinivas R Vunnam, MD(2), Wallace H Greene, PhD(3), Rama Vunnam, MD(1)(1) Penn State Health Milton S. Hershey Medical Center, (2) University of Nebraska Medical Center, (3) Penn State College of Medicine14 July 2020 Time to advocate for Stool testing in hospitalized COVID-19 patients To the Editor: Dr. Chen and colleagues1 published on the detection of SARS-CoV-2 in the sputum or feces up to 39 and 13 days, respectively, after pharyngeal swabs became negative. This finding adds to growing evidence of prolonged viral shedding beyond the recommended isolation period for patients. To better understand fecal-oral and fecal-respiratory routes of transmission and to improve infection control strategies, we believe it's time to time to advocate for Stool testing in hospitalized COVID-19 patients. Existing data report increased prevalence of GI symptoms up to 12% of COVID-19 patients, with viral shedding observed in 40.5% of all patients2 . In a systematic review by Cheung et al., fecal viral shedding was reported in 70.3% of patients after respiratory specimens became negative3. Xiao et al. were able to isolate the SARS-CoV-2 virus from feces on two viral-RNA-positive patients, and the authors were able to show that the isolated virus was infectious to susceptible cells and could be neutralized by antibodies when the sample is exposed to the patient's serum4. This result may suggest evidence of fecal-oral transmission or fecal-respiratory transmission through aerosolized feces. Furthermore, on April 9, 2020 Food and Drug Administration (FDA) released a safety alert on the potential risk of transmission of SARS-CoV-2 by fecal microbiota for transplantation (FMT)5. Up-to-date isolation guidelines may be inadequate to mitigate the spread of infection in both clinical and community settings and thus we want to emphasize the following points: Despite the increased prevalence of GI symptoms and evolving evidence that prolonged viral shedding, to date, there is no FDA validated emergency use authorization (EUA) stool testing. Since the updated data on the increasing prevalence of GI symptoms, there has been no updated guideline from the Center for Disease Control (CDC), WHO or Gastroenterology societies on contact isolation for those patients with GI manifestations. Based on current data, we urge for the expansion of our testing of viral RNA detection to stool samples to understand viral shedding dynamics better. As hospitalists we recognize the limitations of current testing capabilities, feasibility to perform stool testing in all COVID-19 patients. However, a rigorous approach, such as stool testing in addition to nasopharyngeal swab testing to confirm disease recovery, may have implications, especially in moderate and severe covid-19 patients require hospitalization. Hospitalized patients who require gastrointestinal interventions, intraabdominal surgical procedures, and care transition, discharging patients to long term or short term health facilities. REFERENCES: Chen C, Gao G, Xu Y, et al. SARS-CoV-2-Positive Sputum and Feces After Conversion of Pharyngeal Samples in Patients With COVID-19. Annals of internal medicine. 2020;172(12):832-834. Parasa S, Desai M, Thoguluva Chandrasekar V, et al. Prevalence of Gastrointestinal Symptoms and Fecal Viral Shedding in Patients With Coronavirus Disease 2019: A Systematic Review and Meta-analysis. JAMA Network Open. 2020;3(6):e2011335-e2011335. Cheung KS, Hung IFN, Chan PPY, et al. Gastrointestinal Manifestations of SARS-CoV-2 Infection and Virus Load in Fecal Samples From a Hong Kong Cohort: Systematic Review and Meta-analysis. Gastroenterology. 2020. Xiao F, Sun J, Xu Y, et al. Infectious SARS-CoV-2 in Feces of Patient with Severe COVID-19. Emerg Infect Dis. 2020;26(8). Administration USFD. Information Pertaining to Additional Safety Protections Regarding Use of Fecal Microbiota for Transplantation - Screening Donors for COVID-19 and Exposure to SARS-CoV-2 and Testing for SARS-CoV-2. 2020, April 09; https://www.fda.gov/vaccines-blood-biologics/safety-availability-biologics/safety-alert-regarding-use-fecal-microbiota-transplantation-and-additional-safety-protections. Disclosures: NA Chen Chen, PhD, Liming Wang, PhD, Pengcheng Du, PhD, Hui Zeng, MD, Fujie Zhang, MDInstitute of Infectious Diseases, Beijing Ditan Hospital, Capital Medical University, Beijing27 July 2020 Time to advocate for stool testing in hospitalized COVID-19 patients. Thank you for your comments and continuous interest in our study. In addition to our observation on the positive test of SARS-CoV-2 in feces, authors noticed that the virus was isolated from feces and present as a high prevalence 1. Thus, it is important to understand the fecal-oral and fecal respiratory routes of transmission. Currently, the commonly recognized transmission route of COVID-19 is through droplets by airway breathing and close contact via contaminated hands2. Several recent outbreaks provided the contaminant food may also cause the infection, especially the reemergence of SARS-CoV-2 in Beijings Xinfadi Wholesale Market after 56 days silent of the virus3. Sparking concern that salmon could be contaminated with the deadly virus, and whether SARS-CoV-2 could from to is These the potential risk of fecal-oral and fecal-respiratory routes in addition to respiratory route of SARS-CoV-2. is evidence to the fecal-oral or fecal-respiratory transmission data of of SARS-CoV-2 in feces has been In our hospital, of the in the of SARS-CoV-2 in feces is not However, there are increasing GI patients infected with COVID-19 especially those who to be negative in pharyngeal swabs that the SARS-CoV-2 in not only to the also to the other of respiratory and gastrointestinal In our recent study two SARS-CoV-2 types in to different The further of SARS-CoV-2 in gastrointestinal and respiratory should be These of virus important for virus to the different We it is time to more on of evidence to the establishment of other transmission route other than respiratory transmission. current evidence of fecal-oral or fecal-respiratory is to either for the of disease or for the of the REFERENCES: Parasa S, Desai M, Thoguluva Chandrasekar V, et al. Prevalence of Gastrointestinal Symptoms and Fecal Viral Shedding in Patients With Coronavirus Disease 2019: A Systematic Review and Meta-analysis. JAMA Network Open. 2020; R, Li Y, AL, Wang Y, et al. transmission as the route for the spread of COVID-19. of the National of 2020; D, D, et al. Coronavirus disease 2019 (COVID-19) serious with and 2020. Zhao, et al. of COVID-19 Xinfadi Beijing China 2020, Xiao F, M, X, Li C, for gastrointestinal infection of SARS-CoV-2. Gastroenterology. 2020; Article, and Disclosure Chen Chen, Guiju Gao, Yanli Xu, Lin Pu, Qi Wang, Liming Wang, Wenling Wang, Yangzi Song, Meiling Chen, Linghang Wang, MD, Fengting Yu, Siyuan Yang, Yunxia Tang, Li Zhao, Huijuan Wang, Yajie Wang, Hui Zeng, MD, Fujie Zhang, MD, Beijing Ditan Hospital, Capital Medical University, and Beijing Key Laboratory of Emerging Infectious Diseases, Beijing, China (C.C., G.G., Y.X., L.P., Q.W., L.W., Y.S., M.C., L.W., F.Y., S.Y., Y.T., Y.W., H.Z., Key Laboratory, National Institute for Viral Disease Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China (W.W., L.Z., with an C. 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