Заболевания желудочно-кишечного тракта в контексте инфекции COVID-19

1. Янушевич О.О., Маев И.В., Крихели Н.И., и др. Распространенность и прогностическое значение гастроэнтерологических проявлений COVID-19: данные Российской университетской клиники. Терапевтический архив. 2021;93(8):853-61 [Ianushevich OO, Maev IV, Krikheli NI, et al. Prevalence and prognostic value of gastroenterological manifestations of COVID-19: data from the Russian University Clinic. Terapevticheskii Arkhiv (Ter. Arkh.). 2021;93(8):853‑61 (in Russian)]. DOI:10.26442/00403660.2021.08.200977
2. Holshue ML, DeBolt C, Lindquist S, et al. First Case of 2019 Novel Coronavirus in the United States. N Engl J Med. 2020;382(10):929-36. DOI:10.1056/NEJMoa2001191
3. Fang D, Ma JD, Guan JL, et al. A single-center, descriptive study on the digestive system of COVID-19 inpatients in wuhan. Zhonghua Xiaohua Zazhi. 2020;40:E005. 
4. Docherty AB, Harrison EM, Green CA, et al. Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study. BMJ. 2020;369:m1985. DOI:10.1136/bmj.m1985
5. Jones DL, Baluja MQ, Graham DW, et al. Shedding of SARS-CoV-2 in feces and urine and its potential role in person-to-person transmission and the environment-based spread of COVID-19. Sci Total Environ. 2020;749:141364. DOI:10.1016/j.scitotenv.2020.141364
6. Lin L, Jiang X, Zhang Z, et al. Gastrointestinal symptoms of 95 cases with SARS-CoV-2 infection. Gut. 2020;69(6):997-1001. DOI:10.1136/gutjnl-2020-321013
7. Chai X, Hu L, Zhang Y, et al. Specific ACE2 Expression in Cholangiocytes May Cause Liver Damage After 2019-nCoV Infection. BioRxiv.org. 2020:2020.02.03.931766. DOI:10.1101/2020.02.03.931766
8. Lin L, Lu L, Cao W, Li T. Hypothesis for potential pathogenesis of SARS-CoV-2 infection – a review of immune changes in patients with viral pneumonia. Emerg Microbes Infect. 2020;9(1):727-32. DOI:10.1080/22221751.2020.1746199
9. Wang D, Hu B, Hu C, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA. 2020;323(11):1061-9. DOI:10.1001/jama.2020.1585
10. Han C, Duan C, Zhang S, et al. Digestive Symptoms in COVID-19 Patients With Mild Disease Severity: Clinical Presentation, Stool Viral RNA Testing, and Outcomes. Am J Gastroenterol. 2020;115(6):916-23. DOI:10.14309/ajg.0000000000000664
11. Esposito G, Pesce M, Seguella L, et al. Can the enteric nervous system be an alternative entrance door in SARS-CoV-2 neuroinvasion? Brain Behav Immun. 2020;87:93-4. DOI:10.1016/j.bbi.2020.04.060
12. Fang D, Ma J, Guan J, et al. Manifestations of Digestive system in hospitalized patients with novel coronavirus pneumonia in Wuhan, China: a single-center, descriptive study. Chinese Journal of Digestion. 2020:E005. 
13. Gu J, Han B, Wang J. COVID-19: Gastrointestinal Manifestations and Potential Fecal-Oral Transmission. Gastroenterology. 2020;158(6):1518-9. DOI:10.1053/j.gastro.2020.02.054
14. Luo S, Zhang X, Xu H. Don’t Overlook Digestive Symptoms in Patients With 2019 Novel Coronavirus Disease (COVID-19). Clin Gastroenterol Hepatol. 2020;18(7):1636-7. DOI:10.1016/j.cgh.2020.03.043
15. Zhang FC, Yin ZB, Tang XP. Clinical analysis of 260 cases of SARS in Guangzhou. Zhonghua Chuanranbing Zazhi. 2003;21:84-8. 
16. Gao QY, Chen YX, Fang JY. 2019 Novel coronavirus infection and gastrointestinal tract. J Dig Dis. 2020;21(3):125-6. DOI:10.1111/1751-2980.12851
17. Price E. Could the severity of COVID-19 be increased by low gastric acidity? Crit Care. 2020;24(1):456. DOI:10.1186/s13054-020-03182-0
18. Hunt RH, East JE, Lanas A, et al. COVID-19 and Gastrointestinal Disease: Implications for the Gastroenterologist. Dig Dis. 2021;39(2):119-39. DOI:10.1159/000512152
19. Manolis AS, Manolis TA, Manolis AA, et al. COVID-19 Infection: Viral Macro- and Micro-Vascular Coagulopathy and Thromboembolism/Prophylactic and Therapeutic Management. J Cardiovasc Pharmacol Ther. 2021;26(1):12-24. DOI:10.1177/1074248420958973
20. Sultan S, Altayar O, Siddique SM, et al. AGA Institute Rapid Review of the Gastrointestinal and Liver Manifestations of COVID-19, Meta-Analysis of International Data, and Recommendations for the Consultative Management of Patients with COVID-19. Gastroenterology. 2020;159(1):320-34.e27. DOI:10.1053/j.gastro.2020.05.001
21. Norsa L, Indriolo A, Sansotta N, et al. Uneventful Course in Patients With Inflammatory Bowel Disease During the Severe Acute Respiratory Syndrome Coronavirus 2 Outbreak in Northern Italy. Gastroenterology. 2020;159(1):371-2. DOI:10.1053/j.gastro.2020.03.062
22. Cheung S, Quiwa JC, Pillai A, et al. Superior Mesenteric Artery Thrombosis and Acute Intestinal Ischemia as a Consequence of COVID-19 Infection. Am J Case Rep. 2020;21:e925753. DOI:10.12659/AJCR.925753
23. Keshavarz P, Rafiee F, Kavandi H, et al. Ischemic gastrointestinal complications of COVID-19: a systematic review on imaging presentation. Clin Imaging. 2021;73:86-95. DOI:10.1016/j.clinimag.2020.11.054
24. Singh B, Kaur P. COVID-19 and acute mesenteric ischemia: A review of literature. Hematol Transfus Cell Ther. 2021;43(1):112-6. DOI:10.1016/j.htct.2020.10.959
25. Theoharides TC. COVID-19, pulmonary mast cells, cytokine storms, and beneficial actions of luteolin. Biofactors. 2020;46(3):306-8. DOI:10.1002/biof.1633
26. Gu S, Chen Y, Wu Z, et al. Alterations of the Gut Microbiota in Patients With Coronavirus Disease 2019 or H1N1 Influenza. Clin Infect Dis. 2020;71(10):2669‑78. DOI:10.1093/cid/ciaa709
27. Domínguez-Díaz C, García-Orozco A, Riera-Leal A, et al. Microbiota and Its Role on Viral Evasion: Is It With Us or Against Us? Front Cell Infect Microbiol. 2019;9:256. DOI:10.3389/fcimb.2019.00256
28. Huang Y, Mao K, Chen X, et al. S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense. Science. 2018;359(6371):114-9. DOI:10.1126/science.aam5809
29. McAleer JP, Kolls JK. Contributions of the intestinal microbiome in lung immunity. Eur J Immunol. 2018;48(1):39-49. DOI:10.1002/eji.201646721
30. World Health Organization. A clinical case definition of post COVID-19 condition by a Delphi consensus, 6 October 2021. Available at: https://apps.who.int/iris/bitstream/handle/10665/345824/WHO-2019-nCoV-Post-COVID-19-condition-Clinic.... Accessed: 26.02.2021.
31. COVID-19 rapid guideline: managing the long-term effects of COVID-19 NICE guideline [NG188] Published: 18 December 2020. Last updated: 11 November 2021. Available at: https://www.nice.org.uk/guidance/NG188. Accessed: 26.02.2021.
32. Mahmoud MH, Alghamdi FA, Alghamdi GA, et al. Study of Post-COVID-19 Syndrome in Saudi Arabia. Cureus. 2021;13(9):e17787. DOI:10.7759/cureus.17787
33. Petersen MS, Kristiansen MF, Hanusson KD, et al. Long COVID in the Faroe Islands: A Longitudinal Study Among Nonhospitalized Patients. Clin Infect Dis. 2021;73(11):e4058-63. DOI:10.1093/cid/ciaa1792
34. Yong SJ. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53(10):737-54. 
DOI:10.1080/23744235.2021.1924397
35. DosSantos MF, Devalle S, Aran V, et al. Neuromechanisms of SARS-CoV-2: A Review. Front Neuroanat. 2020;14:37. DOI:10.3389/fnana.2020.00037
36. Varatharaj A, Thomas N, Ellul MA, et al. Neurological and neuropsychiatric complications of COVID-19 in 153 patients: a UK-wide surveillance study. Lancet Psychiatry. 2020;7(10):875-82. DOI:10.1016/S2215-0366(20)30287-X
37. Ghoshal UC, Ghoshal U, Rahman MM, et al. Post-infection functional gastrointestinal disorders following coronavirus disease-19: A case-control study. J Gastroenterol Hepatol. 2021. DOI:10.1111/jgh.15717
38. Schmulson M, Ghoshal UC, Barbara G. Managing the Inevitable Surge of Post-COVID-19 Functional Gastrointestinal Disorders. Am J Gastroenterol. 2021;116(1):4-7. DOI:10.14309/ajg.0000000000001062
39. Ghoshal UC, Rahman MM. Post-infection irritable bowel syndrome in the tropical and subtropical regions: Vibrio cholerae is a new cause of this well-known condition. Indian J Gastroenterol. 2019;38(2):87-94. DOI:10.1007/s12664-019-00959-2
40. Huang C, Huang L, Wang Y, et al. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet. 2021;397(10270):220-32.
DOI:10.1016/S0140-6736(20)32656-8
41. Weng J, Li Y, Li J, et al. Gastrointestinal sequelae 90 days after discharge for COVID-19. Lancet Gastroenterol Hepatol. 2021;6(5):344-6. DOI:10.1016/S2468-1253(21)00076-5
42. Noviello D, Costantino A, Muscatello A, et al. Functional gastrointestinal and somatoform symptoms five months after SARS-CoV-2 infection: A controlled cohort study. Neurogastroenterol Motil. 2022;34(2):e14187. DOI:10.1111/nmo.14187
43. Marshall JK, Thabane M, Borgaonkar MR, James C. Postinfectious irritable bowel syndrome after a food-borne outbreak of acute gastroenteritis attributed to a viral pathogen. Clin Gastroenterol Hepatol. 2007;5(4):457-60. DOI:10.1016/j.cgh.2006.11.025
44. Zanini B, Ricci C, Bandera F, et al. Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am J Gastroenterol. 2012;107(6):891-9. DOI:10.1038/ajg.2012.102

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1. Ianushevich OO, Maev IV, Krikheli NI, et al. Prevalence and prognostic value of gastroenterological manifestations of COVID-19: data from the Russian University Clinic. Terapevticheskii Arkhiv (Ter. Arkh.). 2021;93(8):853‑61 (in Russian). DOI:10.26442/00403660.2021.08.200977
2. Holshue ML, DeBolt C, Lindquist S, et al. First Case of 2019 Novel Coronavirus in the United States. N Engl J Med. 2020;382(10):929-36. DOI:10.1056/NEJMoa2001191
3. Fang D, Ma JD, Guan JL, et al. A single-center, descriptive study on the digestive system of COVID-19 inpatients in wuhan. Zhonghua Xiaohua Zazhi. 2020;40:E005. 
4. Docherty AB, Harrison EM, Green CA, et al. Features of 20 133 UK patients in hospital with covid-19 using the ISARIC WHO Clinical Characterisation Protocol: prospective observational cohort study. BMJ. 2020;369:m1985. DOI:10.1136/bmj.m1985
5. Jones DL, Baluja MQ, Graham DW, et al. Shedding of SARS-CoV-2 in feces and urine and its potential role in person-to-person transmission and the environment-based spread of COVID-19. Sci Total Environ. 2020;749:141364. DOI:10.1016/j.scitotenv.2020.141364
6. Lin L, Jiang X, Zhang Z, et al. Gastrointestinal symptoms of 95 cases with SARS-CoV-2 infection. Gut. 2020;69(6):997-1001. DOI:10.1136/gutjnl-2020-321013
7. Chai X, Hu L, Zhang Y, et al. Specific ACE2 Expression in Cholangiocytes May Cause Liver Damage After 2019-nCoV Infection. BioRxiv.org. 2020:2020.02.03.931766. DOI:10.1101/2020.02.03.931766
8. Lin L, Lu L, Cao W, Li T. Hypothesis for potential pathogenesis of SARS-CoV-2 infection – a review of immune changes in patients with viral pneumonia. Emerg Microbes Infect. 2020;9(1):727-32. DOI:10.1080/22221751.2020.1746199
9. Wang D, Hu B, Hu C, et al. Clinical Characteristics of 138 Hospitalized Patients With 2019 Novel Coronavirus-Infected Pneumonia in Wuhan, China. JAMA. 2020;323(11):1061-9. DOI:10.1001/jama.2020.1585
10. Han C, Duan C, Zhang S, et al. Digestive Symptoms in COVID-19 Patients With Mild Disease Severity: Clinical Presentation, Stool Viral RNA Testing, and Outcomes. Am J Gastroenterol. 2020;115(6):916-23. DOI:10.14309/ajg.0000000000000664
11. Esposito G, Pesce M, Seguella L, et al. Can the enteric nervous system be an alternative entrance door in SARS-CoV-2 neuroinvasion? Brain Behav Immun. 2020;87:93-4. DOI:10.1016/j.bbi.2020.04.060
12. Fang D, Ma J, Guan J, et al. Manifestations of Digestive system in hospitalized patients with novel coronavirus pneumonia in Wuhan, China: a single-center, descriptive study. Chinese Journal of Digestion. 2020:E005. 
13. Gu J, Han B, Wang J. COVID-19: Gastrointestinal Manifestations and Potential Fecal-Oral Transmission. Gastroenterology. 2020;158(6):1518-9. DOI:10.1053/j.gastro.2020.02.054
14. Luo S, Zhang X, Xu H. Don’t Overlook Digestive Symptoms in Patients With 2019 Novel Coronavirus Disease (COVID-19). Clin Gastroenterol Hepatol. 2020;18(7):1636-7. DOI:10.1016/j.cgh.2020.03.043
15. Zhang FC, Yin ZB, Tang XP. Clinical analysis of 260 cases of SARS in Guangzhou. Zhonghua Chuanranbing Zazhi. 2003;21:84-8. 
16. Gao QY, Chen YX, Fang JY. 2019 Novel coronavirus infection and gastrointestinal tract. J Dig Dis. 2020;21(3):125-6. DOI:10.1111/1751-2980.12851
17. Price E. Could the severity of COVID-19 be increased by low gastric acidity? Crit Care. 2020;24(1):456. DOI:10.1186/s13054-020-03182-0
18. Hunt RH, East JE, Lanas A, et al. COVID-19 and Gastrointestinal Disease: Implications for the Gastroenterologist. Dig Dis. 2021;39(2):119-39. DOI:10.1159/000512152
19. Manolis AS, Manolis TA, Manolis AA, et al. COVID-19 Infection: Viral Macro- and Micro-Vascular Coagulopathy and Thromboembolism/Prophylactic and Therapeutic Management. J Cardiovasc Pharmacol Ther. 2021;26(1):12-24. DOI:10.1177/1074248420958973
20. Sultan S, Altayar O, Siddique SM, et al. AGA Institute Rapid Review of the Gastrointestinal and Liver Manifestations of COVID-19, Meta-Analysis of International Data, and Recommendations for the Consultative Management of Patients with COVID-19. Gastroenterology. 2020;159(1):320-34.e27. DOI:10.1053/j.gastro.2020.05.001
21. Norsa L, Indriolo A, Sansotta N, et al. Uneventful Course in Patients With Inflammatory Bowel Disease During the Severe Acute Respiratory Syndrome Coronavirus 2 Outbreak in Northern Italy. Gastroenterology. 2020;159(1):371-2. DOI:10.1053/j.gastro.2020.03.062
22. Cheung S, Quiwa JC, Pillai A, et al. Superior Mesenteric Artery Thrombosis and Acute Intestinal Ischemia as a Consequence of COVID-19 Infection. Am J Case Rep. 2020;21:e925753. DOI:10.12659/AJCR.925753
23. Keshavarz P, Rafiee F, Kavandi H, et al. Ischemic gastrointestinal complications of COVID-19: a systematic review on imaging presentation. Clin Imaging. 2021;73:86-95. DOI:10.1016/j.clinimag.2020.11.054
24. Singh B, Kaur P. COVID-19 and acute mesenteric ischemia: A review of literature. Hematol Transfus Cell Ther. 2021;43(1):112-6. DOI:10.1016/j.htct.2020.10.959
25. Theoharides TC. COVID-19, pulmonary mast cells, cytokine storms, and beneficial actions of luteolin. Biofactors. 2020;46(3):306-8. DOI:10.1002/biof.1633
26. Gu S, Chen Y, Wu Z, et al. Alterations of the Gut Microbiota in Patients With Coronavirus Disease 2019 or H1N1 Influenza. Clin Infect Dis. 2020;71(10):2669‑78. DOI:10.1093/cid/ciaa709
27. Domínguez-Díaz C, García-Orozco A, Riera-Leal A, et al. Microbiota and Its Role on Viral Evasion: Is It With Us or Against Us? Front Cell Infect Microbiol. 2019;9:256. DOI:10.3389/fcimb.2019.00256
28. Huang Y, Mao K, Chen X, et al. S1P-dependent interorgan trafficking of group 2 innate lymphoid cells supports host defense. Science. 2018;359(6371):114-9. DOI:10.1126/science.aam5809
29. McAleer JP, Kolls JK. Contributions of the intestinal microbiome in lung immunity. Eur J Immunol. 2018;48(1):39-49. DOI:10.1002/eji.201646721
30. World Health Organization. A clinical case definition of post COVID-19 condition by a Delphi consensus, 6 October 2021. Available at: https://apps.who.int/iris/bitstream/handle/10665/345824/WHO-2019-nCoV-Post-COVID-19-condition-Clinic.... Accessed: 26.02.2021.
31. COVID-19 rapid guideline: managing the long-term effects of COVID-19 NICE guideline [NG188] Published: 18 December 2020. Last updated: 11 November 2021. Available at: https://www.nice.org.uk/guidance/NG188. Accessed: 26.02.2021.
32. Mahmoud MH, Alghamdi FA, Alghamdi GA, et al. Study of Post-COVID-19 Syndrome in Saudi Arabia. Cureus. 2021;13(9):e17787. DOI:10.7759/cureus.17787
33. Petersen MS, Kristiansen MF, Hanusson KD, et al. Long COVID in the Faroe Islands: A Longitudinal Study Among Nonhospitalized Patients. Clin Infect Dis. 2021;73(11):e4058-63. DOI:10.1093/cid/ciaa1792
34. Yong SJ. Long COVID or post-COVID-19 syndrome: putative pathophysiology, risk factors, and treatments. Infect Dis (Lond). 2021;53(10):737-54. 
DOI:10.1080/23744235.2021.1924397
35. DosSantos MF, Devalle S, Aran V, et al. Neuromechanisms of SARS-CoV-2: A Review. Front Neuroanat. 2020;14:37. DOI:10.3389/fnana.2020.00037
36. Varatharaj A, Thomas N, Ellul MA, et al. Neurological and neuropsychiatric complications of COVID-19 in 153 patients: a UK-wide surveillance study. Lancet Psychiatry. 2020;7(10):875-82. DOI:10.1016/S2215-0366(20)30287-X
37. Ghoshal UC, Ghoshal U, Rahman MM, et al. Post-infection functional gastrointestinal disorders following coronavirus disease-19: A case-control study. J Gastroenterol Hepatol. 2021. DOI:10.1111/jgh.15717
38. Schmulson M, Ghoshal UC, Barbara G. Managing the Inevitable Surge of Post-COVID-19 Functional Gastrointestinal Disorders. Am J Gastroenterol. 2021;116(1):4-7. DOI:10.14309/ajg.0000000000001062
39. Ghoshal UC, Rahman MM. Post-infection irritable bowel syndrome in the tropical and subtropical regions: Vibrio cholerae is a new cause of this well-known condition. Indian J Gastroenterol. 2019;38(2):87-94. DOI:10.1007/s12664-019-00959-2
40. Huang C, Huang L, Wang Y, et al. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet. 2021;397(10270):220-32.
DOI:10.1016/S0140-6736(20)32656-8
41. Weng J, Li Y, Li J, et al. Gastrointestinal sequelae 90 days after discharge for COVID-19. Lancet Gastroenterol Hepatol. 2021;6(5):344-6. DOI:10.1016/S2468-1253(21)00076-5
42. Noviello D, Costantino A, Muscatello A, et al. Functional gastrointestinal and somatoform symptoms five months after SARS-CoV-2 infection: A controlled cohort study. Neurogastroenterol Motil. 2022;34(2):e14187. DOI:10.1111/nmo.14187
43. Marshall JK, Thabane M, Borgaonkar MR, James C. Postinfectious irritable bowel syndrome after a food-borne outbreak of acute gastroenteritis attributed to a viral pathogen. Clin Gastroenterol Hepatol. 2007;5(4):457-60. DOI:10.1016/j.cgh.2006.11.025
44. Zanini B, Ricci C, Bandera F, et al. Incidence of post-infectious irritable bowel syndrome and functional intestinal disorders following a water-borne viral gastroenteritis outbreak. Am J Gastroenterol. 2012;107(6):891-9. DOI:10.1038/ajg.2012.102

И.В. Маев1, М.А. Осадчук*2

1 ФГБОУ ВО «Московский государственный медико-стоматологический университет им. А.И. Евдокимова» Минздрава России, Москва, Россия;
2 ФГАОУ ВО «Первый Московский государственный медицинский университет им. И.М. Сеченова» Минздрава России (Сеченовский Университет), Москва, Россия
*osadchuk.mikhail@yandex.ru

________________________________________________

Igor V. Maev1, Mikhail A. Osadchuk*2

1 Yevdokimov Moscow State University of Medicine and Dentistry, Moscow, Russia;
2 Sechenov First Moscow State Medical University (Sechenov University), Moscow, Russia
*osadchuk.mikhail@yandex.ru