References

nogr

Экспериментальная и клиническая гастроэнтерология

Experimental and Clinical Gastroenterology

1682-8658

«Global Media Technologies»

10.31146/1682-8658-ecg-202-6-41-49

nogr-2092

Research Article

КЛИНИЧЕСКАЯ ГАСТРОЭНТЕРОЛОГИЯ

CLINICAL GASTROENTEROLOGY

COVID у детей и пищеварительная система: клинико-патогенетические корреляции

COVID in children and the digestive system: clinical and pathogenetic correlation

https://orcid.org/0000-0002-5869-2893

Печкуров

Дмитрий Владимирович

Pechkurov

D. V.

dmpechkurov@yandex.ru

Романова

Анастасия Андереевна

Romanova

A. A.

noemail@neicon.ru

https://orcid.org/0000-0001-8552-1662

Тяжева

Алена Александровна

Tyazheva

A. A.

noemail@neicon.ru

https://orcid.org/0000-0002-3131-1368

Порецкова

Галина Юрьевна

Poreckova

G. Yu.

noemail@neicon.ru

ФГБОУ ВО «Самарский государственный медицинский университет Министерства здравоохранения Российской Федерации»РоссияSamara State Medical UniversityRussian Federation

2022

21112022

064149

2022

Печкуров Д.В., Романова А.А., Тяжева А.А., Порецкова Г.Ю.

Pechkurov D.V., Romanova A.A., Tyazheva A.A., Poreckova G.Y.

Данная работа распространяется под лицензией Creative Commons Attribution 4.0.

This work is licensed under a Creative Commons Attribution 4.0 License.

https://www.nogr.org/jour/article/view/2092

Новая коронавирусная инфекция может вызывать широкий спектр клинических проявлений, начиная от бессимптомной инфекции и заканчивая тяжелыми поражениями и смертью. В России на момент написания обзора зарегистрировано более 12,5 миллиона подтвержденных случаев COVID-19, почти 334 000 случаев летальных исходов. Вирус SARS-CoV-2 также обладает тропизмом к сердечно-сосудистой системе, желудочно-кишечному тракту, печени, поджелудочной железе, почкам и центральной нервной системе. В этом обзоре дана клиническая оценка и продемонстрированы патогенетические механизмы поражений желудочно-кишечного тракта при COVID-19 у детей

Coronaviruses, seven of which are known to infect humans, can range from asymptomatic infection to malnutrition and death. Russia has over 12.4 million confirmed cases of COVID-19 at the time of writing, with nearly 334,000 deaths. While all other coronaviruses affect cardiovascular disease, the SARS-CoV-2 virus also has a tropism for the cardiovascular system, gastrointestinal tract, liver, pancreas, kidneys, and nervous system. In this review, we describe the important gastrointestinal manifestations of COVID-19 in children and discuss possible underlying pathophysiological mechanisms for their occurrence.

COVID-19SARS-CoV-2желудочно-кишечные проявленияпатогенез

COVID-19SARS-CoV-2gastrointestinal manifestations

References1

World Health, Organization. Novel coronavirus (2019-nCoV): situation report, Geneva: World Health Organization; 2020. Available: https://apps.who.int/iris/handle/10665/330760 Accessed at: 2020-01-21.

Gorbalenya A. E., Baker S. C., Baric R. S., de Groot R. J., Drosten C., Gulyaeva A. A., et al. The species severe acute respiratory syndrome-related coronavirus: classifying 2019-nCoV and naming it SARS-CoV-2. NatMicrobiol. 2020;5(4):536-44. doi: 10.1038/s41564-020-0695-z.

Zhu N., Zhang D., Wang W., Li X., Yang B., Song J., et al. A novel coronavirus from patients with pneumonia in China, 2019. N Engl J Med. 2020;382(8):727-33. doi: 10.1056/NEJMoa2001017.

Goldman-Israelow B. Coronavirus replication cycle (template).BioRender.com; 2020 [cited 2020 11/01/2020]; Available from: https://app.biorender.com/biorender-templates/figures/5e99f5395fd61e0028682c01/t-5e56d97d1b689000850f8f93-coronavirus-replication-cycle. Access: 05/05/2022.

Hoffmann M., Kleine-Weber H., Schroeder S., Krüger N., Herrler T., Erichsen S., et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell. 2020 Apr 16;181(2):271-280.e8. doi: 10.1016/j.cell.2020.02.052.

vanDoorn A.S., Meijer B., Frampton C. M.A., Barclay M. L., de Boer N. K.H. Systematic Review With Meta-Analysis: SARS-CoV-2 Stool Testing and the Potential for Faecal-Oral Transmission. Aliment PharmacolTher. 2020;52:1276-88. doi: 10.1111/apt.16036.

Lin L., Jiang X., Zhang Z., Huang S., Zhang Z., Fang Z., et al. Gastrointestinal Symptoms of 95 Cases With SARS-CoV-2 Infection. Gut. 2020;69:997-1001. doi: 10.1136/gutjnl-2020-321013

Hirose R., Nakaya T., Naito Y., Daidoji T., Watanabe Y., Yasuda H., et al. Mechanism of Human Influenza Virus RNA Persistence and Virion Survival in Feces: Mucus Protects Virions From Acid and Digestive Juices. J Infect Dis (2017) 216:105-9. doi: 10.1093/infdis/jix224.

Leung W. K., To K. F., Chan P. K., Chan H. L., Wu A. K., Lee N., et al. Enteric Involvement of Severe Acute Respiratory Syndrome-Associated Coronavirus Infection. Gastroenterology (2003) 125:1011-7. doi: 10.1016/s0016-5085(03)01215-0.

Jeong H. W., Kim S. M., Kim H. S., Kim Y. I., Kim J. H., Cho J. Y., et al. Viable SARS-CoV-2 in Various Specimens From COVID-19 Patients. ClinMicrobiol Infect Off PublEurSocClinMicrobiol Infect Dis (2020) 26:1520-4. doi: 10.1016/j.cmi.2020.07.020.

Lamers M. M., Beumer J., van der Vaart J., Knoops K., Puschhof J., Breugem T. I., et al. SARS-CoV-2 Productively Infects Human Gut Enterocytes. Science (2020) 369:50-4. doi: 10.1126/science.abc1669.

Hu F., Chen F., Ou Z., Fan Q., Tan X., Wang Y., et al. A Compromised Specific Humoral Immune Response Against the SARS-CoV-2 Receptor-Binding Domain is Related to Viral Persistence and Periodic Shedding in the Gastrointestinal Tract. Cell MolImmunol (2020) 17:1119-25. doi: 10.1038/s41423-020-00550-2.

Li X-J., Zhang Z-W., Zong Z-Y. A Case of a Readmitted Patient Who Recovered From COVID-19 in Chengdu, China. Crit Care (2020) 24:152. doi: 10.1186/s13054-020-02877-8.

Kumar A., Kumari C., Faiq M. A., Pareek V., Narayan R. K. SARS-CoV-2 Infectivity Vis-A-Vis Human Gut and Mesentery: Pathogenic Implications for COVID-19. SocSci Electron Publ. doi: 10.13140/RG.2.2.34820.96644.

Donoghue M., Hsieh F., Baronas E., Godbout K., Gosselin M., Stagliano N., et al. A Novel Angiotensin-Converting Enzyme-Related Carboxypeptidase (ACE2) Converts Angiotensin I to Angiotensin 1-9. Circ Res (2000) 87: E1-9. doi: 10.1161/01.RES.87.5.e1.

Meng Y., Yu C. H., Li W., Li T., Luo W., Huang S., et al. Angiotensin-Converting Enzyme 2/Angiotensin-(1-7)/Mas Axis Protects Against Lung Fibrosis by Inhibiting the MAPK/NF-κb Pathway. Am J Respir Cell MolBiol (2014) 50:723-36.doi: 10.1165/rcmb.2012-0451OC.

Kuba K., Imai Y., Rao S., Gao H., Guo F., Guan B., et al. A Crucial Role of Angiotensin Converting Enzyme 2 (ACE2) in SARS Coronavirus-Induced Lung Injury. Nat Med (2005) 11:875-9. doi: 10.1038/nm1267.

Xiuyuan O., Yan L., Xiaobo L., Pei L., Dan M., Lili R., et al. Characterization of Spike Glycoprotein of SARS-CoV-2 on Virus Entry and its Immune Cross-Reactivity With SARS-CoV. Nat Commun (2020) 11:1620. doi: 10.1038/s41467-020-15562-9.

Conti P., Caraffa A., Gallenga C. E., Ross R., Kritas S. K., Frydas I., et al. Coronavirus-19 (SARS-CoV-2) Induces Acute Severe Lung Inflammation via IL-1 Causing Cytokine Storm in COVID-19: A Promising Inhibitory Strategy. J BiolRegulHomeost Agents (2020) 34:1971-5. doi: 10.23812/20-1-E.

Chen H., Zou T. H., Xuan B., Yan Y., Yan T., Shen C., et al. Single Cell Transcriptome Revealed SARS-CoV-2 Entry Genes Enriched in Colon Tissues and Associated With Coronavirus Infection and Cytokine Production. Signal Transduct Target Ther (2020) 5:121. doi: 10.1038/s41392-020-00237-0.

Kimura A., Kishimoto T. IL-6: Regulator of Treg/Th17 Balance. Eur J Immunol (2010) 40:1830-5. doi: 10.1002/eji.201040391.

Zhang L., Han C., Zhang S., Duan C., Shang H., Bai T., et al. Diarrhea and Altered Inflammatory Cytokine Pattern in Severe Coronavirus Disease 2019: Impact on Disease Course and in-Hospital Mortality. J GastroenterolHepatol (2020) 36(2):421-9. doi: 10.1111/jgh.15166.

Lin L, Jiang X, Zhang Z, Huang S, Zhang Z, Fang Z, et al. Gastrointestinal Symptoms of 95 Cases With SARS-CoV-2 Infection. Gut (2020) 69:997-1001. doi: 10.1136/gutjnl-2020-321013.

Wang D., Hu B., Hu C., Zhu F., Liu X., Zhang J., 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.

Broer A., Juelich T., Vanslambrouck J. M., Tietze N., Solomon P. S., Holst J., et al. Impaired Nutrient Signaling and Body Weight Control in a Na+ Neutral Amino Acid Cotransporter (Slc6a19)-Deficient Mouse. J BiolChem (2011) 286:26638-51. doi: 10.1074/jbc.M111.241323.

Nikolaus S., Schulte B., Al-Massad N., Thieme F., Schulte D. M., Bethge J., et al. Increased Tryptophan Metabolism Is Associated With Activity of Inflammatory Bowel Diseases. Gastroenterology (2017) 153:1504-16.e1502. doi: 10.1053/j.gastro.2017.08.028.

Lv L., Jiang H., Chen Y., Gu S., Xia J., Zhang H., et al. The Faecal Metabolome in COVID-19 Patients is Altered and Associated With Clinical Features and Gut Microbes. AnalyticaChimActa (2021) 1152:338267. doi: 10.1016/j.aca.2021.338267.

Andrews P. L., Cai W., Rudd J. A. COVID-19, nausea, and vomiting. Gastroenterology and Hepatology (2020):36(3)646-656. doi: 10.1111/jgh.15261.

Hagbom M., Istrate C., Engblom D., et al. Rotavirus stimulates release of serotonin (5-HT) from human enterochromaffin cells and activates brain structures involved in nausea and vomiting. PLoSPathog. 2011; 7: e1002115.

Westerberg S., Hagbom M., Rajan A., et al.Interaction of human enterochromaffin cells with human enteric adenovirus 41 leads to serotonin release and subsequent activation of enteric glia cells. J. Virol. 2018; 92: e00026- e00018.

Bialowas S., Hagbom M., Nordgren J., et al. Rotavirus and serotonin cross-talk in diarrhoea. PLoS ONE. 2016; 11: e0159660.

Li Z., Chalazonitis A., Huang Y. Y., Mann J. J., Margolis K. G., Yang Q. M., Kim D. O., Côté F., Mallet J., Gershon M. D. Essential roles of enteric neuronal serotonin in gastrointestinal motility and the development/survival of enteric dopaminergic neurons. J Neurosci. 2011;31:8998-9009.

Atkinson W., Lockhart S., Whorwell P. J., Keevil B., Houghton L. A. Altered 5-hydroxytryptamine signaling in patients with constipation- and diarrhea-predominant irritable bowel syndrome. Gastroenterology. 2006;130:34-43.

Ha S., Jin B., Clemmensen B., Park P., Mahboob S., Gladwill V., Lovely F. M., Gottfried-Blackmore A., Habtezion A., Verma S., Ro S. Serotonin is elevated in COVID-19-associated diarrhoea. Gut. 2021: epub ahead of print.

Effenberger M., Grabherr F., Mayr L., et al. Faecal calprotectin indicates intestinal inflammation in COVID-19. Gut. 2020;69:1543-1544.

Jose R.J., Manuel A. COVID-19 Cytokine Storm: The Interplay Between Inflammation and Coagulation. Lancet Respir Med (2020) 8: e46-7. doi: 10.1016/S2213-2600(20)30216-2.

Ranucci M., Ballotta A., Di Dedda U., Baryshnikova E., Dei Poli M., Resta M., et al. The Procoagulant Pattern of Patients With COVID-19 Acute Respiratory Distress Syndrome. J Thromb Haemost (2020) 18:1747-51. doi: 10.1111/jth.14854.

Pamukçu B. Inflammation and Thrombosis in Patients With COVID-19: A Prothrombotic and Inflammatory Disease Caused by SARS Coronavirus-2. Anatol J Cardiol (2020) 24:224-34. doi: 10.14744/AnatolJCardiol.2020.56727.

Liu Z., Xiao X., Wei X., Li J., Yang J., Tan H., et al.Composition and Divergence of Coronavirus Spike Proteins and Host ACE2 Receptors Predict Potential Intermediate Hosts of SARS-CoV-2. J Med Virol (2020) 92:595-601. doi: 10.1002/jmv.25726.

Leisman D.E., Deutschman C. S., Legrand M. Facing COVID-19 in the ICU: Vascular Dysfunction, Thrombosis, and Dysregulated Inflammation.Intensive Care Med (2020) 46:1105-8. doi: 10.1007/s00134-020-06059-6.

Guzik T.J., Mohiddin S. A., Dimarco A., Patel V., Savvatis K., Marelli-Berg F.M., et al. COVID-19 and the Cardiovascular System: Implications for Risk Assessment, Diagnosis, and Treatment Options. Cardiovasc Res (2020) 116:1666-87. doi: 10.1093/cvr/cvaa106.

Connors J.M, Levy JH. COVID-19 and its Implications for Thrombosis and Anticoagulation. Blood (2020) 135:2033-40. doi: 10.1182/blood.2020006000.

Mehta P., McAuley D.F., Brown M., Sanchez E., Tattersall R. S., Manson J. J., et al. COVID-19: Consider Cytokine Storm Syndromes and Immunosuppression. Lancet (2020) 395:1033-4. doi: 10.1016/S0140-6736(20)30628-0.

Wu C-Y., Yu X. P., Ma A. H.Y., Wang L. P., Yang N. B., Li G. X., et al. Coronavirus Disease 19 With Gastrointestinal Symptoms as Initial Manifestations: A Case Report. J Int Med Res (2020) 48:300060520952256. doi: 10.1177/0300060520952256.

Cappell M. S. Moderately Severe Diarrhea and Impaired Renal Function With COVID-19 Infection. Am J Gastroenterol (2020) 115:947-8. doi: 10.14309/ajg.0000000000000681.

Shi H., Han X., Jiang N., Cao Y., Alwalid O., Gu J., et al. Radiological Findings From 81 Patients With COVID-19 Pneumonia in Wuhan, China: A Descriptive Study. Lancet Infect Dis (2020) 20:425-34. doi: 10.1016/S1473-3099(20)30086-4.

Sun S-H., Chen Q., Gu H. J., Yang G., Wang Y. X., Huang X. Y., et al. A Mouse Model of SARS-CoV-2 Infection and Pathogenesis. Cell Host Microbe (2020) 28:124-33.e4. doi: 10.1016/j.chom.2020.05.020.

Jiang R-D., Liu M. Q., Chen Y., Shan C., Zhou Y. W., Shen X. R., et al. Pathogenesis of SARS-CoV-2 in Transgenic Mice Expressing Human Angiotensin-Converting Enzyme 2. Cell (2020) 182:50-8.e8.

Wong S.H., Lui R. N., Sung J. J. Covid-19 and the Digestive System. J Gastroenterol Hepatol (2020) 35:744-8. doi: 10.1111/jgh.15047.

Karki S., Rawal S. B., Malla S., Rayamajhi J., Thapa B. B. A Case Report on Spontaneous Hemoperitoneum in COVID-19 Patient.Int J Surg Case Rep (2020) 75:211-3. doi: 10.1016/j.ijscr.2020.09.078.

Moazzam Z., Salim A., Ashraf A., Jehan F., Arshad M.Intussusception in an Infant as a Manifestation of COVID-19. J Pediatr Surg Case Rep (2020) 59:101533. doi: 10.1016/j.epsc.2020.101533.

Chiu C.Y., Sarwal A., Mon A. M., Tan Y. E., Shah V. Gastrointestinal: COVID-19 Related Ischemic Bowel Disease. J Gastroenterol Hepatol (2020) 36(4):850. doi: 10.1111/jgh.15254.

Giuffrè M., Bozzato A. M., Di Bella S., Occhipinti A. A., Martingano P., Cavallaro M. F.M., et al. Spontaneous Rectal Perforation in a Patient With SARS-CoV-2 Infection. J Pers Med (2020) 10:157. doi: 10.3390/jpm10040157.

Purayil N., Sirajudeen J., Va N., Mathew J. COVID-19 Presenting as Acute Abdominal Pain: A Case Report. Cureus (2020) 12: e9659. doi: 10.7759/cureus.9659.

Chen T., Yang Q., Duan H. A Severe Coronavirus Disease 2019 Patient With High-Risk Predisposing Factors Died From Massive Gastrointestinal Bleeding: A Case Report. BMC Gastroenterol (2020) 20:318. doi: 10.1186/s12876-020-01458-x.

Khader M., Al Bishawi A., Kambal A., Abdelmajid A. SARS-CoV-2 Infection Presenting as Colitis With Chest and Abdomen CT Findings. Radiol Case Rep (2020) 15:2427-32. doi: 10.1016/j.radcr.2020.09.035.

Schulz C., Mayerle J., Stubbe H. C., Sirtl S, Lerch MM, Malfertheiner P. [COVID-19 From a Gastroenterological Perspective]. Dtsch Med Wochenschr (2020) 145:1033-8. doi: 10.1055/a-1167-5825.

Jin X., Lian J. S., Hu J. H., Gao J., Zheng L., Zhang Y. M., et al. Epidemiological, Clinical and Virological Characteristics of 74 Cases of Coronavirus-Infected Disease 2019 (COVID-19) With Gastrointestinal Symptoms. Gut (2020) 69:1002-9. doi: 10.1136/gutjnl-2020-320926.

Adukia S.A., Ruhatiya R. S., Maheshwarappa H. M., Manjunath R. B., Jain G. N. Extrapulmonary Features of COVID-19: A Concise Review. Indian J Crit Care Med (2020) 24:575-80. doi: 10.5005/jp-journals-10071-23476.

Sun J-K., Liu Y., Zou L., Zhang W. H., Li J. J., Wang Y., et al. Acute Gastrointestinal Injury in Critically Ill Patients With COVID-19 in Wuhan, China. World J Gastroenterol (2020) 26:6087-97. doi: 10.3748/wjg.v26.i39.6087.

Schulz C., Mayerle J., Stubbe H. C., Sirtl S., Lerch M. M., Malfertheiner P. [COVID-19 From a Gastroenterological Perspective]. Dtsch Med Wochenschr (2020) 145:1033-8. doi: 10.1055/a-1167-5825.

Cheung S., Quiwa J. C., Pillai A., Onwu C., Tharayil Z. J., Gupta R. 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.

Andrews P.L., Rudd J. A. The Physiology and Pharmacology of Nausea and Vomiting Induced by Anticancer Chemotherapy in Humans. Management of Chemotherapy-Induced Nausea and Vomiting. Springer, 2016; 5-44.

Elmunzer B.J., Spitzer R. L., Foster L. D., et al. Digestive manifestations in patients hospitalized with COVID-19. medRxiv. 2020.

Pan L., Mu M., Yang P., et al. Clinical characteristics of COVID-19 patients with digestive symptoms in Hubei, China: a descriptive, cross-sectional, multicenter study. Am. J. Gastroenterol. 2020; 115: 766-773.

Argenziano M.G., Bruce S. L., Slater C. L., et al. Characterization and clinical course of 1000 patients with coronavirus disease 2019 in New York: retrospective case series. BMJ 2020; 369: m1996.

Xiao-Ping Xie, Li-Ping Sheng, Chao-Qun Han, et al. Features of capsule endoscopy in COVID-19 patients with a six-month follow-up: A prospective observational study. Medical Virology (2021) 94(1):246-252. doi: 10.1002/jmv.27308.

Sharma S., Kumar R., Shalimar. Management of Gastrointestinal Bleeding in Coronavirus Disease: Exploring the Options. Am J Gastroenterol (2020) 116(4):843-4. doi: 10.14309/ajg.0000000000000979.

Bhayana R., Som A., Li M. D., Carey D. E., Anderson M. A., Blake M. A., et al. Abdominal Imaging Findings in COVID-19: Preliminary Observations. Radiology (2020) 297: E207-15. doi: 10.1148/radiol.2020201908.

Giuffrè M., Di Bella S., Sambataro G., Zerbato V., Cavallaro M., Occhipinti A. A., et al. COVID-19-Induced Thrombosis in Patients Without Gastrointestinal Symptoms and Elevated Fecal Calprotectin: Hypothesis Regarding Mechanism of Intestinal Damage Associated With COVID-19. Trop Med Infect Dis (2020) 5:147. doi: 10.3390/tropicalmed5030147.

Farina D., Rondi P., Botturi E., Renzulli M., Borghesi A., Guelfi D., et al. Gastrointestinal: Bowel Ischemia in a Suspected Coronavirus Disease (COVID-19) Patient. J Gastroenterol Hepatol (2020) 36(1):41. doi: 10.1111/jgh.15094.

Liao M., et al. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19.Nat. Med.26, 842-844 (2020).

Udeh R., Advani S., de Guadiana Romualdo L. G., Dolja-Gore X. Calprotectin, an emerging biomarker of interest in COVID-19: A systematic review and meta-analysis. J. Clin. Med. 2021;10:775.

Ayling R. M., Kok K. Fecal calprotectin.Adv. Clin. Chem.2018;87: 161-190.

Jena A., Kumar-M P., Singh A. K., Sharma V. Fecal calprotectin levels in COVID-19: Lessons from a systematic review on its use in inflammatory bowel disease during the pandemic. Dig. Liver Dis. 2020;53, 295-297.

Gu J., Han B., Wang, J. COVID-19: Gastrointestinal manifestations and potential fecal-oral transmission. Gastroenterology. 2020;158, 1518-1519.

Reisinger E. C., Fritzsche C., Krause R., Krejs G. J. Diarrhea caused by primarily non-gastrointestinal infections.Nat. Clin. Pract. Gastroenterol. Hepatol. 2005;2:216-222.

The authors declare that there are no conflicts of interest present.