Intestinal Damage, Inflammation and Microbiota Alteration during COVID-19 Infection
Abstract
:1. Introduction
2. Role of ACE2 Receptors in the Pathogenesis of COVID-19 Disease
3. Inflammation, Acute and Chronic GI Conditions and the Role of Endoscopy in COVID-19 Patients
4. Calprotectin
5. Role of the Microbiota and the Immune System
6. Probiotics’ Role in Patients with COVID-19 Infection
7. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Ghazanfar, H.; Kandhi, S.; Shin, D.; Muthumanickam, A.; Gurjar, H.; Qureshi, Z.A.; Shaban, M.; Farag, M.; Haider, A.; Budhathoki, P.; et al. Impact of COVID-19 on the Gastrointestinal Tract: A Clinical Review. Cureus 2022, 14, e23333. [Google Scholar] [CrossRef] [PubMed]
- Shih, A.R.; Misdraji, J. COVID-19: Gastrointestinal and hepatobiliary manifestations. Hum. Pathol. 2022, 132, 39–55. [Google Scholar] [CrossRef] [PubMed]
- Knyazev, E.; Nersisyan, S.; Tonevitsky, A. Endocytosis and Transcytosis of SARS-CoV-2 Across the Intestinal Epithelium and Other Tissue Barriers. Front. Immunol. 2021, 12, 636966. [Google Scholar] [CrossRef] [PubMed]
- Elmunzer, B.J.; Spitzer, R.L.; Foster, L.D.; Merchant, A.A.; Howard, E.F.; Patel, V.A.; West, M.K.; Qayed, E.; Nustas, R.; Zakaria, A.; et al. Digestive Manifestations in Patients Hospitalized With Coronavirus Disease 2019. Clin. Gastroenterol. Hepatol. 2021, 19, 1355–1365.e4. [Google Scholar] [CrossRef] [PubMed]
- Jin, X.; Lian, J.S.; Hu, J.H.; Gao, J.; Zheng, L.; Zhang, Y.M.; Hao, S.R.; Jia, H.Y.; Cai, H.; Zhang, X.L.; et al. Epidemiological, clinical and virological characteristics of 74 cases of coronavirus-infected disease 2019 (COVID-19) with gastrointestinal symptoms. Gut 2020, 69, 1002–1009. [Google Scholar] [CrossRef] [Green Version]
- Zollner, A.; Koch, R.; Jukic, A.; Pfister, A.; Meyer, M.; Rössler, A.; Kimpel, J.; Adolph, T.E.; Tilg, H. Postacute COVID-19 is Characterized by Gut Viral Antigen Persistence in Inflammatory Bowel Diseases. Gastroenterology 2022, 163, 495–506.e8. [Google Scholar] [CrossRef]
- Devaux, C.A.; Lagier, J.-C.; Raoult, D. New Insights Into the Physiopathology of COVID-19: SARS-CoV-2-Associated Gastrointestinal Illness. Front. Med. 2021, 8, 640073. [Google Scholar] [CrossRef]
- Morone, G.; Palomba, A.; Iosa, M.; Caporaso, T.; De Angelis, D.; Venturiero, V.; Savo, A.; Coiro, P.; Carbone, D.; Gimigliano, F.; et al. Incidence and Persistence of Viral Shedding in COVID-19 Post-acute Patients With Negativized Pharyngeal Swab: A Systematic Review. Front. Med. 2020, 7, 562. [Google Scholar] [CrossRef]
- Wang, Y.; Li, Y.; Zhang, Y.; Liu, Y.; Liu, Y. Are gastrointestinal symptoms associated with higher risk of Mortality in COVID-19 patients? A systematic review and meta-analysis. BMC Gastroenterol. 2022, 22, 106. [Google Scholar] [CrossRef]
- Natarajan, A.; Zlitni, S.; Brooks, E.F.; Vance, S.E.; Dahlen, A.; Hedlin, H.; Park, R.M.; Han, A.; Schmidtke, D.T.; Verma, R.; et al. Gastrointestinal symptoms and fecal shedding of SARS-CoV-2 RNA suggest prolonged gastrointestinal infection. Med 2022, 3, 371–387.e9. [Google Scholar] [CrossRef]
- Cheung, K.S.; Hung, I.F.N.; Chan, P.P.Y.; Lung, K.C.; Tso, E.; Liu, R.; Ng, Y.Y.; Chu, M.Y.; Chung, T.W.H.; Tam, A.R.; 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, 159, 81–95. [Google Scholar] [CrossRef] [PubMed]
- Guo, M.; Tao, W.; Flavell, R.A.; Zhu, S. Potential intestinal infection and faecal–oral transmission of SARS-CoV-2. Nat. Rev. Gastroenterol. Hepatol. 2021, 18, 269–283. [Google Scholar] [CrossRef] [PubMed]
- Liu, Y.-C.; Kuo, R.-L.; Shih, S.-R. COVID-19: The first documented coronavirus pandemic in history. Biomed. J. 2020, 43, 328–333. [Google Scholar] [CrossRef] [PubMed]
- Li, F. Structure, Function, and Evolution of Coronavirus Spike Proteins. Annu. Rev. Virol. 2016, 3, 237–261. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xu, X.; Yu, C.; Qu, J.; Zhang, L.; Jiang, S.; Huang, D.; Chen, B.; Zhang, Z.; Guan, W.; Ling, Z.; et al. Imaging and clinical features of patients with 2019 novel coronavirus SARS-CoV-2. Eur. J. Nucl. Med. Mol. Imaging 2020, 47, 1275–1280. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hoffmann, M.; Kleine-Weber, H.; Schroeder, S.; Krüger, N.; Herrler, T.; Erichsen, S.; Schiergens, T.S.; Herrler, G.; Wu, N.-H.; Nitsche, A.; et al. SARS-CoV-2 Cell Entry Depends on ACE2 and TMPRSS2 and Is Blocked by a Clinically Proven Protease Inhibitor. Cell 2020, 181, 271–280.e8. [Google Scholar] [CrossRef] [PubMed]
- Tai, W.; He, L.; Zhang, X.; Pu, J.; Voronin, D.; Jiang, S.; Zhou, Y.; Du, L. Characterization of the receptor-binding domain (RBD) of 2019 novel coronavirus: Implication for development of RBD protein as a viral attachment inhibitor and vaccine. Cell. Mol. Immunol. 2020, 17, 613–620. [Google Scholar] [CrossRef] [Green Version]
- Hou, P.; Xu, Q.; Na, J.; Zhang, B.L.; Wu, H.; Li, P.; Zhao, X.X. Angiotensin-converting enzyme 2 and coronavirus: Research update on pathogenesis of the infection induced by this indissoluble bond. Zhonghua Xin Xue Guan Bing Za Zhi 2020, 48, 539–545. [Google Scholar]
- Hamming, I.; Cooper, M.; Haagmans, B.; Hooper, N.; Korstanje, R.; Osterhaus, A.; Timens, W.; Turner, A.; Navis, G.; van Goor, H. The emerging role of ACE2 in physiology and disease. J. Pathol. 2007, 212, 1–11. [Google Scholar] [CrossRef]
- Sanchis-Gomar, F.; Lavie, C.J.; Perez-Quilis, C.; Henry, B.M.; Lippi, G. Angiotensin-Converting Enzyme 2 and Antihypertensives (Angiotensin Receptor Blockers and Angiotensin-Converting Enzyme Inhibitors) in Coronavirus Disease 2019. Mayo Clin. Proc. 2020, 95, 1222–1230. [Google Scholar] [CrossRef]
- Beyerstedt, S.; Casaro, E.B.; Rangel, É.B. COVID-19: Angiotensin-converting enzyme 2 (ACE2) expression and tissue susceptibility to SARS-CoV-2 infection. Eur. J. Clin. Microbiol. Infect. Dis. 2021, 40, 905–919. [Google Scholar] [CrossRef] [PubMed]
- Ning, L.; Shan, G.; Sun, Z.; Zhang, F.; Xu, C.; Lou, X.; Li, S.; Du, H.; Chen, H.; Xu, G. Quantitative Proteomic Analysis Reveals the Deregulation of Nicotinamide Adenine Dinucleotide Metabolism and CD38 in Inflammatory Bowel Disease. BioMed Res. Int. 2019, 2019, 3950628. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Garg, M.; Royce, S.G.; Tikellis, C.; Shallue, C.; Batu, D.; Velkoska, E.; Burrell, L.M.; Patel, S.K.; Beswick, L.; Jackson, A.; et al. Imbalance of the renin–angiotensin system may contribute to inflammation and fibrosis in IBD: A novel therapeutic target? Gut 2020, 69, 841–851. [Google Scholar] [CrossRef] [PubMed]
- An, P.; Ji, M.; Ren, H.; Su, J.; Ding, N.S.; Kang, J.; Yin, A.; Zhou, Q.; Shen, L.; Zhao, L.; et al. Prevention of COVID-19 in patients with inflammatory bowel disease in Wuhan, China. Lancet Gastroenterol. Hepatol. 2020, 5, 525–527. [Google Scholar] [CrossRef] [PubMed]
- Potdar, A.A.; Dube, S.; Naito, T.; Li, K.; Botwin, G.; Haritunians, T.; Li, D.; Casero, D.; Yang, S.; Bilsborough, J.; et al. Altered Intestinal ACE2 Levels Are Associated With Inflammation, Severe Disease, and Response to Anti-Cytokine Therapy in Inflammatory Bowel Disease. Gastroenterology 2021, 160, 809–822.e7. [Google Scholar] [CrossRef]
- Monteleone, G.; Ardizzone, S. Are Patients with Inflammatory Bowel Disease at Increased Risk for COVID-19 Infection? J. Crohns. Colitis 2020, 14, 1334–1336. [Google Scholar] [CrossRef] [PubMed]
- Wong, E.; Cohen, T.; Romi, E.; Levin, M.; Peleg, Y.; Arad, U.; Yaron, A.; Milla, M.E.; Sagi, I. Harnessing the natural inhibitory domain to control TNFα Converting Enzyme (TACE) activity in vivo. Sci. Rep. 2016, 6, 35598. [Google Scholar] [CrossRef] [Green Version]
- Hakeam, H.A.; Alsemari, M.; Al Duhailib, Z.; Ghonem, L.; Alharbi, S.A.; Almutairy, E.; Bin Sheraim, N.M.; Alsalhi, M.; Alhijji, A.; AlQahtani, S.; et al. Association of Angiotensin-Converting Enzyme Inhibitors and Angiotensin II Blockers With Severity of COVID-19: A Multicenter, Prospective Study. J. Cardiovasc. Pharmacol. Ther. 2021, 26, 244–252. [Google Scholar] [CrossRef]
- Hippisley-Cox, J.; Young, D.; Coupland, C.; Channon, K.M.; Tan, P.S.; Harrison, D.A.; Rowan, K.; Aveyard, P.; Pavord, I.D.; Watkinson, P.J. Risk of severe COVID-19 disease with ACE inhibitors and angiotensin receptor blockers: Cohort study including 8.3 million people. Heart 2020, 106, 1503–1511. [Google Scholar] [CrossRef]
- COVID-19: Issues Related to Gastrointestinal Disease in Adults. Available online: https://www.uptodate.com/contents/covid-19-issues-related-to-gastrointestinal-disease-in-adults?search=&source=covid19_landing&usage_type=main_section (accessed on 11 March 2023).
- Almario, C.V.; Chey, W.D.; Spiegel, B.M. Increased Risk of COVID-19 Among Users of Proton Pump Inhibitors. Am. J. Gastroenterol. 2020, 115, 1707–1715. [Google Scholar] [CrossRef]
- Haberman, R.; Axelrad, J.; Chen, A.; Castillo, R.; Yan, D.; Izmirly, P.; Neimann, A.; Adhikari, S.; Hudesman, D.; Scher, J.U. COVID-19 in Immune-Mediated Inflammatory Diseases—Case Series from New York. N. Engl. J. Med. 2020, 383, 85–88. [Google Scholar] [CrossRef] [PubMed]
- Brenner, E.J.; Ungaro, R.C.; Gearry, R.B.; Kaplan, G.G.; Kissous-Hunt, M.; Lewis, J.D.; Ng, S.C.; Rahier, J.-F.; Reinisch, W.; Ruemmele, F.M.; et al. Corticosteroids, But Not TNF Antagonists, Are Associated With Adverse COVID-19 Outcomes in Patients With Inflammatory Bowel Diseases: Results From an International Registry. Gastroenterology 2020, 159, 481–491.e3. [Google Scholar] [CrossRef] [PubMed]
- Bangma, A.; Voskuil, M.D.; Weersma, R.K. TNFα-Antagonist Use and Mucosal Inflammation Are Associated with Increased Intestinal Expression of SARS-CoV-2 Host Protease TMPRSS2 in Patients with Inflammatory Bowel Disease. Gastroenterology 2021, 160, 2621–2622. [Google Scholar] [CrossRef] [PubMed]
- Rubin, D.T.; Feuerstein, J.D.; Wang, A.Y.; Cohen, R.D. AGA Clinical Practice Update on Management of Inflammatory Bowel Disease During the COVID-19 Pandemic: Expert Commentary. Gastroenterology 2020, 159, 350–357. [Google Scholar] [CrossRef] [PubMed]
- Lei, H.-Y.; Ding, Y.-H.; Nie, K.; Dong, Y.-M.; Xu, J.-H.; Yang, M.-L.; Liu, M.-Q.; Wei, L.; Nasser, M.; Xu, L.-Y.; et al. Potential effects of SARS-CoV-2 on the gastrointestinal tract and liver. Biomed. Pharmacother. 2021, 133, 111064. [Google Scholar] [CrossRef]
- Arjmand, B.; Alavi-Moghadam, S.; Sarvari, M.; Rezaei-Tavirani, M.; Mafi, A.R.; Arjmand, R.; Nikandish, M.; Nasli-Esfahani, E.; Larijani, B. Critical roles of cytokine storm and bacterial infection in patients with COVID-19: Therapeutic potential of mesenchymal stem cells. Inflammopharmacology 2023, 31, 171–206. [Google Scholar] [CrossRef]
- Chen, G.; Wu, D.; Guo, W.; Cao, Y.; Huang, D.; Wang, H.; Wang, T.; Zhang, X.; Chen, H.; Yu, H.; et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J. Clin. Investig. 2020, 130, 2620–2629. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Calitri, C.; Fumi, I.; Ignaccolo, M.G.; Banino, E.; Benetti, S.; Lupica, M.M.; Fantone, F.; Pace, M.; Garofalo, F. Gastrointestinal involvement in paediatric COVID-19—from pathogenesis to clinical management: A comprehensive review. World J. Gastroenterol. 2021, 27, 3303–3316. [Google Scholar] [CrossRef]
- Xiao, F.; Tang, M.; Zheng, X.; Liu, Y.; Li, X.; Shan, H. Evidence for Gastrointestinal Infection of SARS-CoV-2. Gastroenterology 2020, 158, 1831–1833.e3. [Google Scholar] [CrossRef] [PubMed]
- Patel, H.K.; Makker, J.; Alemam, A.; Chilimuri, S. Diarrhea due to SARS-CoV-2-Related Exocrine Pancreatic Insufficiency. Case Rep. Gastrointest. Med. 2021, 2021, 9920981. [Google Scholar] [CrossRef] [PubMed]
- El Moheb, M.; Naar, L.; Christensen, M.A.; Kapoen, C.; Maurer, L.R.; Farhat, M.; Kaafarani, H.M.A. Gastrointestinal Complications in Critically Ill Patients With and Without COVID-19. JAMA 2020, 324, 1899–1901, Erratum in JAMA 2021, 325, 1113. [Google Scholar] [CrossRef] [PubMed]
- Nersisyan, S.A. Induction of Hypoxic Response in Caco-2 Cells Promote the Expression of Genes Involved in SARS-CoV-2 Endocytosis and Transcytosis. Dokl. Biochem. Biophys. 2022, 506, 206–209. [Google Scholar] [CrossRef] [PubMed]
- Wei, X.-S.; Wang, X.; Niu, Y.-R.; Ye, L.-L.; Peng, W.-B.; Wang, Z.-H.; Yang, W.-B.; Yang, B.-H.; Zhang, J.-C.; Ma, W.-L.; et al. Diarrhea Is Associated With Prolonged Symptoms and Viral Carriage in Corona Virus Disease 2019. Clin. Gastroenterol. Hepatol. 2020, 18, 1753–1759.e2. [Google Scholar] [CrossRef] [PubMed]
- Tian, Y.; Rong, L.; Nian, W.; He, Y. Review article: Gastrointestinal features in COVID-19 and the possibility of faecal transmission. Aliment. Pharmacol. Ther. 2020, 51, 843–851. [Google Scholar] [CrossRef] [PubMed]
- Schettino, M.; Pellegrini, L.; Picascia, D.; Saibeni, S.; Bezzio, C.; Bini, F.; Omazzi, B.F.; Devani, M.; Arena, I.; Bongiovanni, M.; et al. Clinical Characteristics of COVID-19 Patients With Gastrointestinal Symptoms in Northern Italy: A Single-Center Cohort Study. Am. J. Gastroenterol. 2021, 116, 306–310. [Google Scholar] [CrossRef]
- Vanella, G.; Capurso, G.; Burti, C.; Fanti, L.; Ricciardiello, L.; Lino, A.S.; Boskoski, I.; Bronswijk, M.; Tyberg, A.; Nair, G.K.K.; et al. Gastrointestinal mucosal damage in patients with COVID-19 undergoing endoscopy: An international multicentre study. BMJ Open Gastroenterol. 2021, 8, e000578. [Google Scholar] [CrossRef]
- Massironi, S.; Viganò, C.; Dioscoridi, L.; Filippi, E.; Pagliarulo, M.; Manfredi, G.; Conti, C.B.; Signorelli, C.; Redaelli, A.E.; Bonato, G.; et al. Endoscopic Findings in Patients Infected With 2019 Novel Coronavirus in Lombardy, Italy. Clin. Gastroenterol. Hepatol. 2020, 18, 2375–2377. [Google Scholar] [CrossRef]
- Yantiss, R.K.; Qin, L.; He, B.; Crawford, C.V.; Seshan, S.; Patel, S.; Wahid, N.; Jessurun, J. Intestinal Abnormalities in Patients With SARS-CoV-2 Infection: Histopathologic Changes Reflect Mechanisms of Disease. Am. J. Surg. Pathol. 2022, 46, 89–96. [Google Scholar] [CrossRef]
- Xie, X.; Sheng, L.; Han, C.; Jin, Y.; Bai, T.; Lin, R.; Ding, Z.; Hou, X. Features of capsule endoscopy in COVID-19 patients with a six-month follow-up: A prospective observational study. J. Med. Virol. 2022, 94, 246–252. [Google Scholar] [CrossRef] [PubMed]
- Livanos, A.E.; Jha, D.; Cossarini, F.; Gonzalez-Reiche, A.S.; Tokuyama, M.; Aydillo, T.; Parigi, T.L.; Ladinsky, M.S.; Ramos, I.; Dunleavy, K.; et al. Intestinal Host Response to SARS-CoV-2 Infection and COVID-19 Outcomes in Patients With Gastrointestinal Symptoms. Gastroenterology 2021, 160, 2435–2450.e34. [Google Scholar] [CrossRef]
- Burgueño, J.F.; Reich, A.; Hazime, H.; Quintero, M.A.; Fernandez, I.; Fritsch, J.; Santander, A.M.; Brito, N.; Damas, O.M.; Deshpande, A.; et al. Expression of SARS-CoV-2 Entry Molecules ACE2 and TMPRSS2 in the Gut of Patients With IBD. Inflamm. Bowel Dis. 2020, 26, 797–808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dalal, A.; Sonika, U.; Kumar, M.; George, R.; Kumar, A.; Srivastava, S.; Sachdeva, S.; Sharma, B.C. COVID-19 Rapid Antigen Test: Role in Screening Prior to Gastrointestinal Endoscopy. Clin. Endosc. 2021, 54, 522–525. [Google Scholar] [CrossRef] [PubMed]
- Zhang, S.; Wu, X.; Pan, H.; Wu, D.; Xu, T.; Shen, N.; Zhang, Y.; Feng, Y.; Wang, Q.; Jiang, Q.; et al. Gastrointestinal endoscopy infection control strategy during COVID-19 pandemic: Experience from a tertiary medical center in China. Dig. Endosc. 2021, 33, 577–586. [Google Scholar] [CrossRef] [PubMed]
- Bowyer, B.; Thukral, C.; Patel, S.; Dovalovsky, K.; Bowyer, S.G.; Ford, J.; Fox, T.; Ringler, E. Outcomes of symptom screening and universal COVID-19 reverse transcriptase polymerase chain reaction testing before endoscopy in a community-based ambulatory surgery center. Gastrointest. Endosc. 2021, 93, 1060–1064.e1. [Google Scholar] [CrossRef]
- Kuftinec, G.; Elmunzer, B.J.; Amin, S. North American Alliance for the Study of Digestive Manifestations of COVID-19. The role of endoscopy and findings in COVID-19 patients, an early North American Cohort. BMC Gastroenterol. 2021, 21, 205. [Google Scholar] [CrossRef]
- Emara, M.H.; Zaghloul, M.; Abdel-Gawad, M.; Makhlouf, N.A.; Abdelghani, M.; Abdeltawab, D.; Mahros, A.M.; Bekhit, A.; Behl, N.S.; Mostafa, S.; et al. Effect of COVID-19 on gastrointestinal endoscopy practice: A systematic review. Ann. Med. 2022, 54, 2875–2884. [Google Scholar] [CrossRef] [PubMed]
- Pohl, H. Endoscopy during COVID—What have we learned? Endoscopy 2021, 53, 171–172. (In German) [Google Scholar] [CrossRef]
- Ojetti, V.; Saviano, A.; Covino, M.; Acampora, N.; Troiani, E.; Franceschi, F.; Abbate, V.; Addolorato, G.; Agostini, F.; Ainora, M.E.; et al. COVID-19 and intestinal inflammation: Role of fecal calprotectin. Dig. Liver Dis. 2020, 52, 1231–1233. [Google Scholar] [CrossRef]
- Udeh, R.; Advani, S.; de Guadiana Romualdo, L.; Dolja-Gore, X. Calprotectin, an Emerging Biomarker of Interest in COVID-19: A Systematic Review and Meta-Analysis. J. Clin. Med. 2021, 10, 775. [Google Scholar] [CrossRef] [PubMed]
- Shokri-Afra, H.; Alikhani, A.; Moradipoodeh, B.; Noorbakhsh, F.; Fakheri, H.; Moradi-Sardareh, H. Elevated fecal and serum calprotectin in COVID-19 are not consistent with gastrointestinal symptoms. Sci. Rep. 2021, 11, 22001. [Google Scholar] [CrossRef]
- Yamamoto, S.; Saito, M.; Tamura, A.; Prawisuda, D.; Mizutani, T.; Yotsuyanagi, H. The human microbiome and COVID-19: A systematic review. PLoS ONE 2021, 16, e0253293. [Google Scholar] [CrossRef] [PubMed]
- Zuo, T.; Zhang, F.; Lui, G.C.Y.; Yeoh, Y.K.; Li, A.Y.L.; Zhan, H.; Wan, Y.; Chung, A.C.K.; Cheung, C.P.; Chen, N.; et al. Alterations in Gut Microbiota of Patients With COVID-19 During Time of Hospitalization. Gastroenterology 2020, 159, 944–955.e948. [Google Scholar] [CrossRef] [PubMed]
- Ghavami, S.B.; Pourhamzeh, M.; Farmani, M.; Raftar, S.K.A.; Shahrokh, S.; Shpichka, A.; Aghdaei, H.A.; Hakemi-Vala, M.; Hossein-Khannazer, N.; Timashev, P.; et al. Cross-talk between immune system and microbiota in COVID-19. Expert Rev. Gastroenterol. Hepatol. 2021, 15, 1281–1294. [Google Scholar] [CrossRef] [PubMed]
- Xu, X.; Zhang, W.; Guo, M.; Xiao, C.; Fu, Z.; Yu, S.; Jiang, L.; Wang, S.; Ling, Y.; Liu, F.; et al. Integrated analysis of gut microbiome and host immune responses in COVID-19. Front. Med. 2022, 16, 263–275. [Google Scholar] [CrossRef] [PubMed]
- Schirmer, M.; Smeekens, S.P.; Vlamakis, H.; Jaeger, M.; Oosting, M.; Franzosa, E.A.; ter Horst, R.; Jansen, T.; Jacobs, L.; Bonder, M.J.; et al. Linking the Human Gut Microbiome to Inflammatory Cytokine Production Capacity. Cell 2016, 167, 1897. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dumas, A.; Bernard, L.; Poquet, Y.; Lugo-Villarino, G.; Neyrolles, O. The role of the lung microbiota and the gut-lung axis in respiratory infectious diseases. Cell. Microbiol. 2018, 20, e12966. [Google Scholar] [CrossRef] [Green Version]
- Jabczyk, M.; Nowak, J.; Hudzik, B.; Zubelewicz-Szkodzińska, B. Microbiota and Its Impact on the Immune System in COVID-19—A Narrative Review. J. Clin. Med. 2021, 10, 4537. [Google Scholar] [CrossRef]
- Ma, P.-J.; Wang, M.-M.; Wang, Y. Gut microbiota: A new insight into lung diseases. Biomed. Pharmacother. 2022, 155, 113810. [Google Scholar] [CrossRef]
- Budden, K.F.; Gellatly, S.L.; Wood, D.L.A.; Cooper, M.A.; Morrison, M.; Hugenholtz, P.; Hansbro, P.M. Emerging pathogenic links between microbiota and the gut–lung axis. Nat. Rev. Microbiol. 2017, 15, 55–63. [Google Scholar] [CrossRef]
- Vutcovici, M.; Brassard, P.; Bitton, A. Inflammatory bowel disease and airway diseases. World J. Gastroenterol. 2016, 22, 7735–7741. [Google Scholar] [CrossRef]
- Hasegawa, K.; Linnemann, R.W.; Mansbach, J.M.; Ajami, N.J.; Espinola, J.A.; Petrosino, J.F.; Piedra, P.A.; Stevenson, M.D.; Sullivan, A.F.; Thompson, A.D.; et al. The Fecal Microbiota Profile and Bronchiolitis in Infants. Pediatrics 2016, 138, e20160218. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- de Oliveira, G.L.V.; Oliveira, C.N.S.; Pinzan, C.F.; de Salis, L.V.V.; Cardoso, C.R.D.B. Microbiota Modulation of the Gut-Lung Axis in COVID-19. Front. Immunol. 2021, 12, 635471. [Google Scholar] [CrossRef] [PubMed]
- Dhar, D.; Mohanty, A. Gut microbiota and COVID-19—Possible link and implications. Virus Res. 2020, 285, 198018. [Google Scholar] [CrossRef] [PubMed]
- Qi, F.; Qian, S.; Zhang, S.; Zhang, Z. Single cell RNA sequencing of 13 human tissues identify cell types and receptors of human coronaviruses. Biochem. Biophys. Res. Commun. 2020, 526, 135–140. [Google Scholar] [CrossRef]
- Rinninella, E.; Raoul, P.; Cintoni, M.; Franceschi, F.; Miggiano, G.A.D.; Gasbarrini, A.; Mele, M.C. What Is the Healthy Gut Microbiota Composition? A Changing Ecosystem across Age, Environment, Diet, and Diseases. Microorganisms 2019, 7, 14. [Google Scholar] [CrossRef] [Green Version]
- Shah, T.; Shah, Z.; Baloch, Z.; Cui, X. The role of microbiota in respiratory health and diseases, particularly in tuberculosis. Biomed. Pharmacother. 2021, 143, 112108. [Google Scholar] [CrossRef]
- Heier, I.; Malmström, K.; Sajantila, A.; Lohi, J.; Mäkelä, M.; Jahnsen, F.L. Characterisation of bronchus-associated lymphoid tissue and antigen-presenting cells in central airway mucosa of children. Thorax 2011, 66, 151–156. [Google Scholar] [CrossRef] [Green Version]
- Neag, M.A.; Vulturar, D.-M.; Gherman, D.; Burlacu, C.-C.; Todea, D.A.; Buzoianu, A.D. Gastrointestinal microbiota: A predictor of COVID-19 severity? World J. Gastroenterol. 2022, 28, 6328–6344. [Google Scholar] [CrossRef]
- Prasad, R.; Patton, M.J.; Floyd, J.L.; Fortmann, S.; DuPont, M.; Harbour, A.; Wright, J.; Lamendella, R.; Stevens, B.R.; Oudit, G.Y.; et al. Plasma Microbiome in COVID-19 Subjects: An Indicator of Gut Barrier Defects and Dysbiosis. Int. J. Mol. Sci. 2022, 23, 9141. [Google Scholar] [CrossRef]
- Xiang, H.; Liu, Q.-P. Alterations of the gut microbiota in coronavirus disease 2019 and its therapeutic potential. World J. Gastroenterol. 2022, 28, 6689–6701. [Google Scholar] [CrossRef]
- Choi, S.-M.; Xie, H.; Campbell, A.P.; Kuypers, J.; Leisenring, W.; Boudreault, A.A.; Englund, J.A.; Corey, L.; Boeckh, M. Influenza Viral RNA Detection in Blood as a Marker to Predict Disease Severity in Hematopoietic Cell Transplant Recipients. J. Infect. Dis. 2012, 206, 1872–1877. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Qian, Q.; Fan, L.; Liu, W.; Li, J.; Yue, J.; Wang, M.; Ke, X.; Yin, Y.; Chen, Q.; Jiang, C. Direct Evidence of Active SARS-CoV-2 Replication in the Intestine. Clin. Infect. Dis. 2021, 73, 361–366. [Google Scholar] [CrossRef] [PubMed]
- Katz-Agranov, N.; Zandman-Goddard, G. Autoimmunity and COVID-19—The microbiotal connection. Autoimmun. Rev. 2021, 20, 102865. [Google Scholar] [CrossRef]
- Harmer, D.; Gilbert, M.; Borman, R.; Clark, K.L. Quantitative mRNA expression profiling of ACE 2, a novel homologue of angiotensin converting enzyme. FEBS Lett. 2002, 532, 107–110. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dang, A.T.; Marsland, B.J. Microbes, metabolites, and the gut–lung axis. Mucosal Immunol. 2019, 12, 843–850. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Yeoh, Y.K.; Zuo, T.; Lui, G.C.-Y.; Zhang, F.; Liu, Q.; Li, A.Y.; Chung, A.C.; Cheung, C.P.; Tso, E.Y.; Fung, K.S.; et al. Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19. Gut 2021, 70, 698–706. [Google Scholar] [CrossRef] [PubMed]
- Khan, A.A.; Singh, H.; Bilal, M.; Ashraf, M.T. Microbiota, probiotics and respiratory infections: The three musketeers can tip off potential management of COVID-19. Am. J. Transl. Res. 2021, 13, 10977–10993. [Google Scholar]
- Bottari, B.; Castellone, V.; Neviani, E. Probiotics and COVID-19. Int. J. Food Sci. Nutr. 2021, 72, 293–299. [Google Scholar] [CrossRef] [PubMed]
- Hu, J.; Zhang, L.; Lin, W.; Tang, W.; Chan, F.K.; Ng, S.C. Review article: Probiotics, prebiotics and dietary approaches during COVID-19 pandemic. Trends Food Sci. Technol. 2021, 108, 187–196. [Google Scholar] [CrossRef] [PubMed]
- Gutiérrez-Castrellón, P.; Gandara-Martí, T.; Abreu, A.T.A.Y.; Nieto-Rufino, C.D.; López-Orduña, E.; Jiménez-Escobar, I.; Jiménez-Gutiérrez, C.; López-Velazquez, G.; Espadaler-Mazo, J. Probiotic improves symptomatic and viral clearance in Covid19 outpatients: A randomized, quadruple-blinded, placebo-controlled trial. Gut Microbes 2022, 14, 2018899. [Google Scholar] [CrossRef]
- King, S.; Glanville, J.; Sanders, M.E.; Fitzgerald, A.; Varley, D. Effectiveness of probiotics on the duration of illness in healthy children and adults who develop common acute respiratory infectious conditions: A systematic review and meta-analysis. Br. J. Nutr. 2014, 112, 41–54. [Google Scholar] [CrossRef] [PubMed]
- Saviano, A.; Potenza, A.; Siciliano, V.; Petruzziello, C.; Tarli, C.; Migneco, A.; Nasella, F.; Franceschi, F.; Ojetti, V. COVID-19 Pneumonia and Gut Inflammation: The Role of a Mix of Three Probiotic Strains in Reducing Inflammatory Markers and Need for Oxygen Support. J. Clin. Med. 2022, 11, 3758. [Google Scholar] [CrossRef] [PubMed]
- Brahma, S.; Naik, A.; Lordan, R. Probiotics: A gut response to the COVID-19 pandemic but what does the evidence show? Clin. Nutr. ESPEN 2022, 51, 17–27. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, Q.V.; Chong, L.C.; Hor, Y.-Y.; Lew, L.-C.; Rather, I.A.; Choi, S.-B. Role of Probiotics in the Management of COVID-19: A Computational Perspective. Nutrients 2022, 14, 274. [Google Scholar] [CrossRef] [PubMed]
- Khaled, J.M. Probiotics, prebiotics, and COVID-19 infection: A review article. Saudi J. Biol. Sci. 2021, 28, 865–869. [Google Scholar] [CrossRef] [PubMed]
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Saviano, A.; Brigida, M.; Petruzziello, C.; Zanza, C.; Candelli, M.; Morabito Loprete, M.R.; Saleem, F.; Ojetti, V. Intestinal Damage, Inflammation and Microbiota Alteration during COVID-19 Infection. Biomedicines 2023, 11, 1014. https://doi.org/10.3390/biomedicines11041014
Saviano A, Brigida M, Petruzziello C, Zanza C, Candelli M, Morabito Loprete MR, Saleem F, Ojetti V. Intestinal Damage, Inflammation and Microbiota Alteration during COVID-19 Infection. Biomedicines. 2023; 11(4):1014. https://doi.org/10.3390/biomedicines11041014
Chicago/Turabian StyleSaviano, Angela, Mattia Brigida, Carmine Petruzziello, Christian Zanza, Marcello Candelli, Maria Rita Morabito Loprete, Faiz Saleem, and Veronica Ojetti. 2023. "Intestinal Damage, Inflammation and Microbiota Alteration during COVID-19 Infection" Biomedicines 11, no. 4: 1014. https://doi.org/10.3390/biomedicines11041014