Microbial co-infections in COVID-19: Associated microbiota and underlying mechanisms of pathogenesis

Hoque, 2020, Genomic diversity and evolution, diagnosis, prevention, and therapeutics of the pandemic COVID-19 disease, PeerJ, 8, e9689, 10.7717/peerj.9689 Rahman, 2020, Epitope-based chimeric peptide vaccine design against S, M and E proteins of SARS-CoV-2 etiologic agent of global pandemic COVID-19: an in silico approach, PeerJ, 8, 10.7717/peerj.9572 Zhu, 2019, A novel coronavirus from patients with pneumonia in China, N. Engl. J. Med., 2020 Reid, 1999, Origin and evolution of the 1918 “Spanish” influenza virus hemagglutinin gene, Proc. Natl. Acad. Sci. Unit. States Am., 96, 1651, 10.1073/pnas.96.4.1651 Li, 2020, Substantial undocumented infection facilitates the rapid dissemination of novel coronavirus (SARS-CoV-2), Science, 368, 489, 10.1126/science.abb3221 Mirzaei, 2020, Bacterial co‐infections with SARS‐CoV‐2, IUBMB Life, 72, 2097, 10.1002/iub.2356 Paget, 2019, Mechanisms of bacterial superinfection post-influenza: a role for unconventional T cells, Front. Immunol., 10, 336, 10.3389/fimmu.2019.00336 Jia, 2017, Mechanisms of severe mortality-associated bacterial co-infections following influenza virus infection, Frontiers in cellular and infection microbiology, 7, 338, 10.3389/fcimb.2017.00338 Quah, 2018, Impact of microbial Aetiology on mortality in severe community-acquired pneumonia, BMC Infect. Dis., 18, 451, 10.1186/s12879-018-3366-4 Memish, 2020, Middle East respiratory syndrome, Lancet, 395, 1063, 10.1016/S0140-6736(19)33221-0 Hoque, 2020 Chen, 2020, Epidemiological and clinical characteristics of 99 cases of 2019 novel coronavirus pneumonia in Wuhan, China: a descriptive study, Lancet, 395, 507, 10.1016/S0140-6736(20)30211-7 Shen, 2020, Genomic diversity of SARS-CoV-2 in coronavirus disease 2019 patients, Clin. Infect. Dis., 71, 713, 10.1093/cid/ciaa203 Zhou, 2020, Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study, Lancet, 10.1016/S0140-6736(20)30566-3 Martines, 2020, Pathology and pathogenesis of SARS-CoV-2 associated with fatal coronavirus disease, United States, Emerg. Infect. Dis., 26, 2005, 10.3201/eid2609.202095 Assiri, 2013, Epidemiological, demographic, and clinical characteristics of 47 cases of Middle East respiratory syndrome coronavirus disease from Saudi Arabia: a descriptive study, Lancet Infect. Dis., 13, 752, 10.1016/S1473-3099(13)70204-4 Cao, 2020, A trial of lopinavir–ritonavir in adults hospitalized with severe Covid-19, N. Engl. J. Med., 395, 1054 Zahariadis, 2006, Risk of ruling out severe acute respiratory syndrome by ruling in another diagnosis: variable incidence of atypical bacteria coinfection based on diagnostic assays, Can. Respir. J. J. Can. Thorac. Soc., 13 Zheng, 2019, Mining, analyzing, and integrating viral signals from metagenomic data, Microbiome, 7, 1, 10.1186/s40168-019-0657-y Lin, 2020, Novel coronavirus pneumonia outbreak in 2019: computed tomographic findings in two cases, Korean J. Radiol., 21, 365, 10.3348/kjr.2020.0078 Guan, 2020, Clinical characteristics of coronavirus disease 2019 in China, N. Engl. J. Med., 382, 1708, 10.1056/NEJMoa2002032 McCullers, 2014, The co-pathogenesis of influenza viruses with bacteria in the lung, Nat. Rev. Microbiol., 12, 252, 10.1038/nrmicro3231 Chen, 2020, The microbial coinfection in COVID-19, Appl. Microbiol. Biotechnol., 1 Lansbury, 2020, Co-infections in people with COVID-19: a systematic review and meta-analysis, J. Infect., 81, 266, 10.1016/j.jinf.2020.05.046 Joseph, 2013, Bacterial and viral infections associated with influenza, Influenza and other Respiratory Viruses, 7, 105, 10.1111/irv.12089 Wang, 2020, Clinical characteristics of 138 hospitalized patients with 2019 novel coronavirus–infected pneumonia in Wuhan, China, J. Am. Med. Assoc., 323, 1061, 10.1001/jama.2020.1585 Wu, 2020, Co-infection with SARS-CoV-2 and influenza A virus in patient with pneumonia, China, Emerg. Infect. Dis., 26, 1324, 10.3201/eid2606.200299 Wan, 2020, Clinical features and treatment of COVID‐19 patients in northeast Chongqing, J. Med. Virol., 92, 797, 10.1002/jmv.25783 Kalantar-Zadeh, 2020, Considering the effects of microbiome and diet on SARS-CoV-2 infection: nanotechnology roles, ACS Nano, 14, 5179, 10.1021/acsnano.0c03402 Netea, 2020, Trained immunity: a tool for reducing susceptibility to and the severity of SARS-CoV-2 infection, Cell, 181, 969, 10.1016/j.cell.2020.04.042 Salas-Benito, 2015, Viral interference and persistence in mosquito-borne flaviviruses, J. Immunol. Res., 2015, 10.1155/2015/873404 Makoti, 2020, HIV and human Coronavirus coinfections: a historical perspective, Viruses, 12, 937, 10.3390/v12090937 Griffiths, 2011, The nature and consequences of coinfection in humans, J. Infect., 63, 200, 10.1016/j.jinf.2011.06.005 Van Der Hoek, 2006, Human coronavirus NL63, a new respiratory virus, FEMS (Fed. Eur. Microbiol. Soc.) Microbiol. Rev., 30, 760 Bengoechea, 2020, SARS‐CoV‐2, bacterial co‐infections, and AMR: the deadly trio in COVID‐19?, EMBO Mol. Med., 12, 10.15252/emmm.202012560 Griffiths, 2015, Reported co-infection deaths are more common in early adulthood and among similar infections, BMC Infect. Dis., 15, 411, 10.1186/s12879-015-1118-2 Nepogodiev, 2020, Mortality and pulmonary complications in patients undergoing surgery with perioperative SARS-CoV-2 infection: an international cohort study, Lancet, 396, 27, 10.1016/S0140-6736(20)31182-X Nickbakhsh, 2019, Virus–virus interactions impact the population dynamics of influenza and the common cold, Proc. Natl. Acad. Sci. Unit. States Am., 116, 27142, 10.1073/pnas.1911083116 Hoque, 2019, Metagenomic deep sequencing reveals association of microbiome signature with functional biases in bovine mastitis, Sci. Rep., 9, 1, 10.1038/s41598-019-49468-4 Konno, 2020, SARS-CoV-2 ORF3b is a potent interferon antagonist whose activity is increased by a naturally occurring elongation variant, Cell Rep., 32, 108185, 10.1016/j.celrep.2020.108185 Lambert, 2010, Influenza vaccines for the future, N. Engl. J. Med., 363, 2036, 10.1056/NEJMra1002842 Zheng, 2020, Co-infection of SARS-CoV-2 and influenza virus in early stage of the COVID-19 epidemic in Wuhan, China, J. Infect., 81, 128, 10.1016/j.jinf.2020.05.041 Azekawa, 2020, Co-infection with SARS-CoV-2 and influenza A virus, IDCases, 20, 10.1016/j.idcr.2020.e00775 Ding, 2020, The clinical characteristics of pneumonia patients coinfected with 2019 novel coronavirus and influenza virus in Wuhan, China, J. Med. Virol., 92, 1549, 10.1002/jmv.25781 Zhu, 2020, Co-infection with respiratory pathogens among COVID-2019 cases, Virus Res., 285, 198005, 10.1016/j.virusres.2020.198005 Garcia-Vidal, 2020, Incidence of co-infections and superinfections in hospitalized patients with COVID-19: a retrospective cohort study, Clin. Microbiol. Infect., 27, 83, 10.1016/j.cmi.2020.07.041 Kunutsor, 2020, Hepatic manifestations and complications of COVID-19: a systematic review and meta-analysis, J. Infect., 81, e72, 10.1016/j.jinf.2020.06.043 Zhang, 2020, Liver injury in COVID-19: management and challenges, The lancet Gastroenterology & Hepatology, 5, 428, 10.1016/S2468-1253(20)30057-1 Wander, 2020, COVID-19 Presenting as Acute Hepatitis, Am J Gastroenterol, 10.14309/ajg.0000000000000660 Alqahtani, 2020, Liver injury in COVID-19: the current evidence, United European Gastroenterology Journal, 8, 509, 10.1177/2050640620924157 Mehta, 2020, COVID-19: consider cytokine storm syndromes and immunosuppression, Lancet (London, England), 395, 1033, 10.1016/S0140-6736(20)30628-0 Huang, 2020, Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China, Lancet, 395, 497, 10.1016/S0140-6736(20)30183-5 Khinda, 2020, Association between markers of immune response at hospital admission and COVID‐19 disease severity and mortality: a meta‐analysis and meta‐regression, J. Med. Virol., 93, 1078, 10.1002/jmv.26411 Zhang, 2020, Clinical features and short-term outcomes of 221 patients with COVID-19 in Wuhan, China, J. Clin. Virol., 104364, 10.1016/j.jcv.2020.104364 Ali, 2020, Relationship between COVID-19 infection and liver injury: a review of recent data, Front. Med., 7, 458, 10.3389/fmed.2020.00458 Cai, 2020, COVID-19: abnormal liver function tests, J. Hepatol., 73, 566, 10.1016/j.jhep.2020.04.006 Epelboin, 2020, COVID-19 and dengue co-infection in a returning traveller, J. Trav. Med., 27, 10.1093/jtm/taaa114 Yan, 2020, Covert COVID-19 and false-positive dengue serology in Singapore, Lancet Infect. Dis., 20, 536, 10.1016/S1473-3099(20)30158-4 Lorenz, 2020, Have measures against COVID-19 helped to reduce dengue cases in Brazil?, Trav. Med. Infect. Dis., 10.1016/j.tmaid.2020.101827 Cardona‐Ospina, 2020, Dengue and COVID‐19, overlapping epidemics? An analysis from Colombia, J. Med. Virol., 93, 522, 10.1002/jmv.26194 Pinky, 2016, Coinfections of the respiratory tract: viral competition for resources, PLoS One, 11, 10.1371/journal.pone.0155589 Navarro, 2020, COVID-19 and dengue, co-epidemics in Ecuador and other countries in Latin America: pushing strained health care systems over the edge, Trav. Med. Infect. Dis., 37, 10.1016/j.tmaid.2020.101656 Lorenz, 2020, COVID-19 and Dengue Fever: A Dangerous Combination for the Health System in Brazil, Trav. Med. Infect. Dis., 35, 10.1016/j.tmaid.2020.101659 Tamuzi, 2020, Implications of COVID-19 in high burden countries for HIV/TB: a systematic review of evidence, BMC Infect. Dis., 20, 1, 10.1186/s12879-020-05450-4 Soriano, 2020, Impact of new coronavirus epidemics on HIV-infected patients, AIDS Rev., 22, 10.24875/AIDSRev.M20000031 Tang, 2020, Sustained IFN-I stimulation impairs MAIT cell responses to bacteria by inducing IL-10 during chronic HIV-1 infection, Science Advances, 6, eaaz0374, 10.1126/sciadv.aaz0374 Chaung, 2020, Coinfection with COVID‐19 and Coronavirus HKU1–the critical need for repeat testing if clinically indicated, J. Med. Virol., 92, 1785, 10.1002/jmv.25890 MacIntyre, 2018, The role of pneumonia and secondary bacterial infection in fatal and serious outcomes of pandemic influenza a (H1N1) pdm09, BMC Infect. Dis., 18, 637, 10.1186/s12879-018-3548-0 Manna, 2020, Molecular pathogenesis of secondary bacterial infection associated to viral infections including SARS-CoV-2, Journal of Infection and Public Health, 13, 1397, 10.1016/j.jiph.2020.07.003 Langford, 2020, Bacterial co-infection and secondary infection in patients with COVID-19: a living rapid review and meta-analysis, Clin. Microbiol. Infect., 26, 1622, 10.1016/j.cmi.2020.07.016 Morens, 2008, Predominant role of bacterial pneumonia as a cause of death in pandemic influenza: implications for pandemic influenza preparedness, J. Infect. Dis., 198, 962, 10.1086/591708 Klein, 2016, The frequency of influenza and bacterial coinfection: a systematic review and meta‐analysis, Influenza and other Respiratory Viruses, 10, 394, 10.1111/irv.12398 Huttner, 2020, COVID-19: don't neglect antimicrobial stewardship principles!, Clin. Microbiol. Infect., 26, 808, 10.1016/j.cmi.2020.04.024 Cox, 2020, Co-infections: potentially lethal and unexplored in COVID-19, The Lancet Microbe, 1, e11, 10.1016/S2666-5247(20)30009-4 Yeoh, 2021, Gut microbiota composition reflects disease severity and dysfunctional immune responses in patients with COVID-19, Gut, 70, 698, 10.1136/gutjnl-2020-323020 Mostafa, 2020, Metagenomic next-generation sequencing of nasopharyngeal specimens collected from confirmed and suspect covid-19 patients, mBio, 11 Kaul, 2020, Microbiome disturbance and resilience dynamics of the upper respiratory tract during influenza A virus infection, Nat. Commun., 11, 1 Bassetti, 2020, Bacterial and fungal superinfections in critically ill patients with COVID-19, Intensive Care Med., 46, 2071, 10.1007/s00134-020-06219-8 Lehmann, 2020, Community acquired co-infection in COVID-19: a retrospective observational experience, Clin. Infect. Dis., 72, 1450, 10.1093/cid/ciaa902 Fu, 2020, Secondary bacterial infections in critical ill patients of COVID-19, Open Forum Infectious Diseases, 7 Lai, 2020, Co-infections among patients with COVID-19: the need for combination therapy with non-anti-SARS-CoV-2 agents?, J. Microbiol. Immunol. Infect., 53, 505, 10.1016/j.jmii.2020.05.013 Ginsburg, 2020, COVID-19 pneumonia and the appropriate use of antibiotics, The Lancet Global Health, 8, e1453, 10.1016/S2214-109X(20)30444-7 Khatiwada, 2020, Lung microbiome and coronavirus disease 2019 (COVID-19): possible link and implications, Human Microbiome J., 17, 100073, 10.1016/j.humic.2020.100073 Peddu, 2020, Metagenomic analysis reveals clinical SARS-CoV-2 infection and bacterial or viral superinfection and colonization, Clin. Chem., 66, 966, 10.1093/clinchem/hvaa106 Gao, 2020, 2019 Novel coronavirus infection and gastrointestinal tract, J. Digestive Diseases, 21, 125, 10.1111/1751-2980.12851 Xiao, 2020, Evidence for gastrointestinal infection of SARS-CoV-2, Gastroenterology, 158, 1831, 10.1053/j.gastro.2020.02.055 Gu, 2020, Alterations of the gut microbiota in patients with coronavirus disease 2019 or H1N1 influenza, Clin. Infect. Dis., 71, 2669, 10.1093/cid/ciaa709 Salehi, 2020, Coronavirus disease 2019 (COVID-19): a systematic review of imaging findings in 919 patients, Am. J. Roentgenol., 1 Yang, 2020, Clinical course and outcomes of critically ill patients with SARS-CoV-2 pneumonia in Wuhan, China: a single-centered, retrospective, observational study, The Lancet Respiratory Medicine, 8, 475, 10.1016/S2213-2600(20)30079-5 Song, 2020, Fungal co-infections associated with global COVID-19 pandemic: a clinical and diagnostic perspective from China, Mycopathologia, 1 Clancy, 2020, PRO: the COVID-19 pandemic will result in increased antimicrobial resistance rates, JAC-Antimicrobial Resistance, 2, dlaa049, 10.1093/jacamr/dlaa049 Díaz-Muñoz, 2017, Viral coinfection is shaped by host ecology and virus–virus interactions across diverse microbial taxa and environments, Virus Evolution, 3, 10.1093/ve/vex011 Contou, 2020, Bacterial and viral co-infections in patients with severe SARS-CoV-2 pneumonia admitted to a French ICU, Ann. Intensive Care, 10, 1, 10.1186/s13613-020-00736-x Lee, 2020, ACE2 localizes to the respiratory cilia and is not increased by ACE inhibitors or ARBs, Nat. Commun., 11, 1 You, 2017, Simultaneous detection of respiratory syncytial virus and human metapneumovirus by one-step multiplex real-time RT-PCR in patients with respiratory symptoms, BMC Pediatr., 17, 89, 10.1186/s12887-017-0843-7 Avadhanula, 2006, Respiratory viruses augment the adhesion of bacterial pathogens to respiratory epithelium in a viral species-and cell type-dependent manner, J. Virol., 80, 1629, 10.1128/JVI.80.4.1629-1636.2006 Vareille, 2011, The airway epithelium: soldier in the fight against respiratory viruses, Clin. Microbiol. Rev., 24, 210, 10.1128/CMR.00014-10 Denney, 2018, The role of respiratory epithelium in host defence against influenza virus infection, Biomed. J., 41, 218, 10.1016/j.bj.2018.08.004 Wang, 2020, Case report: one case of coronavirus disease 2019 (COVID-19) in patient Co-infected by HIV with a low CD4+ T cell count, Int. J. Infect. Dis. Iverson, 2011, Influenza virus primes mice for pneumonia from Staphylococcus aureus, JID (J. Infect. Dis.), 203, 880, 10.1093/infdis/jiq113 Smith, 2013, Kinetics of coinfection with influenza A virus and Streptococcus pneumoniae, PLoS Pathog., 9, 10.1371/journal.ppat.1003238 Nguyen, 2015, Streptococcus pneumoniae enhances human respiratory syncytial virus infection in vitro and in vivo, PLoS One, 10, 10.1371/journal.pone.0127098 Roux, 2014, Ecology and evolution of viruses infecting uncultivated SUP05 bacteria as revealed by single-cell-and meta-genomics, Elife, 3, 10.7554/eLife.03125 Arunachalam, 2020, Systems biological assessment of immunity to mild versus severe COVID-19 infection in humans, Science, 369, 1210, 10.1126/science.abc6261 Rossi, 2020, Viral strategies predisposing to respiratory bacterial superinfections, Pediatr. Pulmonol., 55, 1061, 10.1002/ppul.24699 Luo, 2019, Combination of lymphocyte number and function in evaluating host immunity, Aging (Albany NY), 11, 12685, 10.18632/aging.102595 Qin, 2020, Dysregulation of immune response in patients with COVID-19 in Wuhan, China, Clin. Infect. Dis. Smith, 2016, A critical, nonlinear threshold dictates bacterial invasion and initial kinetics during influenza, Sci. Rep., 6, 1, 10.1038/srep38703 McArdle, 2018, When do co-infections matter?, Curr. Opin. Infect. Dis., 31, 209, 10.1097/QCO.0000000000000447 Kumar, 2018, Virological and immunological outcomes of coinfections, Clin. Microbiol. Rev., 31, 10.1128/CMR.00111-17 Roux, 2013, Chimeric viruses blur the borders between the major groups of eukaryotic single-stranded DNA viruses, Nat. Commun., 4, 1, 10.1038/ncomms3700 Suwanwongse, 2020, Can coinfection with influenza worsen COVID-19 outcomes?, Journal of Investigative Medicine High Impact Case Reports, 8, 10.1177/2324709620953282 Ma, 2020, Clinical characteristics of critically ill patients Co-infected with SARS-CoV-2 and the influenza virus in Wuhan, China, Int. J. Infect. Dis., 10.1016/j.ijid.2020.05.068 Wu, 2020, Liver diseases in COVID-19: etiology, treatment and prognosis, World J. Gastroenterol., 26, 2286, 10.3748/wjg.v26.i19.2286 Lozano-Sepulveda, 2020, SARS-CoV-2 another kind of liver aggressor, how does it do that?, Ann. Hepatol., 19, 592, 10.1016/j.aohep.2020.08.062 Zou, 2020, Characteristics of liver function in patients with SARS-CoV-2 and chronic HBV coinfection, Clin. Gastroenterol. Hepatol., 19, 597, 10.1016/j.cgh.2020.06.017 Lin, 2020, Patients with SARS-CoV-2 and HBV co-infection are at risk of greater liver injury, Genes & Diseases Verduyn, 2020 Saddique, 2020, Emergence of co-infection of COVID-19 and dengue: a serious public health threat, J. Infect., 81, e16, 10.1016/j.jinf.2020.08.009 Xu, 2020 Hu, 2020, Coinfection with HIV and SARS-CoV-2 in Wuhan, China: a 12-person case series, J. Acquir. Immune Defic. Syndr., 85, 1, 10.1097/QAI.0000000000002424 Yang, 2020, Clinical characteristics of COVID-19 patients with HIV coinfection in Wuhan, China, Expet Rev. Respir. Med., 1 Alothaid, 2020, Similarities between the effect of SARS-CoV-2 and HCV on the cellular level, and the possible role of ion channels in COVID19 progression: a review of potential targets for diagnosis and treatment, Channels, 14, 403, 10.1080/19336950.2020.1837439 Reddy, 2020, SARS‐CoV‐2 and the liver: considerations in hepatitis B and hepatitis C infections, Clinical Liver Disease, 15, 191, 10.1002/cld.970 Murphy, 2020, Effects of asthma and human rhinovirus A16 on the expression of SARS-CoV-2 entry factors in human airway epithelium, Am. J. Respir. Cell Mol. Biol., 63, 859, 10.1165/rcmb.2020-0394LE Orozco-Hernández, 2020, SARS-CoV-2 and rhinovirus/enterovirus co-infection in a critically ill young adult patient in Colombia, Biomedica, 40, 34, 10.7705/biomedica.5516 Motta, 2020, Adenovirus and novel coronavirus (SARS-Cov2) coinfection: a case report, IDCases, 22, 10.1016/j.idcr.2020.e00936 Nieto‐Moro, 2020, SARS‐CoV‐2 and Streptococcus pneumoniae coinfection as a cause of severe pneumonia in an infant, Pediatr. Pulmonol., 55, 2198, 10.1002/ppul.24916 Rodriguez-Nava, 2020, A retrospective study of coinfection of SARS-CoV-2 and Streptococcus pneumoniae in 11 hospitalized patients with severe COVID-19 pneumonia at a single center, Med. Sci. Mon. Int. Med. J. Exp. Clin. Res., 26 Duployez, 2020, Panton-valentine leukocidin–secreting staphylococcus aureus pneumonia complicating COVID-19, Emerg. Infect. Dis., 26, 1939, 10.3201/eid2608.201413 Cusumano, 2020, ofaa518 Hosoda, 2020, COVID-19 and Fatal Sepsis Caused by Hypervirulent Klebsiella pneumoniae, Japan, 2020, Emerg. Infect. Dis, 27 Oliva, 2020, Co-infection of SARS-CoV-2 with Chlamydia or Mycoplasma pneumoniae: a case series and review of the literature, Infection, 48, 871, 10.1007/s15010-020-01483-8 Amin, 2020, Association of mortality and recent Mycoplasma pneumoniae infection in COVID‐19 patients, J. Med. Virol., 93, 1180, 10.1002/jmv.26467 Arashiro, 2020, SARS-CoV-2 and Legionella co-infection in a person returning from a Nile cruise, J. Trav. Med., 27, 10.1093/jtm/taaa053 Moriguchi, 2020, A first case of meningitis/encephalitis associated with SARS-Coronavirus-2, Int. J. Infect. Dis., 94, 55, 10.1016/j.ijid.2020.03.062 Gallacher, 2020, Meningococcal meningitis and COVID-19 co-infection, BMJ Case Reports CP, 13 Crisan-Dabija, 2020 Liu, 2020 Sy, 2020, Previous and active tuberculosis increases risk of death and prolongs recovery in patients with COVID-19, Infectious Diseases, 52, 902, 10.1080/23744235.2020.1806353 Lai, 2020, COVID-19 associated with pulmonary aspergillosis: a literature review, J. Microbiol. Immunol. Infect., 54, 46, 10.1016/j.jmii.2020.09.004 Al-Hatmi, 2020, COVID-19 associated invasive candidiasis, J. Infect., 82, e45, 10.1016/j.jinf.2020.08.005