Long-term complications of COVID-19

Amar D Desai, Michael Lavelle, Brian C Boursiquot, Elaine Y Wan, Amar D Desai, Michael Lavelle, Brian C Boursiquot, Elaine Y Wan

Abstract

SARS-CoV-2 has rapidly spread across the globe and infected hundreds of millions of people worldwide. As our experience with this virus continues to grow, our understanding of both short-term and long-term complications of infection with SARS-CoV-2 continues to grow as well. Just as there is heterogeneity in the acute infectious phase, there is heterogeneity in the long-term complications seen following COVID-19 illness. The purpose of this review article is to present the current literature with regards to the epidemiology, pathophysiology, and proposed management algorithms for the various long-term sequelae that have been observed in each organ system following infection with SARS-CoV-2. We will also consider future directions, with regards to newer variants of the virus and their potential impact on the long-term complications observed.

Keywords: COVID-19; SARS-CoV-2; long COVID-19; post-COVID-19; sequelae.

Conflict of interest statement

No conflicts of interest, financial or otherwise, are declared by the authors.

Figures

Figure 1.
Figure 1.
Schematic representation of long-term sequelae observed following COVID-19 infection. Created with BioRender.com.

References

    1. Dong E, Du H, Gardner L. An interactive web-based dashboard to track COVID-19 in real time. Lancet Infect Dis 20: 533–534, 2020. doi:10.1016/S1473-3099(20)30120-1.
    1. Faria NR, Mellan TA, Whittaker C, Claro IM, Candido DDS, Mishra S, et al. . Genomics and epidemiology of a novel SARS-CoV-2 lineage in Manaus, Brazil. medRxiv, 2021. doi:10.1101/2021.02.26.21252554.
    1. Planas D, Veyer D, Baidaliuk A, Staropoli I, Guivel-Benhassine F, Rajah MM, Planchais C, Porrot F, Robillard N, Puech J, Prot M, Gallais F, Gantner P, Velay A, Le Guen J, Kassis-Chikhani N, Edriss D, Belec L, Seve A, Courtellemont L, Péré H, Hocqueloux L, Fafi-Kremer S, Prazuck T, Mouquet H, Bruel T, Simon-Lorière E, Rey FA, Schwartz O. Reduced sensitivity of SARS-CoV-2 variant delta to antibody neutralization. Nature 596: 276–280, 2021. doi:10.1038/s41586-021-03777-9.
    1. Centers for Disease Control and Prevention. COVID-19 Weekly Cases and Deaths per 100,000 Population by Age, Race/Ethnicity, and Sex. 2021. .
    1. Nalbandian A, Sehgal K, Gupta A, Madhavan MV, McGroder C, Stevens JS, Cook JR, Nordvig AS, Shalev D, Sehrawat TS, Ahluwalia N, Bikdeli B, Dietz D, Der-Nigoghossian C, Liyanage-Don N, Rosner GF, Bernstein EJ, Mohan S, Beckley AA, Seres DS, Choueiri TK, Uriel N, Ausiello JC, Accili D, Freedberg DE, Baldwin M, Schwartz A, Brodie D, Garcia CK, Elkind MSV, Connors JM, Bilezikian JP, Landry DW, Wan EY. Post-acute COVID-19 syndrome. Nat Med 27: 601–615, 2021. doi:10.1038/s41591-021-01283-z.
    1. SeyedAlinaghi S, Afsahi AM, MohsseniPour M, Behnezhad F, Salehi MA, Barzegary A, Mirzapour P, Mehraeen E, Dadras O. Late complications of COVID-19; a systematic review of current evidence. Arch Acad Emerg Med 9: e14, 2021. doi:10.22037/aaem.v9i1.1058.
    1. Sudre CH, Murray B, Varsavsky T, Graham MS, Penfold RS, Bowyer RC, Pujol JC, Klaser K, Antonelli M, Canas LS, Molteni E, Modat M, Jorge Cardoso M, May A, Ganesh S, Davies R, Nguyen LH, Drew DA, Astley CM, Joshi AD, Merino J, Tsereteli N, Fall T, Gomez MF, Duncan EL, Menni C, Williams FMK, Franks PW, Chan AT, Wolf J, Ourselin S, Spector T, Steves CJ. Attributes and predictors of long COVID. Nat Med 27: 626–631, 2021. [Erratum in Nat Med 27: 1116, 2021]. doi:10.1038/s41591-021-01292-y.
    1. Gupta A, Madhavan MV, Sehgal K, Nair N, Mahajan S, Sehrawat TS, Bikdeli B, Ahluwalia N, Ausiello JC, Wan EY, Freedberg DE, Kirtane AJ, Parikh SA, Maurer MS, Nordvig AS, Accili D, Bathon JM, Mohan S, Bauer KA, Leon MB, Krumholz HM, Uriel N, Mehra MR, Elkind MSV, Stone GW, Schwartz A, Ho DD, Bilezikian JP, Landry DW. Extrapulmonary manifestations of COVID-19. Nat Med 26: 1017–1032, 2020. doi:10.1038/s41591-020-0968-3.
    1. Hoffmann M, Kleine-Weber H, Schroeder S, Krüger N, Herrler T, Erichsen S, Schiergens TS, Herrler G, Wu NH, Nitsche A, Müller MA, Drosten C, Pöhlmann S. SARS-CoV-2 cell entry depends on ACE2 and TMPRSS2 and is blocked by a clinically proven protease inhibitor. Cell 181: 271–280.e8, 2020. doi:10.1016/j.cell.2020.02.052.
    1. 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 526: 135–140, 2020. doi:10.1016/j.bbrc.2020.03.044.
    1. Pan X-W, Xu D, Zhang H, Zhou W, Wang L-H, Cui X-G. Identification of a potential mechanism of acute kidney injury during the COVID-19 outbreak: a study based on single-cell transcriptome analysis. Intensive Care Med 46: 1114–1116, 2020. doi:10.1007/s00134-020-06026-1.
    1. Ziegler CGK, Allon SJ, Nyquist SK, Mbano IM, Miao VN, Tzouanas CN, et al. . SARS-CoV-2 receptor ACE2 is an interferon-stimulated gene in human airway epithelial cells and is detected in specific cell subsets across tissues. Cell 181: 1016–1035.e19, 2020. doi:10.1016/j.cell.2020.04.035.
    1. Jin Y, Ji W, Yang H, Chen S, Zhang W, Duan G. Endothelial activation and dysfunction in COVID-19: from basic mechanisms to potential therapeutic approaches. Signal Transduct Target Ther 5: 293, 2020. doi:10.1038/s41392-020-00454-7.
    1. Zhao Y-M, Shang Y-M, Song W-B, Li Q-Q, Xie H, Xu Q-F, Jia JL, Li LM, Mao HL, Zhou XM, Luo H, Gao YF, Xu AG. Follow-up study of the pulmonary function and related physiological characteristics of COVID-19 survivors three months after recovery. EClinicalMedicine 25: 100463, 2020. doi:10.1016/j.eclinm.2020.100463.
    1. Ehrenfeld M, Tincani A, Andreoli L, Cattalini M, Greenbaum A, Kanduc D, Alijotas-Reig J, Zinserling V, Semenova N, Amital H, Shoenfeld Y. Covid-19 and autoimmunity. Autoimmun Rev 19: 102597, 2020. doi:10.1016/j.autrev.2020.102597.
    1. Ngai JC, Ko FW, Ng SS, To K-W, Tong M, Hui DS. The long-term impact of severe acute respiratory syndrome on pulmonary function, exercise capacity and health status. Respirology 15: 543–550, 2010. doi:10.1111/j.1440-1843.2010.01720.x.
    1. Shang J, Ye G, Shi K, Wan Y, Luo C, Aihara H, Geng Q, Auerbach A, Li F. Structural basis of receptor recognition by SARS-CoV-2. Nature 581: 221–224, 2020. doi:10.1038/s41586-020-2179-y.
    1. Carfì A, Bernabei R, Landi F; Gemelli Against COVID-19 Post-Acute Care Study Group. Persistent symptoms in patients after acute COVID-19. JAMA 324: 603–605, 2020. doi:10.1001/jama.2020.12603.
    1. Chopra V, Flanders SA, O'Malley M, Malani AN, Prescott HC. Sixty-day outcomes among patients hospitalized with COVID-19. Ann Intern Med 174: 576–578, 2021. doi:10.7326/M20-5661.
    1. Mandal S, Barnett J, Brill SE, Brown JS, Denneny EK, Hare SS, Heightman M, Hillman TE, Jacob J, Jarvis HC, Lipman MCI, Naidu SB, Nair A, Porter JC, Tomlinson GS, Hurst JR; ARC Study Group. 'Long-COVID': a cross-sectional study of persisting symptoms, biomarker and imaging abnormalities following hospitalisation for COVID-19. Thorax 76: 396–398, 2021. doi:10.1136/thoraxjnl-2020-215818.
    1. Martin-Villares C, Perez Molina-Ramirez C, Bartolome-Benito M, Bernal-Sprekelsen M; COVID ORL ESP Collaborative Group (*). Outcome of 1890 tracheostomies for critical COVID-19 patients: a national cohort study in Spain. Eur Arch Otorhinolaryngol 278: 1605–1612, 2021. doi:10.1007/s00405-020-06220-3.
    1. Salem AM, Al Khathlan N, Alharbi AF, Alghamdi T, AlDuilej S, Alghamdi M, Alfudhaili M, Alsunni A, Yar T, Latif R, Rafique N, Al Asoom L, Sabit H. The long-term impact of COVID-19 pneumonia on the pulmonary function of survivors. Int J Gen Med 14: 3271–3280, 2021. doi:10.2147/IJGM.S319436.
    1. Balbi M, Conti C, Imeri G, Caroli A, Surace A, Corsi A, Mercanzin E, Arrigoni A, Villa G, Di Marco F, Bonaffini PA, Sironi S. Post-discharge chest CT findings and pulmonary function tests in severe COVID-19 patients. Eur J Radiol 138: 109676, 2021. doi:10.1016/j.ejrad.2021.109676.
    1. McDonald LT. Healing after COVID-19: are survivors at risk for pulmonary fibrosis? Am J Physiol Lung Cell Mol Physiol 320: L257–L265, 2021. doi:10.1152/ajplung.00238.2020.
    1. Wichmann D. Autopsy findings and venous thromboembolism in patients with COVID-19. Ann Intern Med 173: 1030, 2020. doi:10.7326/L20-1206.
    1. Lutchmansingh DD, Knauert MP, Antin-Ozerkis DE, Chupp G, Cohn L, Dela Cruz CS, Ferrante LE, Herzog EL, Koff J, Rochester CL, Ryu C, Singh I, Tickoo M, Winks V, Gulati M, Possick JD. A clinic blueprint for post-coronavirus disease 2019 RECOVERY: learning from the past, looking to the future. Chest 159: 949–958, 2021. doi:10.1016/j.chest.2020.10.067.
    1. Raj SR, Arnold AC, Barboi A, Claydon VE, Limberg JK, Lucci V-EM, Numan M, Peltier A, Snapper H, Vernino S; American Autonomic Society. Long-COVID postural tachycardia syndrome: an American Autonomic Society statement. Clin Auton Res 31: 365–368, 2021. doi:10.1007/s10286-021-00798-2.
    1. Puntmann VO, Carerj ML, Wieters I, Fahim M, Arendt C, Hoffmann J, Shchendrygina A, Escher F, Vasa-Nicotera M, Zeiher AM, Vehreschild M, Nagel E. Outcomes of cardiovascular magnetic resonance imaging in patients recently recovered from coronavirus disease 2019 (COVID-19). JAMA Cardiol 5: 1265–1273, 2020. doi:10.1001/jamacardio.2020.3557.
    1. Dweck MR, Bularga A, Hahn RT, Bing R, Lee KK, Chapman AR, White A, Salvo GD, Sade LE, Pearce K, Newby DE, Popescu BA, Donal E, Cosyns B, Edvardsen T, Mills NL, Haugaa K. Global evaluation of echocardiography in patients with COVID-19. Eur Heart J Cardiovasc Imaging 21: 949–958, 2020. doi:10.1093/ehjci/jeaa178.
    1. Kang Y, Chen T, Mui D, Ferrari V, Jagasia D, Scherrer-Crosbie M, Chen Y, Han Y. Cardiovascular manifestations and treatment considerations in COVID-19. Heart 106: 1132–1141, 2020. doi:10.1136/heartjnl-2020-317056.
    1. Zou X, Chen K, Zou J, Han P, Hao J, Han Z. Single-cell RNA-seq data analysis on the receptor ACE2 expression reveals the potential risk of different human organs vulnerable to 2019-nCoV infection. Front Med 14: 185–192, 2020. doi:10.1007/s11684-020-0754-0.
    1. Lindner D, Fitzek A, Bräuninger H, Aleshcheva G, Edler C, Meissner K, Scherschel K, Kirchhof P, Escher F, Schultheiss HP, Blankenberg S, Püschel K, Westermann D. Association of cardiac infection With SARS-CoV-2 in confirmed COVID-19 autopsy cases. JAMA Cardiol 5: 1281–1285, 2020. doi:10.1001/jamacardio.2020.3551.
    1. Guzik TJ, Mohiddin SA, Dimarco A, Patel V, Savvatis K, Marelli-Berg FM, Madhur MS, Tomaszewski M, Maffia P, D'Acquisto F, Nicklin SA, Marian AJ, Nosalski R, Murray EC, Guzik B, Berry C, Touyz RM, Kreutz R, Wang DW, Bhella D, Sagliocco O, Crea F, Thomson EC, McInnes IB. COVID-19 and the cardiovascular system: implications for risk assessment, diagnosis, and treatment options. Cardiovasc Res 116: 1666–1687, 2020. doi:10.1093/cvr/cvaa106.
    1. Siripanthong B, Nazarian S, Muser D, Deo R, Santangeli P, Khanji MY, Cooper LT Jr, Chahal CAA. Recognizing COVID-19-related myocarditis: the possible pathophysiology and proposed guideline for diagnosis and management. Heart Rhythm 17: 1463–1471, 2020. doi:10.1016/j.hrthm.2020.05.001.
    1. Richter D, Guasti L, Koehler F, Squizzato A, Nistri S, Christodorescu R, Dievart F, Gaudio G, Asteggiano R, Ferrini M. Late phase of COVID-19 pandemic in general cardiology. A position paper of the ESC Council for Cardiology Practice. ESC Heart Fail 8: 3483–3494, 2021. doi:10.1002/ehf2.13466.
    1. Hendren NS, Drazner MH, Bozkurt B, Cooper LT Jr.. Description and proposed management of the acute COVID-19 cardiovascular syndrome. Circulation 141: 1903–1914, 2020. doi:10.1161/CIRCULATIONAHA.120.047349.
    1. Maron BJ, Udelson JE, Bonow RO, Nishimura RA, Ackerman MJ, Estes NAM 3rd, Cooper LT Jr, Link MS, Maron MS; American Heart Association Electrocardiography and Arrhythmias Committee of Council on Clinical Cardiology, Council on Cardiovascular Disease in Young, Council on Cardiovascular and Stroke Nursing, Council on Functional Genomics and Translational Biology, and American College of Cardiology. Eligibility and disqualification recommendations for competitive athletes with cardiovascular abnormalities: task force 3: hypertrophic cardiomyopathy, arrhythmogenic right ventricular cardiomyopathy and other cardiomyopathies, and myocarditis: a scientific statement from the American Heart Association and American College of Cardiology. Circulation 132: e273–e280, 2015. doi:10.1161/CIR.0000000000000239.
    1. Lopes RD, Macedo AVS, de Barros E Silva PGM, Moll-Bernardes RJ, Dos Santos TM, Mazza L, Feldman A, D'Andréa Saba Arruda G, de Albuquerque DC, Camiletti AS, de Sousa AS, de Paula TC, Giusti KGD, Domiciano RAM, Noya-Rabelo MM, Hamilton AM, Loures VA, Dionísio RM, Furquim TAB, De Luca FA, Dos Santos Sousa ÍB, Bandeira BS, Zukowski CN, de Oliveira RGG, Ribeiro NB, de Moraes JL, Petriz JLF, Pimentel AM, Miranda JS, de Jesus Abufaiad BE, Gibson CM, Granger CB, Alexander JH, de Souza OF; BRACE CORONA Investigators. Effect of discontinuing vs continuing angiotensin-converting enzyme inhibitors and angiotensin II receptor blockers on days alive and out of the hospital in patients admitted with COVID-19: a randomized clinical trial. JAMA 325: 254–264, 2021. doi:10.1001/jama.2020.25864.
    1. Bozkurt B, Kovacs R, Harrington B. Joint HFSA/ACC/AHA statement addresses concerns Re: using RAAS antagonists in COVID-19. J Card Fail 26: 370, 2020. doi:10.1016/j.cardfail.2020.04.013.
    1. Bikdeli B. Intermediate versus standard-dose prophylactic anticoagulation in critically ill patients with COVID-19 - INSPIRATION-S. In: American College of Cardiology Virtual Annual Scientific Session (ACC 2021), 2021. .
    1. Helms J, Tacquard C, Severac F, Leonard-Lorant I, Ohana M, Delabranche X, Merdji H, Clere-Jehl R, Schenck M, Fagot Gandet F, Fafi-Kremer S, Castelain V, Schneider F, Grunebaum L, Anglés-Cano E, Sattler L, Mertes PM, Meziani F; CRICS TRIGGERSEP Group (Clinical Research in Intensive Care and Sepsis Trial Group for Global Evaluation and Research in Sepsis). High risk of thrombosis in patients with severe SARS-CoV-2 infection: a multicenter prospective cohort study. Intensive Care Med 46: 1089–1098, 2020. doi:10.1007/s00134-020-06062-x.
    1. Klok FA, Kruip MJHA, van der Meer NJM, Arbous MS, Gommers D, Kant KM, Kaptein FHJ, van Paassen J, Stals MAM, Huisman MV, Endeman H. Confirmation of the high cumulative incidence of thrombotic complications in critically ill ICU patients with COVID-19: An updated analysis. Thromb Res 191: 148–150, 2020. doi:10.1016/j.thromres.2020.04.041.
    1. Hadid T, Kafri Z, Al-Katib A. Coagulation and anticoagulation in COVID-19. Blood Rev 47: 100761, 2021. doi:10.1016/j.blre.2020.100761.
    1. Lazzaroni MG, Piantoni S, Masneri S, Garrafa E, Martini G, Tincani A, Andreoli L, Franceschini F. Coagulation dysfunction in COVID-19: the interplay between inflammation, viral infection and the coagulation system. Blood Rev 46: 100745, 2021. doi:10.1016/j.blre.2020.100745.
    1. INSPIRATION Investigators; Sadeghipour P, Talasaz AH, Rashidi F, Sharif-Kashani B, Beigmohammadi MT. Effect of intermediate-dose vs standard-dose prophylactic anticoagulation on thrombotic events, extracorporeal membrane oxygenation treatment, or mortality among patients with COVID-19 admitted to the intensive care unit: the INSPIRATION randomized clinical trial. JAMA 325: 1620–1630, 2021. doi:10.1001/jama.2021.4152.
    1. Paranjpe I, Fuster V, Lala A, Russak AJ, Glicksberg BS, Levin MA, Charney AW, Narula J, Fayad ZA, Bagiella E, Zhao S, Nadkarni GN. Association of treatment dose anticoagulation with in-hospital survival among hospitalized patients with COVID-19. J Am Coll Cardiol 76: 122–124, 2020. doi:10.1016/j.jacc.2020.05.001.
    1. Al-Samkari H, Karp Leaf RS, Dzik WH, Carlson JCT, Fogerty AE, Waheed A, Goodarzi K, Bendapudi PK, Bornikova L, Gupta S, Leaf DE, Kuter DJ, Rosovsky RP. COVID-19 and coagulation: bleeding and thrombotic manifestations of SARS-CoV-2 infection. Blood 136: 489–500, 2020. doi:10.1182/blood.2020006520.
    1. Roberts LN, Whyte MB, Georgiou L, Giron G, Czuprynska J, Rea C, Vadher B, Patel RK, Gee E, Arya R. Postdischarge venous thromboembolism following hospital admission with COVID-19. Blood 136: 1347–1350, 2020. doi:10.1182/blood.2020008086.
    1. Patell R, Bogue T, Koshy A, Bindal P, Merrill M, Aird WC, Bauer KA, Zwicker JI. Postdischarge thrombosis and hemorrhage in patients with COVID-19. Blood 136: 1342–1346, 2020. doi:10.1182/blood.2020007938.
    1. Salisbury R, Iotchkova V, Jaafar S, Morton J, Sangha G, Shah A, Untiveros P, Curry N, Shapiro S. Incidence of symptomatic, image-confirmed venous thromboembolism following hospitalization for COVID-19 with 90-day follow-up. Blood Adv 4: 6230–6239, 2020. doi:10.1182/bloodadvances.2020003349.
    1. Leentjens J, van Haaps TF, Wessels PF, Schutgens REG, Middeldorp S. COVID-19-associated coagulopathy and antithrombotic agents-lessons after 1 year. Lancet Haematol 8: e524–e533, 2021. doi:10.1016/S2352-3026(21)00105-8.
    1. Liew AY, Piran S, Eikelboom JW, Douketis JD. Extended-duration versus short-duration pharmacological thromboprophylaxis in acutely Ill hospitalized medical patients: a systematic review and meta-analysis of randomized controlled trials. J Thromb Thrombolysis 43: 291–301, 2017. doi:10.1007/s11239-016-1461-1.
    1. Moores LK, Tritschler T, Brosnahan S, Carrier M, Collen JF, Doerschug K, Holley AB, Jimenez D, Le Gal G, Rali P, Wells P. Prevention, diagnosis, and treatment of VTE in patients with coronavirus disease 2019: CHEST guideline and expert panel report. Chest 158: 1143–1163, 2020. doi:10.1016/j.chest.2020.05.559.
    1. Bourguignon A, Beaulieu C, Belkaid W, Desilets A, Blais N. Incidence of thrombotic outcomes for patients hospitalized and discharged after COVID-19 infection. Thromb Res 196: 491–493, 2020. doi:10.1016/j.thromres.2020.10.017.
    1. Giannis D, Allen SL, Tsang J, Flint S, Pinhasov T, Williams S, Tan G, Thakur R, Leung C, Snyder M, Bhatia C, Garrett D, Cotte C, Isaacs S, Gugerty E, Davidson A, Marder GS, Schnitzer A, Goldberg B, McGinn T, Davidson KW, Barish MA, Qiu M, Zhang M, Goldin M, Matsagkas M, Arnaoutoglou E, Spyropoulos AC. Postdischarge thromboembolic outcomes and mortality of hospitalized patients with COVID-19: the CORE-19 registry. Blood 137: 2838–2847, 2021. doi:10.1182/blood.2020010529.
    1. Hull RD, Schellong SM, Tapson VF, Monreal M, Samama M-M, Nicol P, Vicaut E, Turpie AG, Yusen RD; EXCLAIM (Extended Prophylaxis for Venous ThromboEmbolism in Acutely Ill Medical Patients With Prolonged Immobilization) study. Extended-duration venous thromboembolism prophylaxis in acutely ill medical patients with recently reduced mobility: a randomized trial. Ann Intern Med 153: 8–18, 2010. doi:10.7326/0003-4819-153-1-201007060-00004.
    1. Huang C, Huang L, Wang Y, Li X, Ren L, Gu X, Kang L, Guo L, Liu M, Zhou X, Luo J, Huang Z, Tu S, Zhao Y, Chen L, Xu D, Li Y, Li C, Peng L, Li Y, Xie W, Cui D, Shang L, Fan G, Xu J, Wang G, Wang Y, Zhong J, Wang C, Wang J, Zhang D, Cao B. 6-month consequences of COVID-19 in patients discharged from hospital: a cohort study. Lancet 397: 220–232, 2021. doi:10.1016/S0140-6736(20)32656-8.
    1. Mikkelsen ME, Christie JD, Lanken PN, Biester RC, Thompson BT, Bellamy SL, Localio AR, Demissie E, Hopkins RO, Angus DC. The adult respiratory distress syndrome cognitive outcomes study: long-term neuropsychological function in survivors of acute lung injury. Am J Respir Crit Care Med 185: 1307–1315, 2012. doi:10.1164/rccm.201111-2025OC.
    1. Mazza MG, De Lorenzo R, Conte C, Poletti S, Vai B, Bollettini I, Melloni EMT, Furlan R, Ciceri F, Rovere-Querini P; COVID-19 BioB Outpatient Clinic Study group. Anxiety and depression in COVID-19 survivors: role of inflammatory and clinical predictors. Brain Behav Immun 89: 594–600, 2020. doi:10.1016/j.bbi.2020.07.037.
    1. Taquet M, Luciano S, Geddes JR, Harrison PJ. Bidirectional associations between COVID-19 and psychiatric disorder: retrospective cohort studies of 62 354 COVID-19 cases in the USA. Lancet Psychiatry 8: 130–140, 2021. doi:10.1016/S2215-0366(20)30462-4.
    1. Heneka MT, Golenbock D, Latz E, Morgan D, Brown R. Immediate and long-term consequences of COVID-19 infections for the development of neurological disease. Alzheimers Res Ther 12: 69, 2020. doi:10.1186/s13195-020-00640-3.
    1. Gu J, Gong E, Zhang B, Zheng J, Gao Z, Zhong Y, Zou W, Zhan J, Wang S, Xie Z, Zhuang H, Wu B, Zhong H, Shao H, Fang W, Gao D, Pei F, Li X, He Z, Xu D, Shi X, Anderson VM, Leong AS. Multiple organ infection and the pathogenesis of SARS. J Exp Med 202: 415–424, 2005. doi:10.1084/jem.20050828.
    1. Helms J, Kremer S, Merdji H, Clere-Jehl R, Schenck M, Kummerlen C, Collange O, Boulay C, Fafi-Kremer S, Ohana M, Anheim M, Meziani F. Neurologic features in severe SARS-CoV-2 infection. N Engl J Med 382: 2268–2270, 2020. doi:10.1056/NEJMc2008597.
    1. Kanjanaumporn J, Aeumjaturapat S, Snidvongs K, Seresirikachorn K, Chusakul S. Smell and taste dysfunction in patients with SARS-CoV-2 infection: a review of epidemiology, pathogenesis, prognosis, and treatment options. Asian Pac J Allergy Immunol 38: 69–77, 2020. doi:10.12932/AP-030520-0826.
    1. Vaira LA, Salzano G, Fois AG, Piombino P, De Riu G. Potential pathogenesis of ageusia and anosmia in COVID-19 patients. Int Forum Allergy Rhinol 10: 1103–1104, 2020. doi:10.1002/alr.22593.
    1. Kaseda ET, Levine AJ. Post-traumatic stress disorder: a differential diagnostic consideration for COVID-19 survivors. Clin Neuropsychol 34: 1498–1514, 2020. doi:10.1080/13854046.2020.1811894.
    1. Sachdeva M, Gianotti R, Shah M, Bradanini L, Tosi D, Veraldi S, Ziv M, Leshem E, Dodiuk-Gad RP. Cutaneous manifestations of COVID-19: report of three cases and a review of literature. J Dermatol Sci 98: 75–81, 2020. doi:10.1016/j.jdermsci.2020.04.011.
    1. Mirza FN, Malik AA, Omer SB, Sethi A. Dermatologic manifestations of COVID-19: a comprehensive systematic review. Int J Dermatol 60: 418–450, 2021. doi:10.1111/ijd.15168.
    1. Garrigues E, Janvier P, Kherabi Y, Le Bot A, Hamon A, Gouze H, Doucet L, Berkani S, Oliosi E, Mallart E, Corre F, Zarrouk V, Moyer JD, Galy A, Honsel V, Fantin B, Nguyen Y. Post-discharge persistent symptoms and health-related quality of life after hospitalization for COVID-19. J Infect 81: e4–e6, 2020. doi:10.1016/j.jinf.2020.08.029.
    1. Killion L, Beatty PE, Salim A. Rare cutaneous manifestation of COVID-19. BMJ Case Rep 14: e240863, 2021. doi:10.1136/bcr-2020-240863.
    1. Daneshgaran G, Dubin DP, Gould DJ. Cutaneous manifestations of COVID-19: an evidence-based review. Am J Clin Dermatol 21: 627–639, 2020. doi:10.1007/s40257-020-00558-4.
    1. Asghar F, Shamim N, Farooque U, Sheikh H, Aqeel R. Telogen effluvium: a review of the literature. Cureus 12: e8320, 2020. doi:10.7759/cureus.8320.
    1. Harrison S, Sinclair R. Telogen effluvium. Clin Exp Dermatol 27: 389–385, 2002. doi:10.1046/j.1365-2230.2002.01080.x.
    1. Nikolopoulou GB, Maltezou HC. COVID-19 in children: where do we stand? Arch Med Res S0188-4409(21)00148-X, 2021. doi:10.1016/j.arcmed.2021.07.002.
    1. Centers for Disease Control and Prevention (CDC). Health advisory on multisystem inflammatory syndrome in children (MIS-C) associated with coronavirus disease 2019, 2019. .
    1. World Health Organization. Multisystem Inflammatory Syndrome in Children and Adolescents with COVID-19: scientific brief. [2020 May 15]
    1. Hoste L, Van Paemel R, Haerynck F. Multisystem inflammatory syndrome in children related to COVID-19: a systematic review. Eur J Pediatr 180: 2019–2034, 2021. doi:10.1007/s00431-021-03993-5.
    1. Payne AB, Gilani Z, Godfred-Cato S, Belay ED, Feldstein LR, Patel MM, et al. . Incidence of multisystem inflammatory syndrome in children among US persons infected with SARS-CoV-2. JAMA Netw Open 4: e2116420, 2021. doi:10.1001/jamanetworkopen.2021.16420.
    1. Godfred-Cato S, Bryant B, Leung J, Oster ME, Conklin L, Abrams J, Roguski K, Wallace B, Prezzato E, Koumans EH, Lee EH, Geevarughese A, Lash MK, Reilly KH, Pulver WP, Thomas D, Feder KA, Hsu KK, Plipat N, Richardson G, Reid H, Lim S, Schmitz A, Pierce T, Hrapcak S, Datta D, Morris SB, Clarke K, Belay E; California MIS-C Response Team. COVID-19-associated multisystem inflammatory syndrome in children - United States, March-July 2020. MMWR Morb Mortal Wkly Rep 69: 1074–1080, 2020. [Erratum in MMWR Morb Mortal Wkly Rep 69: 1229, 2020]. doi:10.15585/mmwr.mm6932e2.
    1. Feldstein LR, Tenforde MW, Friedman KG, Newhams M, Rose EB, Dapul H, et al. . Characteristics and outcomes of US children and adolescents with Multisystem Inflammatory Syndrome in Children (MIS-C) compared with severe acute COVID-19. JAMA 325: 1074–1087, 2021. doi:10.1001/jama.2021.2091.
    1. Feldstein LR, Rose EB, Horwitz SM, Collins JP, Newhams MM, Son MBF, et al. . Multisystem inflammatory syndrome in U.S. Children and Adolescents. N Engl J Med 383: 334–346, 2020. doi:10.1056/NEJMoa2021680.
    1. Singh AK, Khunti K. COVID-19 and diabetes. Annu Rev 73: 2.1–2.19, 2022. doi: 10.1146/annurev-med-042220-011857.
    1. Unnikrishnan R, Misra A. Diabetes and COVID19: a bidirectional relationship. Nutr Diabetes 11: 21, 2021. doi:10.1038/s41387-021-00163-2.
    1. Rubino F, Amiel SA, Zimmet P, Alberti G, Bornstein S, Eckel RH, Mingrone G, Boehm B, Cooper ME, Chai Z, Del Prato S, Ji L, Hopkins D, Herman WH, Khunti K, Mbanya JC, Renard E. New-onset diabetes in Covid-19. N Engl J Med 383: 789–790, 2020. doi:10.1056/NEJMc2018688.
    1. Robbins-Juarez SY, Qian L, King KL, Stevens JS, Husain SA, Radhakrishnan J, Mohan S. Outcomes for patients with COVID-19 and acute kidney injury: a systematic review and meta-analysis. Kidney Int Rep 5: 1149–1160, 2020. doi:10.1016/j.ekir.2020.06.013.
    1. Su H, Yang M, Wan C, Yi L-X, Tang F, Zhu H-Y, Yi F, Yang HC, Fogo AB, Nie X, Zhang C. Renal histopathological analysis of 26 postmortem findings of patients with COVID-19 in China. Kidney Int 98: 219–227, 2020. doi:10.1016/j.kint.2020.04.003.
    1. Velez JCQ, Caza T, Larsen CP. COVAN is the new HIVAN: the re-emergence of collapsing glomerulopathy with COVID-19. Nat Rev Nephrol 16: 565–567, 2020. [Erratum in Nat Rev Nephrol 16: 614, 2020]. doi:10.1038/s41581-020-0332-3.
    1. Peleg Y, Kudose S, D'Agati V, Siddall E, Ahmad S, Nickolas T, Kisselev S, Gharavi A, Canetta P. Acute kidney injury due to collapsing glomerulopathy following COVID-19 infection. Kidney Int Rep 5: 940–945, 2020. doi:10.1016/j.ekir.2020.04.017.
    1. Jhaveri KD, Meir LR, Flores Chang BS, Parikh R, Wanchoo R, Barilla-LaBarca ML, Bijol V, Hajizadeh N. Thrombotic microangiopathy in a patient with COVID-19. Kidney Int 98: 509–512, 2020. doi:10.1016/j.kint.2020.05.025.
    1. Kudose S, Batal I, Santoriello D, Xu K, Barasch J, Peleg Y, Canetta P, Ratner LE, Marasa M, Gharavi AG, Stokes MB, Markowitz GS, D'Agati VD. Kidney biopsy findings in patients with COVID-19. J Am Soc Nephrol 31: 1959–1968, 2020. doi:10.1681/ASN.2020060802.
    1. Sharma P, Uppal NN, Wanchoo R, Shah HH, Yang Y, Parikh R, Khanin Y, Madireddy V, Larsen CP, Jhaveri KD, Bijol V; Northwell Nephrology COVID-19 Research Consortium. COVID-19-associated kidney injury: a case series of kidney biopsy findings. J Am Soc Nephrol 31: 1948–1958, 2020. doi:10.1681/ASN.2020050699.
    1. Golmai P, Larsen CP, DeVita MV, Wahl SJ, Weins A, Rennke HG, Bijol V, Rosenstock JL. Histopathologic and ultrastructural findings in postmortem kidney biopsy material in 12 patients with AKI and COVID-19. J Am Soc Nephrol 31: 1944–1947, 2020. doi:10.1681/ASN.2020050683.
    1. Santoriello D, Khairallah P, Bomback AS, Xu K, Kudose S, Batal I, Barasch J, Radhakrishnan J, D'Agati V, Markowitz G. Postmortem kidney pathology findings in patients with COVID-19. J Am Soc Nephrol 31: 2158–2167, 2020. doi:10.1681/ASN.2020050744.
    1. Chan L, Chaudhary K, Saha A, Chauhan K, Vaid A, Zhao S, Paranjpe I, Somani S, Richter F, Miotto R, Lala A, Kia A, Timsina P, Li L, Freeman R, Chen R, Narula J, Just AC, Horowitz C, Fayad Z, Cordon-Cardo C, Schadt E, Levin MA, Reich DL, Fuster V, Murphy B, He JC, Charney AW, Böttinger EP, Glicksberg BS, Coca SG, Nadkarni GN; Mount Sinai COVID Informatics Center (MSCIC). AKI in hospitalized patients with COVID-19. J Am Soc Nephrol 32: 151–160, 2021. doi:10.1681/ASN.2020050615.
    1. Harel Z, Wald R, Bargman JM, Mamdani M, Etchells E, Garg AX, Ray JG, Luo J, Li P, Quinn RR, Forster A, Perl J, Bell CM. Nephrologist follow-up improves all-cause mortality of severe acute kidney injury survivors. Kidney Int 83: 901–908, 2013. doi:10.1038/ki.2012.451.
    1. Meier P, Bonfils RM, Vogt B, Burnand B, Burnier M. Referral patterns and outcomes in noncritically ill patients with hospital-acquired acute kidney injury. Clin J Am Soc Nephrol 6: 2215–2225, 2011. doi:10.2215/CJN.01880211.
    1. Aiyegbusi OL, Hughes SE, Turner G, Rivera SC, McMullan C, Chandan JS, Haroon S, Price G, Davies EH, Nirantharakumar K, Sapey E, Calvert MJ; TLC Study Group. Symptoms, complications and management of long COVID: a review. J R Soc Med 114: 428–442, 2021. doi:10.1177/01410768211032850.
    1. Cheung KS, Hung IFN, Chan PPY, Lung KC, Tso E, Liu R, Ng YY, Chu MY, Chung TWH, Tam AR, Yip CCY, Leung KH, Fung AY, Zhang RR, Lin Y, Cheng HM, Zhang AJX, To KKW, Chan KH, Yuen KY, Leung WK. Gastrointestinal manifestations of SARS-CoV-2 infection and virus load in fecal samples from a Hong Kong Cohort: systematic review and meta-analysis. Gastroenterology 159: 81–95, 2020. doi:10.1053/j.gastro.2020.03.065.
    1. Wu Y, Guo C, Tang L, Hong Z, Zhou J, Dong X, Yin H, Xiao Q, Tang Y, Qu X, Kuang L, Fang X, Mishra N, Lu J, Shan H, Jiang G, Huang X. Prolonged presence of SARS-CoV-2 viral RNA in faecal samples. Lancet Gastroenterol Hepatol 5: 434–435, 2020. doi:10.1016/S2468-1253(20)30083-2.
    1. Xiao F, Tang M, Zheng X, Liu Y, Li X, Shan H. Evidence for gastrointestinal infection of SARS-CoV-2. Gastroenterology 158: 1831–1833.e3, 2020. doi:10.1053/j.gastro.2020.02.055.
    1. Xu Y, Li X, Zhu B, Liang H, Fang C, Gong Y, Guo Q, Sun X, Zhao D, Shen J, Zhang H, Liu H, Xia H, Tang J, Zhang K, Gong S. Characteristics of pediatric SARS-CoV-2 infection and potential evidence for persistent fecal viral shedding. Nat Med 26: 502–505, 2020. doi:10.1038/s41591-020-0817-4.
    1. Zuo T, Zhang F, Lui GCY, Yeoh YK, Li AYL, Zhan H, Wan Y, Chung ACK, Cheung CP, Chen N, Lai CKC, Chen Z, Tso EYK, Fung KSC, Chan V, Ling L, Joynt G, Hui DSC, Chan FKL, Chan PKS, Ng SC. Alterations in gut microbiota of patients with COVID-19 during time of hospitalization. Gastroenterology 159: 944–955.e8, 2020. doi:10.1053/j.gastro.2020.05.048.
    1. Donati Zeppa S, Agostini D, Piccoli G, Stocchi V, Sestili P. Gut microbiota status in COVID-19: an unrecognized player? Front Cell Infect Microbiol 10: 576551, 2020. doi:10.3389/fcimb.2020.576551.
    1. Zhang C, Shi L, Wang FS. Liver injury in COVID-19: management and challenges. Lancet Gastroenterol Hepatol 5: 428–430, 2020. doi:10.1016/S2468-1253(20)30057-1.
    1. Kanmaniraja D, Kurian J, Holder J, Gunther MS, Chernyak V, Hsu K, Lee J, Mcclelland A, Slasky SE, Le J, Ricci ZJ. Review of COVID-19, part 1: abdominal manifestations in adults and multisystem inflammatory syndrome in children. Clin Imaging 80: 88–110, 2021. doi:10.1016/j.clinimag.2021.06.025.
    1. An Y-W, Song S, Li W-X, Chen Y-X, Hu X-P, Zhao J, Li ZW, Jiang GY, Wang C, Wang JC, Yuan B, Liu HQ. Liver function recovery of COVID-19 patients after discharge, a follow-up study. Int J Med Sci 18: 176–186, 2021. doi:10.7150/ijms.50691.
    1. Wang Y, Liu S, Liu H, Li W, Lin F, Jiang L, Li X, Xu P, Zhang L, Zhao L, Cao Y, Kang J, Yang J, Li L, Liu X, Li Y, Nie R, Mu J, Lu F, Zhao S, Lu J, Zhao J. SARS-CoV-2 infection of the liver directly contributes to hepatic impairment in patients with COVID-19. J Hepatol 73: 807–816, 2020. doi:10.1016/j.jhep.2020.05.002.
    1. Spearman CW, Aghemo A, Valenti L, Sonderup MW. COVID-19 and the liver: a 2021 update. Liver Int 41: 1988–1998, 2021. doi:10.1111/liv.14984.
    1. Díaz LA, Idalsoaga F, Cannistra M, Candia R, Cabrera D, Barrera F, Soza A, Graham R, Riquelme A, Arrese M, Leise MD, Arab JP. High prevalence of hepatic steatosis and vascular thrombosis in COVID-19: a systematic review and meta-analysis of autopsy data. World J Gastroenterol 26: 7693–7706, 2020. doi:10.3748/wjg.v26.i48.7693.
    1. Stokes EK, Zambrano LD, Anderson KN, Marder EP, Raz KM, El Burai Felix S, Tie Y, Fullerton KE. Coronavirus Disease 2019 Case Surveillance - United States, January 22-May 30, 2020. MMWR Morb Mortal Wkly Rep 69: 759–765, 2020. doi:10.15585/mmwr.mm6924e2.
    1. Abdullahi A, Candan SA, Abba MA, Bello AH, Alshehri MA, Afamefuna Victor E, Umar NA, Kundakci B. Neurological and musculoskeletal features of COVID-19: a systematic review and meta-analysis. Front Neurol 11: 687, 2020. doi:10.3389/fneur.2020.00687.
    1. Li MY, Li L, Zhang Y, Wang XS. Expression of the SARS-CoV-2 cell receptor gene ACE2 in a wide variety of human tissues. Infect Dis Poverty 9: 45, 2020. doi:10.1186/s40249-020-00662-x.
    1. Marks M, Marks JL. Viral arthritis. Clin Med (Lond) 16: 129–134, 2016. doi:10.7861/clinmedicine.16-2-129.
    1. Zacharias H, Dubey S, Koduri G, D'Cruz D. Rheumatological complications of Covid 19. Autoimmun Rev 20: 102883, 2021. doi:10.1016/j.autrev.2021.102883.
    1. Piotrowicz K, Gąsowski J, Michel J-P, Veronese N. Post-COVID-19 acute sarcopenia: physiopathology and management. Aging Clin Exp Res 33: 2887–2898, 2021. doi:10.1007/s40520-021-01942-8.
    1. Fan E, Dowdy DW, Colantuoni E, Mendez-Tellez PA, Sevransky JE, Shanholtz C, Himmelfarb CRD, Desai SV, Ciesla N, Herridge MS, Pronovost PJ, Needham DM. Physical complications in acute lung injury survivors: a two-year longitudinal prospective study. Crit Care Med 42: 849–859, 2014. doi:10.1097/CCM.0000000000000040.
    1. Mosleh H, Moradi F, Mehdizadeh M, Ajdary M, Moeinzadeh A, Shabani R. Health concerns regarding the effect of the COVID-19 pandemic on male fertility. Clin Exp Reprod Med 48: 189–193, 2021. doi:10.5653/cerm.2021.04378.
    1. Khalili MA, Leisegang K, Majzoub A, Finelli R, Panner Selvam MK, Henkel R, Mojgan M, Agarwal A. Male fertility and the COVID-19 pandemic: systematic review of the literature. World J Mens Health 38: 506–520, 2020. doi:10.5534/wjmh.200134.
    1. Delle Fave RF, Polisini G, Giglioni G, Parlavecchio A, Dell'Atti L, Galosi AB. COVID-19 and male fertility: taking stock of one year after the outbreak began. Arch Ital Urol Androl 93: 115–119, 2021. doi:10.4081/aiua.2021.1.115.
    1. Li F, Lu H, Zhang Q, Li X, Wang T, Liu Q, Yang Q, Qiang L. Impact of COVID-19 on female fertility: a systematic review and meta-analysis protocol. BMJ Open 11: e045524, 2021. doi:10.1136/bmjopen-2020-045524.
    1. Kang M, Xin H, Yuan J, Taslim Ali Z, Liang Z, Zhang J, Hu T, Lau EHY, Zhang Y, Zhang M, Cowling BJ, Li Y, Wu P. Transmission dynamics and epidemiological characteristics of delta variant infections in China. medRxiv. 2021. doi:10.1101/2021.08.12.21261991.

Source: PubMed

Patrocinadores e Colaboradores

Condições médicas

Intervenções de drogas

3
Se inscrever