Factors Affecting Kidney Functions in One-Year Follow-up After COVID-19 in Kidney Transplant Patients

Year 2023, Volume: 5 Issue: 2, 124 - 134, 29.04.2023

Hakan Ozer , İsmail Baloğlu , Yasin Öztürk , Fethi Yönet , Halil Zeki Tonbul , Nedim Yılmaz Selcuk Kültigin Türkmen

https://doi.org/10.46310/tjim.1165344

Abstract

Background Coronavirus disease (COVID-19) is more severe, and mortality is higher in kidney transplantation (KTx) patients; it is still unclear how renal functions progress and the conditions affecting renal functions in the post-COVID-19 period. We aimed to investigate the changes in kidney functions and the factors affecting this change after COVID-19.
Material and Methods Forty-one kidney transplantation patients who were hospitalised for COVID-19 were included in this retrospective study. The patient's personal information, examination, and treatment information regarding their hospitalisation and follow-ups were obtained from the hospital system.
Results Patients with elevated serum creatinine in the first year post-COVID had higher baseline proteinuria and systemic immune inflammation index (SII). Proteinuria increased more in patients with a long transplantation period, hypertension, high basal creatinine, and SII. Also, proteinuria was higher in patients who developed AKI during the COVID period. In addition, baseline SII was an independent predictor of the change in serum creatinine and proteinuria.
Conclusions We found that patients with signs of increased inflammation, such as high SII were more fragile regarding renal functions. Therefore, the post-COVID-19 follow-up process of KTx patients with COVID-19 should be individualised.

Keywords

COVID-19, kidney functions, kidney transplantation, proteinuria, systemic immune inflammation index

References

• Farouk SS, Fiaccadori E, Cravedi P, Campbell KN. COVID-19 and the kidney: what we think we know so far and what we don't. J Nephrol. 2020 Dec;33(6):1213-8. doi: 10.1007/s40620-020-00789-y.
• Pecly IMD, Azevedo RB, Muxfeldt ES, Botelho BG, Albuquerque GG, Diniz PHP, Silva R, Rodrigues CIS. A review of Covid-19 and acute kidney injury: from pathophysiology to clinical results. J Bras Nefrol. 2021 Oct-Dec;43(4):551-71. doi: 10.1590/2175-8239-JBN-2020-0204.
• 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. 2020 Sep;31(9):1959-68. doi: 10.1681/ASN.2020060802.
• Ho QY, Sultana R, Lee TL, Thangaraju S, Kee T, Htay H. Coronavirus disease 2019 in kidney transplant recipients: a systematic review and meta-analysis. Singapore Med J. 2021 Oct 24. doi: 10.11622/smedj.2021171.
• Verma A, Khorsandi SE, Dolcet A, Prachalias A, Suddle A, Heaton N, Jassem W. Low prevalence and disease severity of COVID-19 in post-liver transplant recipients-A single centre experience. Liver Int. 2020 Aug;40(8):1972-1976. doi: 10.1111/liv.14552.
• Lippi G, Plebani M, Henry BM. Thrombocytopenia is associated with severe coronavirus disease 2019 (COVID-19) infections: A meta-analysis. Clin Chim Acta. 2020 Jul;506:145-148. doi: 10.1016/j.cca.2020.03.022.
• Yang YL, Wu CH, Hsu PF, Chen SC, Huang SS, Chan WL, Lin SJ, Chou CY, Chen JW, Pan JP, Charng MJ, Chen YH, Wu TC, Lu TM, Huang PH, Cheng HM, Huang CC, Sung SH, Lin YJ, Leu HB. Systemic immune-inflammation index (SII) predicted clinical outcome in patients with coronary artery disease. Eur J Clin Invest. 2020 May;50(5):e13230. doi: 10.1111/eci.13230.
• Nalbant A, Demirci T, Kaya T, Aydın A, Altındiş M, Güçlü E. Can prognostic nutritional index and systemic immune-inflammatory index predict disease severity in COVID-19? Int J Clin Pract. 2021 Oct;75(10):e14544. doi: 10.1111/ijcp.14544.
• Qin Z, Li H, Wang L, Geng J, Yang Q, Su B, Liao R. Systemic immune-inflammation index ıs associated with increased urinary albumin excretion: A population-based study. Front Immunol. 2022 Mar 21;13:863640. doi: 10.3389/fimmu.2022.863640.
• Hu B, Yang XR, Xu Y, Sun YF, Sun C, Guo W, Zhang X, Wang WM, Qiu SJ, Zhou J, Fan J. Systemic immune-inflammation index predicts prognosis of patients after curative resection for hepatocellular carcinoma. Clin Cancer Res. 2014 Dec 1;20(23):6212-22. doi: 10.1158/1078-0432.CCR-14-0442.
• Karras A, Livrozet M, Lazareth H, Benichou N, Hulot JS, Fayol A, Chauvet S, Jannot AS, Penet MA, Diehl JL, Godier A, Sanchez O, Mirault T, Thervet E, Pallet N. Proteinuria and clinical outcomes in hospitalized COVID-19 patients: A retrospective single-center study. Clin J Am Soc Nephrol. 2021 Apr 1;16(4):514-21. doi: 10.2215/CJN.09130620.
• Bajpai D, Deb S, Bose S, Gandhi C, Modi T, Katyal A, Saxena N, Patil A, Thakare S, Pajai AE, Haridas A, Keskar VS, Jawale SY, Sultan AG, Jamale TE. Recovery of kidney function after AKI because of COVID-19 in kidney transplant recipients. Transpl Int. 2021 Jun;34(6):1074-82. doi: 10.1111/tri.13886.
• Anton Pampols P, Trujillo H, Melilli E, Urban B, Sandino J, Favá A, Gutierrez E, Bestard O, Mancebo E, Sevillano A, Cruzado JM, Morales E. Immunosuppression minimization in kidney transplant recipients hospitalized for COVID-19. Clin Kidney J. 2021 Jan 29;14(4):1229-1235. doi: 10.1093/ckj/sfab025.
• Pei G, Zhang Z, Peng J, Liu L, Zhang C, Yu C, Ma Z, Huang Y, Liu W, Yao Y, Zeng R, Xu G. Renal involvement and early prognosis in patients with COVID-19 pneumonia. J Am Soc Nephrol. 2020 Jun;31(6):1157-65. doi: 10.1681/ASN.2020030276.
• Ferlicot S, Jamme M, Gaillard F, Oniszczuk J, Couturier A, May O, Grünenwald A, Sannier A, Moktefi A, Le Monnier O, Petit-Hoang C, Maroun N, Brodin-Sartorius A, Michon A, Dobosziewicz H, Andreelli F, Guillet M, Izzedine H, Richard C, Dekeyser M, Arrestier R, Sthelé T, Lefèvre E, Mathian A, Legendre C, Mussini C, Verpont MC, Pallet N, Amoura Z, Essig M, Snanoudj R, Brocheriou-Spelle I, François H, Belenfant X, Geri G, Daugas E, Audard V, Buob D, Massy ZA, Zaidan M; AP-HP/Universities/Inserm COVID-19 research collaboration. The spectrum of kidney biopsies in hospitalized patients with COVID-19, acute kidney injury, and/or proteinuria. Nephrol Dial Transplant. 2021 Feb 12:gfab042. doi: 10.1093/ndt/gfab042.
• Akilesh S, Nast CC, Yamashita M, Henriksen K, Charu V, Troxell ML, Kambham N, Bracamonte E, Houghton D, Ahmed NI, Chong CC, Thajudeen B, Rehman S, Khoury F, Zuckerman JE, Gitomer J, Raguram PC, Mujeeb S, Schwarze U, Shannon MB, De Castro I, Alpers CE, Najafian B, Nicosia RF, Andeen NK, Smith KD. Multicenter clinicopathologic correlation of kidney biopsies performed in COVID-19 patients presenting with acute kidney injury or proteinuria. Am J Kidney Dis. 2021 Jan;77(1):82-93.e1. doi: 10.1053/j.ajkd.2020.10.001.
• Lu L, Feng Y, Liu YH, Tan HY, Dai GH, Liu SQ, Li B, Feng HG. The systemic immune-inflammation index may be a novel and strong marker for the accurate early prediction of acute kidney injury in severe acute pancreatitis patients. J Invest Surg. 2022 May;35(5):962-6. doi: 10.1080/08941939.2021.1970864.
• Huang H, Liu Q, Zhu L, Zhang Y, Lu X, Wu Y, Liu L. Prognostic value of preoperative systemic immune-inflammation index in patients with cervical cancer. Sci Rep. 2019 Mar 1;9(1):3284. doi: 10.1038/s41598-019-39150-0.
• Karimi A, Shobeiri P, Kulasinghe A, Rezaei N. Novel systemic inflammation markers to predict COVID-19 prognosis. Front Immunol. 2021 Oct 22;12:741061. doi: 10.3389/fimmu.2021.741061.
• Fois AG, Paliogiannis P, Scano V, Cau S, Babudieri S, Perra R, Ruzzittu G, Zinellu E, Pirina P, Carru C, Arru LB, Fancellu A, Mondoni M, Mangoni AA, Zinellu A. The systemic inflammation index on admission predicts in-hospital mortality in COVID-19 patients. Molecules. 2020 Dec 4;25(23):5725. doi: 10.3390/molecules25235725.
• Henry BM, de Oliveira MHS, Benoit S, Plebani M, Lippi G. Hematologic, biochemical and immune biomarker abnormalities associated with severe illness and mortality in coronavirus disease 2019 (COVID-19): a meta-analysis. Clin Chem Lab Med. 2020 Jun 25;58(7):1021-1028. doi: 10.1515/cclm-2020-0369.
• Fukao Y, Nagasawa H, Nihei Y, Hiki M, Naito T, Kihara M, Gohda T, Ueda S, Suzuki Y. COVID-19-induced acute renal tubular injury associated with elevation of serum inflammatory cytokine. Clin Exp Nephrol. 2021 Nov;25(11):1240-1246. doi: 10.1007/s10157-021-02101-z.
• Wilk AJ, Rustagi A, Zhao NQ, Roque J, Martínez-Colón GJ, McKechnie JL, Ivison GT, Ranganath T, Vergara R, Hollis T, Simpson LJ, Grant P, Subramanian A, Rogers AJ, Blish CA. A single-cell atlas of the peripheral immune response in patients with severe COVID-19. Nat Med. 2020 Jul;26(7):1070-6. doi: 10.1038/s41591-020-0944-y.
• Ronco C, Reis T, Husain-Syed F. Management of acute kidney injury in patients with COVID-19. Lancet Respir Med. 2020 Jul;8(7):738-42. doi: 10.1016/S2213-2600(20)30229-0.
• Cheng Y, Luo R, Wang K, Zhang M, Wang Z, Dong L, Li J, Yao Y, Ge S, Xu G. Kidney disease is associated with in-hospital death of patients with COVID-19. Kidney Int. 2020 May;97(5):829-38. doi: 10.1016/j.kint.2020.03.005.
• Tomar B, Anders HJ, Desai J, Mulay SR. Neutrophils and neutrophil extracellular traps drive necroinflammation in COVID-19. Cells. 2020 Jun 2;9(6):1383. doi: 10.3390/cells9061383.
• Su H, Yang M, Wan C, Yi LX, Tang F, Zhu HY, 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. 2020 Jul;98(1):219-27. doi: 10.1016/j.kint.2020.04.003.
• Wang H, Li J, Gai Z, Kullak-Ublick GA, Liu Z. TNF-α deficiency prevents renal inflammation and oxidative stress in obese mice. Kidney Blood Press Res. 2017;42(3):416-27. doi: 10.1159/000478869.
• Varga Z, Flammer AJ, Steiger P, Haberecker M, Andermatt R, Zinkernagel AS, Mehra MR, Schuepbach RA, Ruschitzka F, Moch H. Endothelial cell infection and endotheliitis in COVID-19. Lancet. 2020 May 2;395(10234):1417-1418. doi: 10.1016/S0140-6736(20)30937-5.
• Migliorini A, Angelotti ML, Mulay SR, Kulkarni OO, Demleitner J, Dietrich A, Sagrinati C, Ballerini L, Peired A, Shankland SJ, Liapis H, Romagnani P, Anders HJ. The antiviral cytokines IFN-α and IFN-β modulate parietal epithelial cells and promote podocyte loss: implications for IFN toxicity, viral glomerulonephritis, and glomerular regeneration. Am J Pathol. 2013 Aug;183(2):431-40. doi: 10.1016/j.ajpath.2013.04.017.
• Liu J, Li S, Liu J, Liang B, Wang X, Wang H, Li W, Tong Q, Yi J, Zhao L, Xiong L, Guo C, Tian J, Luo J, Yao J, Pang R, Shen H, Peng C, Liu T, Zhang Q, Wu J, Xu L, Lu S, Wang B, Weng Z, Han C, Zhu H, Zhou R, Zhou H, Chen X, Ye P, Zhu B, Wang L, Zhou W, He S, He Y, Jie S, Wei P, Zhang J, Lu Y, Wang W, Zhang L, Li L, Zhou F, Wang J, Dittmer U, Lu M, Hu Y, Yang D, Zheng X. Longitudinal characteristics of lymphocyte responses and cytokine profiles in the peripheral blood of SARS-CoV-2 infected patients. EBioMedicine. 2020 May;55:102763. doi: 10.1016/j.ebiom.2020.102763.
• Halpern SE, Moris D, Shaw BI, Krischak MK, Olaso DG, Kesseli SJ, Ravindra K, McElroy LM, Barbas AS. The systemic immune-inflammation index predicts clinical outcomes in kidney transplant recipients. In Vivo. 2020 Nov-Dec;34(6):3349-60. doi: 10.21873/invivo.12173.
• Ergin G, Değer M, Köprü B, Derici Ü, Arınsoy T. High neutrophil to lymphocyte ratio predicts acute allograft rejection in kidney transplantation; a retrospective study. Turk J Med Sci. 2019 Apr 18;49(2):525-30. doi: 10.3906/sag-1811-41.
• Halazun KJ, Marangoni G, Hakeem A, Fraser SM, Farid SG, Ahmad N. Elevated preoperative recipient neutrophil-lymphocyte ratio is associated with delayed graft function following kidney transplantation. Transplant Proc. 2013 Nov;45(9):3254-7. doi: 10.1016/j.transproceed.2013.07.065.
• Siedlecki A, Irish W, Brennan DC. Delayed graft function in the kidney transplant. Am J Transplant. 2011 Nov;11(11):2279-96. doi: 10.1111/j.1600-6143.2011.03754.x.
• Naesens M, Lerut E, Emonds MP, Herelixka A, Evenepoel P, Claes K, Bammens B, Sprangers B, Meijers B, Jochmans I, Monbaliu D, Pirenne J, Kuypers DR. Proteinuria as a noninvasive marker for renal allograft histology and failure: An observational cohort study. J Am Soc Nephrol. 2016 Jan;27(1):281-92. doi: 10.1681/ASN.2015010062.
• Lombardi R, Ferreiro A, Ponce D, Claure-Del Granado R, Aroca G, Venegas Y, Pereira M, Chavez-Iñiguez J, Rojas N, Villa A, Colombo M, Carlino C, Guimarâes C, Younes-Ibrahim M, Rizo LM, Guzmán G, Varela C, Rosa-Diez G, Janiques D, Ayala R, Coronel G, Roessler E, Amor S, Osorio W, Rivas N, Pereira B, de Azevedo C, Flores A, Ubillo J, Raño J, Yu L, Burdmann EA, Rodríguez L, Galagarza-Gutiérrez G, Curitomay-Cruz J. Latin American registry of renal involvement in COVID-19 disease. The relevance of assessing proteinuria throughout the clinical course. PLoS One. 2022 Jan 27;17(1):e0261764. doi: 10.1371/journal.pone.0261764.
• 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; on behalf of the Mount Sinai COVID Informatics Center (MSCIC). AKI in hospitalized patients with COVID-19. J Am Soc Nephrol. 2021 Jan;32(1):151-60. doi: 10.1681/ASN.2020050615.
• Zhou F, Yu T, Du R, Fan G, Liu Y, Liu Z, Xiang J, Wang Y, Song B, Gu X, Guan L, Wei Y, Li H, Wu X, Xu J, Tu S, Zhang Y, Chen H, Cao B. Clinical course and risk factors for mortality of adult inpatients with COVID-19 in Wuhan, China: a retrospective cohort study. Lancet. 2020 Mar 28;395(10229):1054-62. doi: 10.1016/S0140-6736(20)30566-3.
• Lanzani C, Simonini M, Arcidiacono T, Messaggio E, Bucci R, Betti P, Avino M, Magni G, Maggioni C, Conte C, Querini PR, Ciceri F, Castagna A, Vezzoli G, Manunta P; Bio Angels for COVID-BioB Study Group. Role of blood pressure dysregulation on kidney and mortality outcomes in COVID-19. Kidney, blood pressure and mortality in SARS-CoV-2 infection. J Nephrol. 2021 Apr;34(2):305-14. doi: 10.1007/s40620-021-00997-0.
• Sardu C, Gambardella J, Morelli MB, Wang X, Marfella R, Santulli G. Hypertension, thrombosis, kidney failure, and diabetes: Is COVID-19 an endothelial disease? A comprehensive evaluation of clinical and basic evidence. J Clin Med. 2020 May 11;9(5):1417. doi: 10.3390/jcm9051417.
• AlGhatrif M, Cingolani O, Lakatta EG. The dilemma of coronavirus disease 2019, aging, and cardiovascular disease: Insights from cardiovascular aging science. JAMA Cardiol. 2020 Jul 1;5(7):747-8. doi: 10.1001/jamacardio.2020.1329.
• Alfano G, Damiano F, Fontana F, Ferri C, Melluso A, Montani M, Morisi N, Tei L, Plessi J, Giovanella S, Ligabue G, Mori G, Guaraldi G, Magistroni R, Cappelli G, Donati G. Immunosuppressive therapy reduction and early post-infection graft function in kidney transplant recipients with COVID-19. G Ital Nefrol. 2021 Dec 16;38(6):2021-vol6.
• Chauhan S, Meshram HS, Kute V, Patel H, Desai S, Dave R. Long-term follow-up of SARS-CoV-2 recovered renal transplant recipients: A single-center experience from India. Transpl Infect Dis. 2021 Dec;23(6):e13735. doi: 10.1111/tid.13735.