Kidney Transplantation in the Times of COVID-19 – A Literature Review

Ashraf Imam; Sadi A. Abukhalaf; Riham Imam; Samir Abu-Gazala; Hadar Merhav; Abed Khalaileh

doi:10.12659/AOT.925755

24 July 2020 : Review article

Kidney Transplantation in the Times of COVID-19 – A Literature Review

Ashraf Imam^1ACDEF*, Sadi A. Abukhalaf^1ABCEF, Riham Imam^1BCD, Samir Abu-Gazala^1AEF, Hadar Merhav^1ACD, Abed Khalaileh^1ABCEF

DOI: 10.12659/AOT.925755

Ann Transplant 2020; 25:e925755

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Table 2 Characteristics of all available reported kidney transplant recipients infected with COVID-19.

Study; Country	Number	Age; Sex	Years post-Tx; Donor	Comorbidities	Clinical presentation; Max Temp	Initial WBCC, NC, LC (×109/L)	Initial CRP (mg/L)	Baseline Cr (mg/dL)^	Initial Cr (mg/dL)
Banerjee; UK []¹²	#1	48;M	31; deceased	HTN	Cough, Fever, SOB; N/A	N/A	N/A	3.96	N/A
	#2	67;F	1; DBD	HTN, DM	Cough, Fever, SOB, Hypoxia; N/A	6, N/A, 0.8	83	1.7	2.54; AKI
	#3	54;F	0.25; deceased	DM, CMV infection	SOB, Hypoxia; N/A	11.2, N/A, 0.5	329	1	2.71; AKI
	#4	65;M	1.5; deceased	HTN	SOB, Chest pain; N/A	N/A	N/A	2	N/A
	#5	69;F	0.083; deceased	HTN, DM	SOB, Fever, V/D; 39°C	9.4, N/A, 0.3	N/A	1.9	N/A
	#6	54;M	7; N/A	HTN, HHA	Cough, Fever; 38.5°C	10, N/A, 4	N/A	1.6	2.1; AKI
	#7	45;M	2.5; N/A	HTN	Fever, Flu-like symptoms, Cough, SOB, Hypoxia; N/A	5.5, N/A, 0.3	198	5.1	11; AKI
Bartiromo; Italy []³	#1	36; F	25; deceased	SLS	Cough, Coryza, Fatigue; 36.3°C	N/A, High, Normal	67	1.5	1.77
Chen; China []²⁴	#1	49; M	6; DBD	HTN	Hyporexia, Cough, Fever, SOB; 38.6°C	3.4, 2.59, 0.4	74	1.24	1.89
Gandolfini; Italy []²⁵	#1	75; M	10; deceased	COPD, HTN, Obesity, CAD	Fever, SOB, Flu-like symptoms; 37.5°C	6.5, N/A, 0.8	180	2.1	2.2
	#2	52; F	0.66; DCD	HTN	Fever, SOB, D, Flu-like symptoms; 37.5°C	2.5, N/A, 0.11	158	1.3	2.4; AKI
Guillen; Spain []²⁶	#1	50; M	4; deceased	HTN, PTLD, SP	Fever, V, Dehydration, Cough, Conjunctivitis, Hypoxia; 38.2°C	10.5, N/A, 1.8 but developed lymphopenia	5	1.3	1.6; AKI
Huang; China []²⁷	#1	58; M	12; N/A	None	Cough, Fever, SOB, Hypoxia; 37.6°C	N/A but developed lymphopenia	N/A	N/A	N/A
Ning; China []²⁸	#1	29; M	1.5; Living	HTN	Fever, Fatigue, Chills, Hyporexia, N/V, Chest tightness, nasal stuffiness, Dizziness, Hematuria; 37.7°C	11.4, N/A, 1.5	N/A	N/A	1.1; AKI
Seminari; Italy []²⁹	#1	50; M	4; N/A	HTN, DM	Cough, Fever; 37.5°C	3.5, 1.8, 1.2 but developed lymphopenia	18.6	N/A	1.7
Wang; China []³⁰	#1	49; M	2; N/A	HTN, DM	Fever, Respiratory symptoms; N/A	7, 6, 0.6	22.7	N/A	1.4
Zhang; China []³¹	#1	38; M	0.5; DCD	None	Cough, Fever; 38.9°C	4.7, 2.6, 0.6	6	N/A	1.1
	#2	64; M	4; DCD	Bladder cancer	Fever, Anuria, Cough,, SOB, Flu-like symptoms; 38.3°C	17.6, 16, 0.5	337	N/A	4.6; AKI
	#3	37; F	0.66; DCD	HTN	Cough, Fever; 39°C	5.6, 3.9, 0.3	9.7	N/A	1.5
	#4	47; M	1.2; DCD	None	Cough, Fever, Flu-like symptoms; 39.8°C	4, 2.3, 0.5	13.3	N/A	1.6
	#5	38; M	3; DCD	HTN, DM	Cough, Fever, Flu-like symptoms; 39.1°C	6.4, 3.2, 0.9	33.7	N/A	1.5
Zhu; China []³²	#1	52; M	12; Living	None	Fatigue, SOB, Chest tightness and pain, N, Hyporexia, Abd.P, Cough, Fever, Headache, Weight loss; 38.9°C	9, 7, 1.13 but developed lymphopenia	30	1.57	1.62
Arpali; Turkey []³⁷	#1	28; F	0.5; Living	LLS	Fever, Fatigue, Sore throat, Rhinorrhea; 38°C	3.1, N/A, 0.3	5.7		0.92
Billa; USA []³⁸	#1	44; M	7; deceased	None	SOB; N/A			2.3	2.3; AKI
Fontana; Italy []³⁹	#1	61; M	15; deceased	NMZL, PD, NB	Fever, Chills; 38°C	5.4, 4.2, 1.2 but developed lymphopenia	41	1.5	1.9
Hsu; USA []⁴⁰	#1	39; M	3;	DCM, DM, HTN, Obesity	Fever, Headache, Sore throat, Cough, SOB, Fatigue, Myalgia, Dizziness, Chills; 38.8°C	2.5, N/A, 0.2	67	1	0.85
Kates, USA []⁴¹	#1	54; M	20; deceased	HTN, DM,	Fever, Chills, Fatigue, Cough, SOB, N/V/D; 40°C	6.2, N/A, 2 but developed lymphopenia		1.9	3.4; AKI
Johnson; USA []⁴²	#1	57; M	0.66; deceased	None	Fever, Chills, Hyporexia, Abd. bloating, Back pain, Fatigue, Myalgia, SOB, Anorexia, D, Oliguria; 38.2°C	1.4, 0.7, 0.3		2	3.2;
Kim; Korea []⁴³	#1	36; M	4; Living	None	Fever, Cough, Rhinorrhea, D, Oliguria, Chest discomfort; 38.5°C	6.6, 5.4, 0.6	46	1.47	2
	#2	46; M	9; deceased	DM	Cough; N/A	4, 2, 1.3	27	2	1.85
Fernández-Ruiz; Spain []⁴⁴	#1	78; M	8.3; N/A	HTN, Prostate CA	Fever, SOB
	#2	73; M	1.8; N/A	HTN, DM	Fever, SOB, Cough,
	#3	80; M	3.8; N/A	HTN, DM	SOB, Cough, Myalgia, Hyporexia
	#4	71; F	6; N/A	HTN	Fever, SOB, Cough, Sore throat
	#5	71; M	30; N/A	HTN, DM, CAD	Fever, Abd.P
	#6	76; M	14.8; N/A	HTN, Obesity	Fever, Rhinorrhea
	#7	39; M	16.8; N/A	HTN	Fever, Myalgia
	#8	65: M	6.5; N/A	HTN, DM, OSA	Fever, SOB, Cough
Nair; USA []⁴⁵	#1	51; M	0.42; deceased	HTN, DM, CAD	Fever, Chills, Cough	9.2, N/A, 1.1			0.88
	#2	37; M	7; living	HTN, DM	Cough, Chills, Nasal congestion, Myalgia	5, N/A, 2.4	180		1.93
	#3	63; F	11.6; living	HTN	Fever, Chills, Cough, Myalgia, Headache;	9, N/A, 1.2	34		1.2
	#4	30; F	3.7; living	HTN, DM	Fever, Myalgia, Headache, V	3.7, N/A, 1.2			1.5
	#5	56; M	20; deceased	HTN, DM	Fever, Cough, Fatigue	4, N/A, 0.3	306		4.8; AKI
	#6	80; M	13.8; living	HTN, DM, CAD	Fever, Chills, Fatigue, Myalgia, D	5, N/A, 0.2	87		1.9
	#7	45; M	3.4; deceased	HTN, DM	Fever, Cough, Myalgia, D	5.2, N/A, 1.1	38		1.74
	#8	68; M	11.6; N/A	HTN, DM	Fever, Cough, SOB	6.7, N/A, 0.5	240		1.46; AKI
	#9	75; F	8.6; living	HTN, CA	Fever, Cough, SOB, Fatigue	6.3, N/A, 0.4	50		1.3
	#10	57; F	11.6; deceased	HTN, DM	Cough, SOB, Chills, Fatigue	11, N/N, 1.4	230		1.6; AKI
Zhu; China []⁴⁶	#1	24; M		None	Fever; 38°C	N/A	30		2.24
	#2	55; M		CAD	Cough, SOB, Fatigu	N/A, N/A, 0.3	80		3.48
	#3	29; M		None	Fever, Cough, SOB, Fatigue, D; 38.8°C	N/A, N/A, 0.47	118		2.84
	#4	30; M		HTN	Fever, Cough, SOB, Fatigue; 39°C	N/A, N/A, 0.6	42		2.36
	#5	50; M		HTN	Fever, Cough, SOB, Fatigue; 38.6°C	N/A, N/A, 0.4	40		N
	#6	65; F		None	Fever, Cough, SOB, Fatigue, D; 38°C	N/A, N/A, 0.7	40		N
	#7	52; M		HTN, CAD	Fever, Cough, SOB, Fatigue; 38.9°C	N/A, N/A, 1	54		N
	#8	49; M		None	Fever, Cough, SOB, Fatigue, D; 39.2°C	N/A	49		N
	#9	59; M		HTN, COPD	Fever, Cough, SOB, Fatigue; 38.4°C	N/A, N/A, 0.4	100		5.2; AKI
	#10	37; F		HTN	Fever, Cough, SOB, Fatigue; 40°C	N/A, N/A, 0.2	34		2.14
								^*
Banerjee; UK []¹²	N/A		N/A	N/A	Aza, Pred	No change in ISMs	None	Recovered, N/A
	2032		N/A	1226	Tac, MMF, Pred	Tac, MMF stopped, Abx	Both	Died after 12d
	N/A		N/A	N/A	Tac, MMF, Pred	Tac, MMF stopped, Abx, oseltamivir	MV	Alive but suffers, 7d
	N/A		N/A	N/A	Tac, MMF, Pred	MMF stopped	Both	Alive but suffers
	N/A		N/A	N/A	Tac, MMF, Pred	MMF stopped, Abx, PC, furosemide, Blood transfusion	ICU	Alive but suffers, 7d
	N/A		N/A	N/A	Tac, MMF	MMF stopped, PC	None	Alive but suffers, 11d
	1907		N/A	502	Tac, Aza, Pred	Aza stopped, Tac reduced, Pred increased, HD	None	Recovered, 13d
Bartiromo; Italy []³	N/A		N/A	N/A	Tac, Pred	Tac stopped, hydroxychloroquine, Abx, lopinavir/ritonavir (for 2 days), darunavir/cobicistat	None	Recovered, 14d
Chen; China []²⁴	N/A		57/50	N/A	Tac, MMF, Pred	ISMs stopped, Ribavirin, Abx, IVIG, IVMP	ICU	Recovered, 32d
Gandolfini; Italy []²⁵	N/A		25/45	301	Tac, MMF, Pred	Tac, MMF, stopped, Hydroxychloroquine, Abx, Lopinavir/ritonavir	None	Died, 5d
	832		26/62	718	Tac, MMF, Pred	Tac, MMF, stopped, Abx, Hydroxychloroquine, Darunavir/cobicistat	None	Recovered, 8d
Guillen; Spain []²⁶	8900		N/A	N/A	Tac, Pred, Eve	Tac, Eve stopped, Abx, hydroxychloroquine, Lopinavir/Ritonavir, INF-β	Both	Alive but suffers, 12d
Huang; China []²⁷	N/A		N/A	N/A	MMF, Pred	MMF, Pred stopped, Abx, oseltamivir, Lopinavir/ritonavir, IVMP	MV	Died, 40d
Ning; China []²⁸	N/A		20/23 but elevated later	N/A	MMF, Pred, CsA	No change in ISMs, Abx, lopinavir/ritonavir, IVIG	None	Recovered, 12d
Seminari; Italy []²⁹	N/A		14/22	167 then 277	Tac, MMF	No change in ISMs, Abx	None	Recovered, 13d
Wang; China []³⁰	N/A		N/A	N/A	MMF, Pred, CsA	No change in ISMs, INF-α, ribavirin, lopinavir/ritonavir IVMP	None	Recovered, 12d
Zhang; China []³¹	185		66/41	193	Tac, MMF, Pred	MMF stopped, Tac reduced, oseltamivir	None	Recovered, 16d
	630		21/31	180	MMF, Pred	ISMs stopped, Abx, oseltamivir	None	Alive but suffers, 7d
	1015		70/49	160	Tac, MMF, Pred	Tac, MMF stopped, oseltamivir, IVIG	None	Recovered, 11d
	225		7/26	235	Tac, MMF, Pred	ISMs stopped, oseltamivir	None	Recovered, 19d
	195		20/21	248	Tac, MMF, Pred	No change in ISMs, oseltamivir	None	Recovered, 7d
Zhu; China []³²	N/A		30/29 but elevated later	N/A	Tac, MMF, Pred	ISMs stopped, Abx, IVMP, IVIG, INF-α, GAD	None	Recovered, 18d
Arpali; Turkey []³⁷					Tac, Pred	No change in ISMs, oseltamivir	None	Recovered, 7d
Billa; USA []³⁸	1100			285	Tac, MMF, Pred	Tac reduced, IVMP,	MV	Alive but suffers, 31d
Fontana; Italy []³⁹	N			N	Pred, CsA	CsA stopped, Pred increased, Abx, Hydroxycloroquine, Tocilizumab, IVIG,	None	Recovered, 22d
Hsu; USA []⁴⁰	1124		54/44	361	Tac, MMF, Pred	MMF stopped, hydroxychloroquine, remdesivir	ICU	Recovered, 15d
Kates, USA []⁴¹			34/48		Tac, MMF,	MMF stopped, Tac reduced, Pred, Abx, chloroquine, hydroxychloroquine,	None	Recovered, 16d
Johnson; USA []⁴²					Tac, MMF,	Tac, MMF reduced, Abx, hydroxychloroquine,	None	Recovered, 23d
Kim; Korea []⁴³			35/32		Tac, MMF, Pred	Tac, MMF stopped, lopinavir/ritonavir, IVMP, hydroxychloroquine	None	Recovered, 23d
			10/14		Tac, MMF, Pred	MMF stopped, hydroxychloroquine, Abx,	None	Recovered, 17d
Fernández-Ruiz; Spain []⁴⁴					Tac, Pred	Tac reduced, lopinavir/ritonavir	None	Died, 5d
					Tac, MMF, Pred	Tac reduced, MMF, Pred stopped, lopinavir/ritonavir, hydroxychloroquine, IVIG	None	Alive but suffers, 23d
					Tac, MMF, Pred	Tac reduced, MMF stopped, lopinavir/ritonavir, hydroxychloroquine	None	Alive but suffers, 28d
					Tac, MMF, Pred	Tac reduced, MMF, Pred stopped, lopinavir/ritonavir, hydroxychloroquine, IVIG, IVMP	None	Died, 16d
					Tac	Tac reduced, hydroxychloroquine, IVIG,	None	Alive but suffers, 9d
					MMF, Pred, Srl	MMF stopped, hydroxychloroquine, IVMP	None	Recovered, 13d
					Tac, Pred, Eve	Tac, Eve stopped, hydroxychloroquine, IVMP, Tocilizumab,	None	Alive but suffers, 16d
					Tac, MMF, Pred	Tac, MMF reduced, lopinavir/ritonavir, hydroxychloroquine	None	Alive but suffers, 17d
Nair; USA []⁴⁵					Tac, MMF, Pred, Eve	No change in ISMs	None	Recovered
					Tac, MMF, Pred	MMF stopped, hydroxychloroquine, azithromycin	None	Recovered
					Tac, MMF	MMF stopped, hydroxychloroquine, azithromycin, Abx	None	Recovered
					Tac, MMF, Pred	MMF stopped, hydroxychloroquine, azithromycin, Abx	None	Recovered
					Tac, MMF, Pred	Tac, MMF stopped, hydroxychloroquine, azithromycin, Abx	Both	Died
					Tac, MMF	Tac, MMF stopped, hydroxychloroquine, azithromycin, Abx, IVMP	Both	Recovered
					Tac, MMF, Pred	MMF stopped, hydroxychloroquine, azithromycin, Abx, IVMP	None	Recovered
					Tac, MMF, Pred	MMF stopped, hydroxychloroquine, azithromycin, Abx	ICU	Recovered
					Pred, Srl	Srl stopped, hydroxychloroquine, azithromycin	Both	Died
					Tac, MMF	MMF stopped, hydroxychloroquine, azithromycin, Abx, Pred	Both	Died
Zhu; China []⁴⁶			N		Tac, MMF, Pred	No change in ISMs, Avx	None	Recovered, 43d
			N		Tac, MMF, Pred	MMF stopped, Tac reduced, IVIG, Avx	MV	Recovered, 48d
			N		Tac, MMF, Pred	MMF stopped, IVMP, Avx	None	Recovered, 37d
			N		Tac, MMF, Pred	Tac, MMF stopped, IVIG, IVMP, Avx	None	Recovered, 37d
			104; N/A		Tac, MMF, Pred	Tac, MMF stopped, IVIG, IVMP, Avx	None	Recovered, 34d
			N		Tac, MMF	Tac, MMF stopped, IVIG, IVMP, Avx	MV	Alive but suffers, 49d
			94; N/N		Tac, MMF, Pred	Tac, MMF stopped, IVIG, IVMP, Avx	None	Recovered, 20d
			97; N/A		Tac, MMF	Tac, MMF stopped, IVMP, Avx	None	Recovered, 34d
			61; N/A		CsA, mizoribine	ISMs stopped, IVIG, IVMP, Avx	MV	Died, 6d
			163; N/A		Tac, MMF, Pred	Tac, MMF stopped, IVIG, IVMP, Avx	None	Recovered, 31d
^* Recovered indicates recovery of clinical symptoms and signs not negative COVID-19 testing; ^{^} Initial Creatinine (Cr) indicates Cr serum level in mg/dL unit before encountering COVID-19. ISMs – immunosuppressant medications; Max Temp – maximum temperature; DOI – duration of illness:; ICU – Intensive Care Unit; MV – mechanical ventilation; CRP – C-reactive protein; WBCC – white blood cell count; normal is 3.5–10 (×10/L); NC – neutrophil count, normal is 1.5–8 (×10/L); LC – lymphocyte count, normal is 1–3.5 (×10/L); AKI – acute kidney injury; Aza – azathioprine; MMF – mycophenolate mofetil; Tac – tacrolimus; Pred – prednisone; N/A – not available; DCD – donor after cardiac death; DBD – donor after brain death; Abx – antibiotics; Avx – antivirals; V/D – vomiting/diarrhea; PC – Paracetamol; SLS – Senior-Loken syndrome; LOS – loss of appetite; IVMP – intravenous methylprednisolone; IVIG – intravenous immunoglobin; D – Diarrhea; PTLD – post-transplant lymphoproliferative disease; SP – splenectomy; V – vomiting; Eve – everolimus:; INF-β – interferon beta; CsA – ciclosporin; N/V – nausea/vomiting; INF-α – interferon α; Abd.P – abdominal pain; GAD – glycyrrhizic acid diamine; CMV – cytomegalovirus; HHA – hereditary haemolytic anaemia; HD – hemodialysis; LDH – lactate dehydrogenase; ALT – alanine aminotransferase; AST – aspartate aminotransferase; LLS – lupus-like syndrome; NMZL – nodal marginal zone lymphoma; PD – Parkinson disease; NB – neurogenic bladder; DCM – dilated cardiomyopathy; CAD – coronary artery disease; OSA – obstructive sleep apnea; CA – cancer; Srl – Sirolimus.

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Kidney Transplantation in the Times of COVID-19 – A Literature Review

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