COVID-19 (SARS-CoV-2 infection) in lymphoma patients: A review

Table 1 Characteristics of included studies

Ref.	Location	Type of malignancy included	Duration of study	Total No. of pts with HM included	Matched COVID-19 control	No. of lymphoma pts	No. of NHL pts	No. of HL pts	Mortality rate attributed to COVID-19 (Global)	Mortality rate attributed to COVID-19 (Lymphoma)	Mortality rate attributed to COVID-19 (NHL)	Mortality rate attributed to COVID-19 (HL)
Cancer studies including lymphoma pts
Rüthrich et al[36], 2020	Europe	All	5 mo	435	2636	76	71	5	96/435 (22%)	20/76 (26%)	NR	NR
Lee et al[12], 2020	UK	All	1 mo	1044	282878	79	NR	NR	319/1044 (31%)	25/79 (31%)	NR	NR
Tian et al[50], 2020	China	All	9 wk	232	519	6	6	0	46/232 (20%)	2/6 (33%)	2/6 (33%)	NR
HM studies including lymphoma pts
Aries et al[34], 2020	UK	HM	2 mo	35	No	8	8	0	14/35 (40%)	NR	NR	/
Biernat et al[51], 2020	Poland	HM	1 mo	10	No	3	3	0	7/10 (70%)	NR	NR	/
Booth et al[52], 2020	UK	HM	2 mo	66	No	15	15	0	34/66 (52%)	6/15 (40%)	6/15 (40%)	/
Cattaneo et al[42], 2021	Italy	HM	1 mo	102	101	42	40	2	40/102 (39%)	17/42 (40%)	16/40 (40%)	1/2 (50%)
Fox et al[53], 2020	UK	HM	1 mo	55	No	17	17	0	19/55 (35%)	7/17 (41%)	7/17 (41%)	/
Garcìa-Suàrez et al[54], 2020	Spain	HM	8 wk	697	No	220	187	33	230/697 (33%)	68/220 (31%)	59/187 (32%)	9/33 (27%)
Infante et al[55], 2020	Spain	HM	1 mo	41	No	15	14	1	15/41 (37%)	NR	NR	NR
Lattenist et al[56], 2021	Belgium	HM	2 mo	12	No	2	2	0	6/12 (50%)	2/2 (100%)	2/2 (100%)	/
Malard et al[57], 2020	France	HM	1 mo	25	No	7	7	0	10/25 (40%)	0/7 (0%)	0/7 (0%)	/
Martín-Moro et al[33], 2020	Spain	HM	5 wk	34	No	6	5	1	11/34 (32%)	0/6 (0%)	0/5 (0%)	0/1 (0%)
Mehta et al[32], 2020	USA	HM	3 wk	54	No	20	15	5	20/54 (37%)	8/20 (40%)	5/15 (33%)	3/5 (60%)
Passamonti et al[37], 2020	Italy	HM	12 wk	536	No	170	153	17	198/536 (37%)	65/170 (38%)	62/153 (40%)	3/17 (18%)
Sanchez-Pina et al[58], 2020	Spain	HM	1 mo	39	53	12	NR	NR	14/39 (36%)	2/12 (14%)	NR	NR
van Doesum et al[59], 2020	Europe	HM	9 wk	59	No	17	15	2	NR	NR	NR	NR
Yigenoglu et al[29], 2021	Turkey	HM	15 wk	740	188897	250	223	27	103/740 (14%)	28/250 (11%)	24/223 (11%)	4/27 (14%)
Wood et al[35], 2020	Worldwide	HM	3 mo	250	No	79	68	11	70/250 (28%)	20/79 (25%)	16/68 (24%)	4/11 (36%)
Lymphoma studies
Regalado-Artamendi et al[40], 2021	Spain	Lymphoma	12 wk	177	No	177	158	9	61/177 (29%)	61/177 (29%)	NR	NR
Lamure et al[39], 2020	France	Lymphoma	8 wk	89	No	89	84	5	30/85 (34%)	30/85 (35%)	29/84 (34%)	1/5 (20%)
Laurenge et al[60], 2021	France	PCNSL	2 mo	13	No	13	13	/	3/13 (23%)	3/13 (23%)	3/13 (23%)

COVID-19: Coronavirus disease 2019; HM: Hematologic malignancy; HL: Hodgkin lymphoma; NHL: Non-Hodgkin lymphoma; NR: Not reported; PCNSL: Primary central nervous system lymphoma; pts: Patients; UK: United Kingdom; USA: United States of America.

Table 2 Prognostic factors associated with survival in lymphoma series

Ref.	Details on study cohort	Univariate analysis for predictors of death	Multivariate analysis for predictors of death
Regalado-Artamendi et al[40], 2021	Lymphoma patients	Age ≥ 70 yr	Age ≥ 70 yr
		Comorbidities	Comorbidities
		CURB65 ≥ 3	CURB ≥ 2
		Low platelet count	Active disease
		Low hemoglobin level
		High D-dimer
		C-reactive protein >10 mg/dL
		LDH > 300 U/L
		Active disease1 (reference to CR)
		DLBCL histology (reference to FL)
		High-risk lymphoma2 (reference to low risk)
Lamure et al[39], 2020	Hospitalized lymphoma patients	Age ≥ 70 yr	Age ≥ 70 yr
		Hypertension	Active disease
		Previous cancer
		Bendamustine treatment
		Active disease

¹Partial response or progression.

²High risk according to prognostic index at diagnosis. CR: Complete response; CURB65: Confusion, urea concentration, respiratory rate, blood pressure and age > 65; DLBCL: Diffuse large B cell lymphoma; FL: Follicular lymphoma; LDH: Lactate dehydrogenase.

Table 3 Case reports and case series of coronavirus disease 2019 infection in lymphoma patients

Ref.	No. of patients described	Sex	Age	Details on lymphoma diagnosis	Details on lymphoma treatment	Outcome of COVID-19 infection	Global outcome
Li et al[61], 2020	1	M	26 yr	PMLBCL	R-DA-EPOCH	Recovered	Alive
Tepasse et al[62], 2020	2	M	65 yr	DLBCL with CNS relapse	R-DeVIC	Not recovered	Dead
		M	66 yr	MCL in CR	Rituximab maintenance	Not recovered	Dead
O'Kelly et al[63], 2020	1			cHL second relapse	Pembrolizumab	Recovered	Alive
Baang et al[64], 2021	1	M	60 yr	Relapsed/Refractory MCL	R-CHOP	Recovered	Alive
Moore et al[65], 2020	1	F	63 yr	NHL	Obinotuzumab maintenance	Recovered	Alive
Alsuliman et al[66], 2020	2	M	71 yr	MCL relapsed	Ibrutinib	Recovered	Alive
		M	NR	MCL relapsed	Ibrutinib	Recovered	Alive
Hoffmann et al[67], 2021	3	F	68 yr	DLBCL, FL	R-CHOP	Recovered	Alive
		M	60 yr	DLBCL, FL	R-ICE	Not recovered	Dead
		M	75 yr	DLBCL	R-CHOP	Not recovered	Dead
Yonal-hindilerden et al[68], 2021	1	F	55 yr	Relapsed/Refractory cHL	Brentuximab	Not recovered	Dead
Fujii et al[69], 2021	1	M	43 yr	cHL	A + AVD	Recovered	Alive
Kamel, 2021	1	M	58 yr	ALCL	None	Not recovered	Dead
Santana et al[70], 2021	1	F	47 yr	FL	Rituximab maintenance	Recovered	Alive
Velier et al[71], 2021	1	F	61 yr	WM	None	Recovered	Dead
Pelcovits et al[72], 2021	1	M	43 yr	High Grade B Cell Lymphoma, NOS	R-CODOX-M/IVAC	Recovered	Alive
Otsuka et al[73], 2020	1	M	56 yr	MCL	R-hyper CVAD/MA	Not recovered	Dead

A + AVD: Brentuximab vedotin, dacarbazine, doxorubicin, vinblastine; ALCL: Anaplastic large-cell lymphoma; cHL: Classic Hodgkin lymphoma; CNS: Cerebral nervous system; COVID-19: Coronavirus disease 2019; CR: Complete remission; DLBCL: Diffuse large B-cell lymphoma; F: Female; FL: Follicular lymphoma; M: Male; MCL: Mantle cell lymphoma; NHL: Non-Hodgkin lymphoma; NOS: Not otherwise specified; PMLBCL: Primary mediastinal large B-cell lymphoma; R-CHOP: Rituximab, cyclophosphamide, doxorubicin, vincristine and prednisone; R-CODOX-M/IVAC: Rituximab, cyclophosphamide, vincristine, doxorubicin and methotrexate alternating with ifosfamide, etoposide and cytarabine; R-DA-EPOCH: Dose-adjusted etoposide, prednisone, vincristine, cyclophosphamide, doxorubicin and rituximab; R-DeVIC: Rituximab, dexamethasone, etoposide, ifosfamide carboplatin; R-hyper CVAD/MA: Rituximab/cyclophosphamide/vincristine sulfate/doxorubicin and hydrochloride/dexamethasone/methotrexate/cytarabine; R-ICE: Rituximab, ifosfamide, carboplatin and etoposide; WM: Waldenstrom macroglobulinemia.