Correlation between ABO blood type, susceptibility to SARS-CoV-2 infection and COVID-19 disease severity: A systematic review

Soares, Danyela Martins Bezerra; Araújo, David Augusto Batista Sá; Souza, Jorge Luiz de Brito de; Maurício, Rebeca Bessa; Soares, Emanuela Martins Bezerra; Alves Neto, Franklin de Castro; Pinheiro, Maria Suelly Nogueira; Gama, Vitor Carneiro de Vasconcelos; Braga Neto, Pedro; Nóbrega, Paulo Ribeiro; Aragão, Gislei Frota

doi:10.1016/j.htct.2022.11.001

Danyela Martins Bezerra Soares

article conception and wrote the manuscript

data collection and analysis

read, revised and approved the final version of the manuscript

Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil

https://orcid.org/0000-0003-0084-7351

David Augusto Batista Sá Araújo

article conception and wrote the manuscript

data collection and analysis

read, revised and approved the final version of the manuscript

Universidade Federal do Ceará (UFC), Fortaleza, CE, Brazil

https://orcid.org/0000-0003-4082-1842

Jorge Luiz de Brito de Souza

article conception and wrote the manuscript

Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil

https://orcid.org/0000-0002-0421-5733

Rebeca Bessa Maurício

data collection and analysis

Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil

https://orcid.org/0000-0001-8686-1845

Emanuela Martins Bezerra Soares

data collection and analysis

Uniuersidade Federal do Cariri (UFCA), Barbalha, CE, Brazil

Franklin de Castro Alves Neto

data collection and analysis

Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil

Maria Suelly Nogueira Pinheiro

data collection and analysis

read, revised and approved the final version of the manuscript

Universidade Federal do Ceará (UFC), Fortaleza, CE, Brazil

Vitor Carneiro de Vasconcelos Gama

data collection and analysis

Hospital Geral de Fortaleza (HGF), Fortaleza, CE, Brazil

https://orcid.org/0000-0002-3242-9464

Pedro Braga Neto

read, revised and approved the final version of the manuscript

Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil

Paulo Ribeiro Nóbrega

article conception and wrote the manuscript

read, revised and approved the final version of the manuscript

Universidade Federal do Ceará (UFC), Fortaleza, CE, Brazil

https://orcid.org/0000-0002-0021-9358

Gislei Frota Aragão

read, revised and approved the final version of the manuscript

Universidade Estadual do Ceará (UECE), Fortaleza, CE, Brazil

*Corresponding author at: 1290, Rodolfo Teófilo, Fortaleza, CE, CEP: 60430-372, Brazi. E-mail address: paulo_r_med@yahoo.com.br (P.R. Nóbrega).

Conflicts of interest

The authors have no conflicts of interest to declare.

PICO criteria for Objective 1	Description
Population	Population at risk for SARS-CoV-2 infection (entire population)
Intervention (exposure)	ABO blood group
Comparison	Different blood groups by ABO classification system
Outcome	COVID-19 infection

PICO criteria for Objective 2	Description
Population	Population at risk for SARS-CoV-2 infection (entire population)
Intervention (exposure)	ABO blood group
Comparison	Different blood groups by ABO classification system
Outcome	COVID-19 severe infection, hospitalization, admission to intensive care unit (ICU), need for mechanical ventilation, and mortality

Databases	Descriptors utilized	Date of Search	Number of articles found
Embase	"blood group ABO system" AND "coronavirus disease 2019"	06/02/2022	256
PubMed	"COVID-19" AND "ABO blood-group system"	06/02/2022	132
Science Direct	"COVID-19" AND "ABO blood-group system"	06/02/2022	41
Scopus	"coronavirus disease 2019" and "blood group ABO system"	06/02/2022	216
Virtual Health Library (VHL)	"COVID-19" and "ABO Blood-Group system"	06/02/2022	135
Web of Science	"COVID-19" and "ABO blood-group system"	06/02/2022	18

Authors (year)	Type of study	Selection	Comparability	Outcome
RAY et al. (2020)¹⁴14 RayJG, Colacci M, Schuil MJ, Vermeulen MJ, Park AL. Non-ABO red cell antibodies and risk of COVID-19. Int J Infect Dis. 2021;108:179-82.	Cohort	****	**	***
ZIETZ et al. (2020)¹⁵15 Zietz M, Zucker J, Tatonetti NP. Associations between blood type and COVID-19 infection, intubation, and death. Nat Commun. 2020;11(1):l-6.	Cohort	***	**	***
SARDU et al. (2020)¹³13 Sardu C, Marfella R, Maggi P, Messina V, Cirillo P, Codella V, et al. Implications of ABO blood group in hypertensive patients with covid-19. BMC Cardiovasc Disord. 2020;20(1):1-10.	Cohort	**	**	***
BARNKOB et al. (2020)¹⁶16 Barnkob MB, Pottegárd A, St0vring H, Haunstrup TM, Homburg K, Larsen R, et al. Reduced prevalence of SARS-CoV-2 infection in ABO blood group O. Blood Adv. 2020;4(20):4990-3.	Cohort	***	**	***
MUNIZ-DIAZ et al. (2020)⁵5 Muniz-Diaz E, Llopis J, Parra R, Roig I, Ferrer G, Grifols J, et al. Relationship between the ABO blood group and COVID-19 susceptibility, severity and mortality in two cohorts of patients. Blood Transfusion. 2021;19(1):54.	Cohort	****	**	***
TEVATIA et al. (2020)¹⁷17 TEVATIA MS, SIDHU A, KALRA DK, BARANWAL AK, PANDIT P, GULERIA P, et al. Does PCR cycle threshold for SARS-CoV-2 have association with ABO blood group types? J Clin Diagnost Res. 2020;14(10).	Cohort	****	*	**
NAUFFAL et al. (2021)¹⁸18 Nauffal V, Achanta A, Goldhaber SZ, Piazza G Association of ABO blood group type with cardiovascular events in COVID-19. J. Thromb. Thrombolysis. 2021;51(3):584-6.	Cohort	****	**	***
NALBANT et al. (2022)¹⁹19 Nalbant A, Aydm A, Yaylac« S, Kaya T, Wermeulen CL, Cin-emre H. Association of ABO blood group and age with COVID-19 positive test. Revista da Associação Médica Brasileira. 2021;67:46-50.	Cohort	****	**	***
AMOROSO et al. (2021)²⁰20 Amoroso A, Magistroni P, Vespasiano F, Bella A, Bellino S, Puoti F, et al. of Italian network. Regional transplant coordinating C. HLA and ABO Polymorphisms May Influence SARS-CoV-2 Infection and COVID-19 Severity. Transplantation. 2020.	Cohort	****	*	***
SZYMANSKI et al. (2021)²¹21 Szymanski J, Mohrmann L, Carter J, Nelson R, Chekuri S, Assa A, et al. ABO blood type association with SARS-CoV-2 infection mortality: a single-center population in New York City. Transfusion. 2021;61(4):1064-70.	Cohort	***	*	***
BADEDI et al. (2021)²²22 Badedi M, Alnami A, Darraj H, Alrajhi A, Mutawwam D-A, Somaily M, et al. Clinical characteristics and ABO blood groups in COVID-19 patients, Saudi Arabia. Medicine. 2021;100(30).	Cohort	***	*	***
DE FREITAS DUTRA et al. (2021)²³23 de Freitas Dutra V, Bonet-Bub C, Yokoyama APH, Achkar R, Machado RRG, Assunção M, et ai. Anti-A and SARS-CoV-2: an intriguing association. Vox Sang. 2021;116(5):557-63.	Cohort	**	*	**
DOMÈNECH-MONTOLIU et al. (2021)²⁴24 Domènech-Montoliu S, Puig-Barberà J, Pac-Sa MR, Vidal-Utril-las P, Latorre-Poveda M, Rio-González AD, et al. ABO blood groups and the incidence of complications in COVID-19 patients: a population-based prospective cohort study. Int J Environ Res Public Health. 2021;18(19):10039.	Cohort	**	*	***
TAMAYO-VELASCO et al. (2021)²⁵25 Tamayo-Velasco A, Penarrubia Ponce MJ, Alvarez FJ, Gonzalo-Benito H, de la Fuente I, Perez-Gonzalez S, et al. Can the cytokine profile according to ABO blood groups be related to worse outcome in COVID-19 patients? yes, they can. Front Immunol. 2021: 4088.	Cohort	**	**	**
ISHAQetal. (2021)²⁶26 Ishaq U, Malik A, Malik J, Mehmood A, Qureshi A, Laique T, et al. Association of ABO blood group with COVID-19 severity, acute phase reactants and mortality. PLoS One. 2021;16(12): e0261432.	Cohort	**	*	***
KABRAH et al. (2021)⁵⁹59 Kabrah SM, Abuzerr SS, Baghdadi MA, Kabrah AM, Flemban AF, Bahwerth FS, et al. Susceptibility of ABO blood group to COVID-19 infections: clinico-hematological, radiological, and complications analysis. Medicine. 2021;100(52).	Cohort	***	*	***
MATZHOLD et al. (2021)²⁷27 Matzhold EM, Berghold A, Bemelmans MKB, Banfi C, Stelzl E, Kessler HH, et al. Lewis and ABO histo-blood types and the secretor status of patients hospitalized with COVID-19 implicate a role for ABO antibodies in susceptibility to infection with SARS-CoV-2. Transfusion. 2021;61(9):2736-45.	Cohort	***	*	**
MULLINS et al. (2021)²⁸28 Mullins J, Al-Tarbsheh AH, Chieng H, Chaukiyal P, Ghalib S, Jain E, et al. The association of ABO blood type with the risk and severity of COVID-19 infection. Am J Blood Res. 2021;11 (1):53.	Cohort	**	*	**
GRECO et al. (2021)²⁹29 Greco S, Bella A, Bonsi B, Fabbri N, Califano A, Morrone S, et al. SARS-CoV-2 infection and H1N1 vaccination: does a relationship between the two factors really exist? A retrospective analysis of a territorial cohort in Ferrara, Italy. Eur Rev Med Pharmacol Sei. 2021: 2795-801.	Cohort	****	**	**
AL-YOUHA et al. (2020)³⁰30 Al-Youha SA, Alduaij W, Al-Serri A, Almazeedi SM, Al-Haddad M, Jamal MH, et al. The impact of ABO blood groups on clinical outcomes and susceptibility to COVID-19: a retrospective study in an unselected population. Transfusion. 2021 ;61 (5):1631-41.	Cohort	***	**	**
FAN et al. (2020) (31)	Case control	****	**	***
AD'HIAH et al. (2020)³²32 Ad'hiah AH, Abdullah MH, Alsudani MY, Shnawa RM, Al-Sa'ady AJ, Allami RH, et al. Association between ABO blood groups and susceptibility to COVID-19: profile of age and gender in Iraqi patients. Egypt J Med Hum Genet. 2020;21 (1):1-10.	Case control	****	**	***
ZHAO et al. (2020) (33)	Case control	****	*	***
SAIFY et al. (2020)³⁴34 Saify K, Alborz MS, Saadat M. Susceptibility to the novel coronavirus disease (COVID-19) is associated with ABO and Rh blood groups: a case-control study from Afghanistan. Egypt J Med Hum Genet. 2021;22(1):l-5.	Case control	****	**	*
WU et al. (2020)³⁵35 Wu Y, Feng Z, Li P, Yu Q. Relationship between ABO blood group distribution and clinical characteristics in patients with COVID-19. Clin Chim Acta. 2020;509:220-3.	Case control	**	*	***
KHALIL et al. (2020)³⁶36 Khalil A, Feghali R, Hassoun M. The Lebanese COVID-19 cohort; a challenge for the ABO blood group system. Front Med. 2020;7:585341.	Case control	**	**	**
BADEDI et al. (2020)³⁷37 Badedi M, Makrami A, Alnami A. Co-morbidity and blood group type risk in coronavirus disease 2019 patients: a case -control study. J Infect Public Health. 2021;14(4):550-1.	Case control	***	**	***
BEHBOUDI et al. (2021)³⁸38 Behboudi E, Hamidi V, Gholizadeh F, Grala EM, Ghelmani Y, Nakhaie M, et al. Association between ABO blood groups and rhesus antigen and susceptibility to COVID-19 in the Yazd hospital. New Microbes New Infect. 2021;44:100934.	Case control	**	**	*
TORRES- ALARCÓN et al. (2021)³⁹39 Torres-Alarcón CG, García-Ruíz A, Cahete-Ibáhez CR, Morales-Pogoda II, Muhoz-Arce CM, BE Cid-Domínguez, et al. Blood system ABO antigens as risk factor for severity of SARS-CoV-2 infection. Gaceta médica de México. 2021;157(2):181-7.	Case control	**	*	**
KÍRÍSCietal. (2021)⁴⁰40 KÍRÍSCi Ö, ÖZLÜK S, TOPALCA US, KÖPRÜLÜ ND. Relationship of ABO blood groups to SARS-COV-2 infection causing COVID-19 disease. Konuralp Med J. 2021;13(1):18-23.	Case control	**	**	**
KOLIN et al. (2020)⁴¹41 Ko lin DA, Kulm S, Christos PJ, Elemento O. Clinical, regional, and genetic characteristics of Covid-19 patients from UK Bio-bank. PLoS One. 2020;15(11):e0241264.	Case control	****	**	**
GAMBOA-AGUILAR et al. (2022)⁴²42 Gamboa-Aguilar J, Zamorano-Montano AC, Enriquez-Osorio A, Torres-Cubillas W, López-Arroyo JL, Chapol JAM, et al. Abo blood group, atherothrombotic comorbidities, and COVID-19: a case-control study of their association in the Mexican population. Arch. Med. Res. 2022;53(1):100-8.	Case control	***	***	**
LATZ et al. (2020)⁴³43 Latz CA, DeCarlo C, Boitano L, Png C, Patell R, Conrad MF, et al. Blood type and outcomes in patients with COVID-19. Ann. Hematol. 2020;99(9):2113-8.	Cross-sectional	**	**	**
LIU et al. (2020)⁶6 Liu N, Zhang T, Ma L, Zhang H, Wang H, Wei W, et al. The impact of ABO blood group on COVID-19 infection risk and mortality: a systematic review and meta-analysis. Blood Rev. 2021;48:100785.	Cross-sectional	**	*	**
HOILAND et al. (2020)⁴⁴44 Hoiland RL, Fergusson NA, Mitra AR, Griesdale DE, Devine DV, Stukas S, et al. The association of ABO blood group with indices of disease severity and multiorgan dysfunction in COVID-19. Blood Adv. 2020;4(20):4981-9.	Cross-sectional	***	**	**
GÖKERetal. (2020)⁴⁵45 Göker H, Karakulak EA, Demiroglu H, Ceylan ÇMA, Büyükasik Y, Inkaya AÇ, et al. The effects of blood group types on the risk of COVID-19 infection and its clinical outcome. Turk] Med Sei. 2020;50(4):679-83.	Cross-sectional	***	**	**
KOTILA et al. (2020)⁴⁶46 Kotila TR, Alonge TO, Fowotade A, Famuyiwa 01, Akinbile AS. Association of the ABO blood group with SARS-CoV-2 infection in a community with low infection rate. Vox Sang. 2021;116(8):910-5.	Cross-sectional	**	*	**
YAYLACI et al. (2020)⁴⁷47 Yaylacî S, Dheir H, íssever K, Gene AB, Senocak D, Kocayigit H, et al. The effect of abo and rh blood group antigens on admission to intensive care unit and mortality in patients with COVID-19 infection. Revista da Associação Médica Brasileira. 2020;66:86-90.	Cross-sectional	*	**	**
SOLMAZ et al. (2020)⁴⁸48 Solmaz I, Araç S. ABO blood groups in COVID-19 patients; cross-sectional study. Int. J. Clin. Pract. 2021;75(4):el3927.	Cross-sectional	***	*	**
AL KUWARI et al. (2020)⁴⁹49 Al Kuwari HM, Rahim HFA, Abu-Raddad LJ, Abou-Samra A-B, Al Kanaani Z, Al Khal A, et al. Epidemiological investigation of the first 5685 cases of SARS-CoV-2 infection in Qatar, 28 Febru-ary-18 April 2020. BMJ Open. 2020;10(10):e040428.	Cross-sectional	***	**	**
ALMADHI et al. (2021)⁵⁰50 Almadhi MA, Abdulrahman A, Alawadhi A, Rabaan AA, Atkin S, AlQahtani M. The effect of ABO blood group and antibody class on the risk of COVID-19 infection and severity of clinical outcomes. Sei Rep. 2021;ll(1):l-5.	Cross-sectional	***	**	**
AKTIMUR et al. (2020)⁵¹51 Aktimur SH, Ahmet S, Yazicioglu B, Gunes AK, Serhat G The assessment of the relationship between ABO blood groups and Covid-19 infection. Int J Hematol Oncol. 2020;31(3):121-5.	Cross-sectional	***	**	**
ESREF et al. (2020)⁵²52 Esref A, Solmaz I, Akkoc H, Donmezdil S, Karahan Z, Safak K, et al. Association between the Rh blood group and the Covid-19 susceptibility. Int J Hematol Oncol. 2020;32 (2):081-6.	Cross-sectional	***	*	**
MUNOZ-CULLA et al. (2021)⁵³53 Muhoz-Culla M, Roncancio-Clavijo A, Martinez B, Gorostidi-Aicua M, Pineiro L, Azkune A, et al. O group is a protective factor for COVID19 in Basque population. PLoS One. 2021;16(4): e0249494.	Cross-sectional	***	*	**
KHASAYESI et al. (2021)⁵⁴54 Khasayesi M, Kashi Z, Ilali NM, Ghasemian R, Eslamijoubari M, Hosseini-Khah Z. Association of ABO and rhesus blood groups with the severity of SARS-CoV-2 infection: a cross-sectional analytical study. J Clin Diagnost Res. 2021;15(12).	Cross-sectional	**	*	**
PASANGHA et al. (2020)⁵⁵55 Pasangha E, Dhali A, D'Souza C, Umesh S. Are blood groups related to the distribution and severity of COVID-19? A cross-sectional study in a tertiary care hospital in South India. Qatar Med J.2021;2021(3):63.	Cross-sectional	*	**	**
KOMAL et al. (2021)⁵⁶56 Komal A, Noreen M, Akhtar J, Imran M, Jamal M, Atif M, et al. Analyses of ABO blood groups with susceptibility and symptomatic variations of COVID-19 infection, a questionnaire-based survey. APMIS. 2021;129(10):579-86.	Cross-sectional	**	*	*
HALIM et al. (2021)⁵⁷57 Halim MR, Saha S, Haque IU, Jesmin S, Nishat RJ, Islam AA, et al. ABO blood group and outcomes in patients with COVID-19 admitted in the intensive care unit (ICU): a retrospective study in a tertiary-level hospital in Bangladesh. J Multidiscip Healthc. 2021;14:2429.	Cross-sectional	***	*	**
HERMEL et al. (2021)⁵⁸58 Hermel DJ, Spierling Bagsic SR, Costantini CL, Mason JR, Gahvari ZJ, Saven A. ABO phenotype and clinical correlates of COVID-19 severity in hospitalized patients. Future Sei OA. 2021;7(8):FSO735.	Cross-sectional	***	**	**

Authors, year, place of study	Type of study/ Newcastle score	Sample size (n)	Outcomes of interest	Main results
SOLMAZ et al, 2020, Turkey⁴⁸48 Solmaz I, Araç S. ABO blood groups in COVID-19 patients; cross-sectional study. Int. J. Clin. Pract. 2021;75(4):el3927.	Cross-sectional / 6	128,758 1667 cases^* * Study sample 1 (hospitalized). 127,091 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
AL KUWARI et al, 2020, Pakistan.⁴⁹49 Al Kuwari HM, Rahim HFA, Abu-Raddad LJ, Abou-Samra A-B, Al Kanaani Z, Al Khal A, et al. Epidemiological investigation of the first 5685 cases of SARS-CoV-2 infection in Qatar, 28 Febru-ary-18 April 2020. BMJ Open. 2020;10(10):e040428.	Cross-sectional / 7	3870 1935 cases^* * Study sample 1 (hospitalized). 1935 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group B was more prevalent in COVID patients compared to controls, Group AB was less prevalent in patients
KOTILA et al, 2020, Nigeria⁴⁶46 Kotila TR, Alonge TO, Fowotade A, Famuyiwa 01, Akinbile AS. Association of the ABO blood group with SARS-CoV-2 infection in a community with low infection rate. Vox Sang. 2021;116(8):910-5.	Cross-sectional / 5	9440 302 cases^ Study sample 2 (outpatients). 9138 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group B and AB were more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
LATZ et al, 2020, USA ⁴³43 Latz CA, DeCarlo C, Boitano L, Png C, Patell R, Conrad MF, et al. Blood type and outcomes in patients with COVID-19. Ann. Hematol. 2020;99(9):2113-8.	Cross-sectional / 6	7648 1289 cases 6359 controls² 2 Non-blood donor controls.	COVID-19 infection	- Groups A, B and AB were more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
HOILAND et al, 2020, Canada.⁴⁴44 Hoiland RL, Fergusson NA, Mitra AR, Griesdale DE, Devine DV, Stukas S, et al. The association of ABO blood group with indices of disease severity and multiorgan dysfunction in COVID-19. Blood Adv. 2020;4(20):4981-9.	Cross-sectional / 7	62,341 95 cases^* * Study sample 1 (hospitalized). 62,246 controls² 2 Non-blood donor controls.	COVID-19 infection	- No significant difference
GÖKER et al, 2020, Turkey⁴⁵45 Göker H, Karakulak EA, Demiroglu H, Ceylan ÇMA, Büyükasik Y, Inkaya AÇ, et al. The effects of blood group types on the risk of COVID-19 infection and its clinical outcome. Turk] Med Sei. 2020;50(4):679-83.	Cross-sectional / 7	2068 186 cases^* * Study sample 1 (hospitalized). 1882 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
AKTIMUR et al, 2020, Turkey.⁵¹51 Aktimur SH, Ahmet S, Yazicioglu B, Gunes AK, Serhat G The assessment of the relationship between ABO blood groups and Covid-19 infection. Int J Hematol Oncol. 2020;31(3):121-5.	Cross-sectional / 7	5379 179 cases^* * Study sample 1 (hospitalized). 5200 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
KOMAL, 2021, Pakistan.⁵⁶56 Komal A, Noreen M, Akhtar J, Imran M, Jamal M, Atif M, et al. Analyses of ABO blood groups with susceptibility and symptomatic variations of COVID-19 infection, a questionnaire-based survey. APMIS. 2021;129(10):579-86.	Cross-sectional / 4	1599 305 cases^ Study sample 2 (outpatients). 1294 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group AB was more prevalent in COVID patients compared to controls, Group B was less prevalent in patients
ALMADHI et al, 2021, Bahrain.⁵⁰50 Almadhi MA, Abdulrahman A, Alawadhi A, Rabaan AA, Atkin S, AlQahtani M. The effect of ABO blood group and antibody class on the risk of COVID-19 infection and severity of clinical outcomes. Sei Rep. 2021;ll(1):l-5.	Cross-sectional / 7	7319 2334 cases^ Study sample 2 (outpatients). 4985 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group B was more prevalent in COVID patients compared to controls, Group AB was less prevalent in patients
ZHAO et al, 2020, China.³³33 Zhao J, Yang Y, Huang H, Li D, Gu D, Lu X, et al. Relationship between the ABO blood group and the coronavirus disease 2019 (COVID-19) susceptibility. Clin Infect Dis. 2021;73(2): 328-31.	Cross sectional / 8	29.253 2173 cases 27,080 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
WU et al, 2020, China.³⁵35 Wu Y, Feng Z, Li P, Yu Q. Relationship between ABO blood group distribution and clinical characteristics in patients with COVID-19. Clin Chim Acta. 2020;509:220-3.	Case control / 6	2178 187 cases^* * Study sample 1 (hospitalized). 1991 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
SAIFY et al, 2020, Afghanistan.³⁴34 Saify K, Alborz MS, Saadat M. Susceptibility to the novel coronavirus disease (COVID-19) is associated with ABO and Rh blood groups: a case-control study from Afghanistan. Egypt J Med Hum Genet. 2021;22(1):l-5.	Case control / 7	1340 301 cases^* * Study sample 1 (hospitalized). 1039 controls¹ 1 Blood donor controls.	COVID-19 infection	- No significant difference
AD'HIAH et al, 2020, Iraq. (32)	Case control / 9	1915 1014 cases^* * Study sample 1 (hospitalized). 901 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls.
KÍRiSCietal, 2021, Turkey⁴⁰40 KÍRÍSCi Ö, ÖZLÜK S, TOPALCA US, KÖPRÜLÜ ND. Relationship of ABO blood groups to SARS-COV-2 infection causing COVID-19 disease. Konuralp Med J. 2021;13(1):18-23.	Case control / 6	8299 455 cases^ Study sample 2 (outpatients). 7844 controls² 2 Non-blood donor controls.	COVID-19 infection	- No significant difference
FAN et al, 2020, China.³¹31 Fan Q, Zhang W, Li B, Li D-J, Zhang J, Zhao F. Association between ABO blood group system and COVID-19 susceptibility in Wuhan. Front Cell Infect Microbiol. 2020;10:404.	Case control / 9	208 105 cases^* * Study sample 1 (hospitalized). 103 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
KHALIL et al, 2020, Lebanon.³⁶36 Khalil A, Feghali R, Hassoun M. The Lebanese COVID-19 cohort; a challenge for the ABO blood group system. Front Med. 2020;7:585341.	Case control / 6	6643 146 cases^* * Study sample 1 (hospitalized). 6497 controls² 2 Non-blood donor controls.	COVID-19 infection	- No significant difference
RAY et al, 2020, Canada.¹⁴14 RayJG, Colacci M, Schuil MJ, Vermeulen MJ, Park AL. Non-ABO red cell antibodies and risk of COVID-19. Int J Infect Dis. 2021;108:179-82.	Cohort / 9	225,556 7071 cases^* * Study sample 1 (hospitalized). 218,485 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group AB was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients.
BARNKOB et al., 2020, Denmark.¹⁶16 Barnkob MB, Pottegárd A, St0vring H, Haunstrup TM, Homburg K, Larsen R, et al. Reduced prevalence of SARS-CoV-2 infection in ABO blood group O. Blood Adv. 2020;4(20):4990-3.	Cohort / 7	2211,894 7422 cases^ Study sample 2 (outpatients). 2204,472 controls² 2 Non-blood donor controls.	COVID-19 infection	- Groups A, B and AB were more prevalent in COVID patients compared to controls, Group O was less prevalent in patients
MUNIZ-DIAZ et al., 2020, Spain.⁵5 Muniz-Diaz E, Llopis J, Parra R, Roig I, Ferrer G, Grifols J, et al. Relationship between the ABO blood group and COVID-19 susceptibility, severity and mortality in two cohorts of patients. Blood Transfusion. 2021;19(1):54.	Cohort / 9	76.724 854 cases^ Study sample 2 (outpatients). 75,870 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients.
NALBANT et al., 2022, Turkey.¹⁹19 Nalbant A, Aydm A, Yaylac« S, Kaya T, Wermeulen CL, Cin-emre H. Association of ABO blood group and age with COVID-19 positive test. Revista da Associação Médica Brasileira. 2021;67:46-50.	Cohort / 9	313 220 cases^* * Study sample 1 (hospitalized). 93 controls² 2 Non-blood donor controls.	COVID-19 infection	- No significant difference
AMOROSO et al., 2021, Italy.²⁰20 Amoroso A, Magistroni P, Vespasiano F, Bella A, Bellino S, Puoti F, et al. of Italian network. Regional transplant coordinating C. HLA and ABO Polymorphisms May Influence SARS-CoV-2 Infection and COVID-19 Severity. Transplantation. 2020.	Cohort / 8	40,904 219 cases^ Study sample 2 (outpatients). 40,685 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls
MUNOZ-CULLA et al, 2021, Basque.⁵³53 Muhoz-Culla M, Roncancio-Clavijo A, Martinez B, Gorostidi-Aicua M, Pineiro L, Azkune A, et al. O group is a protective factor for COVID19 in Basque population. PLoS One. 2021;16(4): e0249494.	Cohort / 7	18,208 412 cases^* * Study sample 1 (hospitalized). 17,796 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients.
DE FREITAS DUTRA et al, 2021, Brazil.²³23 de Freitas Dutra V, Bonet-Bub C, Yokoyama APH, Achkar R, Machado RRG, Assunção M, et ai. Anti-A and SARS-CoV-2: an intriguing association. Vox Sang. 2021;116(5):557-63.	Cohort / 5	2642 430 cases^* * Study sample 1 (hospitalized). 2212 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients.
KOLIN et al, 2020, United Kingdom.⁴¹41 Ko lin DA, Kulm S, Christos PJ, Elemento O. Clinical, regional, and genetic characteristics of Covid-19 patients from UK Bio-bank. PLoS One. 2020;15(11):e0241264.	Cohort / 8	397.064 968 cases^ Study sample 2 (outpatients). 396,096 controls² 2 Non-blood donor controls.	COVID-19 infection	- Group A was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients.
MATZHOLD, et al, 2021, Austria.²⁷27 Matzhold EM, Berghold A, Bemelmans MKB, Banfi C, Stelzl E, Kessler HH, et al. Lewis and ABO histo-blood types and the secretor status of patients hospitalized with COVID-19 implicate a role for ABO antibodies in susceptibility to infection with SARS-CoV-2. Transfusion. 2021;61(9):2736-45.	Cohort / 6	250,636 338 cases^* * Study sample 1 (hospitalized). 250,298 controls¹ 1 Blood donor controls.	COVID-19 infection	- Group AB was more prevalent in COVID patients compared to controls, Group O was less prevalent in patients.
TEVATIA et al, 2020, India.¹⁷17 TEVATIA MS, SIDHU A, KALRA DK, BARANWAL AK, PANDIT P, GULERIA P, et al. Does PCR cycle threshold for SARS-CoV-2 have association with ABO blood group types? J Clin Diagnost Res. 2020;14(10).	Cohort / 7	998 116 cases^* * Study sample 1 (hospitalized). 882 controls¹ 1 Blood donor controls.	COVID-19 infection	- No significant difference
DOMÈNECH-MONTOLIU et al, 2021, Spain.²⁴24 Domènech-Montoliu S, Puig-Barberà J, Pac-Sa MR, Vidal-Utril-las P, Latorre-Poveda M, Rio-González AD, et al. ABO blood groups and the incidence of complications in COVID-19 patients: a population-based prospective cohort study. Int J Environ Res Public Health. 2021;18(19):10039.	Cohort / 6	1821 483 cases^* * Study sample 1 (hospitalized). 1338 controls² 2 Non-blood donor controls.	COVID-19 infection	- No significant difference

Authors, year, place of study	Type of study / Newcastle score	Sample size (n)	Outcomes of interest	Main results
LATZ et al., 2020, USA ⁴³43 Latz CA, DeCarlo C, Boitano L, Png C, Patell R, Conrad MF, et al. Blood type and outcomes in patients with COVID-19. Ann. Hematol. 2020;99(9):2113-8.	Cross-sectional / 6	1289	Mortality	- No significant difference
LIU et al., 2020, Germany.⁶6 Liu N, Zhang T, Ma L, Zhang H, Wang H, Wei W, et al. The impact of ABO blood group on COVID-19 infection risk and mortality: a systematic review and meta-analysis. Blood Rev. 2021;48:100785.	Cross-sectional / 5	5391,149	Mortality	- Increased mortality in blood group A, decreased mortality in blood group B
BADEDI, 2020, Saudi Arabia.³⁷37 Badedi M, Makrami A, Alnami A. Co-morbidity and blood group type risk in coronavirus disease 2019 patients: a case -control study. J Infect Public Health. 2021;14(4):550-1.	Case control / 8	323 -108 cases - 215 control	Mortality	- No significant difference
AD'HIAH et al., 2020, Iraq.³²32 Ad'hiah AH, Abdullah MH, Alsudani MY, Shnawa RM, Al-Sa'ady AJ, Allami RH, et al. Association between ABO blood groups and susceptibility to COVID-19: profile of age and gender in Iraqi patients. Egypt J Med Hum Genet. 2020;21 (1):1-10.	Case control / 9	895 - 300 cases - 595 controls	Mortality	- Increased mortality in blood groups A and AB
BEHBOUDI et al., 2021, Iran.³⁸38 Behboudi E, Hamidi V, Gholizadeh F, Grala EM, Ghelmani Y, Nakhaie M, et al. Association between ABO blood groups and rhesus antigen and susceptibility to COVID-19 in the Yazd hospital. New Microbes New Infect. 2021;44:100934.	Case control / 5	398 - 148 cases - 250 controls	Mortality	- No significant difference
GAMBOA-AGUILAR et al., 2022, Mexico⁴²42 Gamboa-Aguilar J, Zamorano-Montano AC, Enriquez-Osorio A, Torres-Cubillas W, López-Arroyo JL, Chapol JAM, et al. Abo blood group, atherothrombotic comorbidities, and COVID-19: a case-control study of their association in the Mexican population. Arch. Med. Res. 2022;53(1):100-8.	Case control / 8	7416 - 2416 cases - 5000 controls	Mortality	- No significant difference
SARDU et al., 2020, Italy.¹³13 Sardu C, Marfella R, Maggi P, Messina V, Cirillo P, Codella V, et al. Implications of ABO blood group in hypertensive patients with covid-19. BMC Cardiovasc Disord. 2020;20(1):1-10.	Cohort / 7	164 cases - 72 type O - 92 non-O	Mortality	- Increased mortality in non-O blood types
BARNKOB et al., 2020, Denmark.¹⁶16 Barnkob MB, Pottegárd A, St0vring H, Haunstrup TM, Homburg K, Larsen R, et al. Reduced prevalence of SARS-CoV-2 infection in ABO blood group O. Blood Adv. 2020;4(20):4990-3.	Cohort / 7	2211,894 - 7422 cases - 2204,472 controls	Mortality	- No significant difference
RAY et al., 2020, Canada.¹⁴14 RayJG, Colacci M, Schuil MJ, Vermeulen MJ, Park AL. Non-ABO red cell antibodies and risk of COVID-19. Int J Infect Dis. 2021;108:179-82.	Cohort/9	225,556 - 7071 cases - 218,485 controls	Mortality	- Increased mortality in blood group B, decreased in blood group O
NAUFFAL et al., 2021, USA.¹⁸18 Nauffal V, Achanta A, Goldhaber SZ, Piazza G Association of ABO blood group type with cardiovascular events in COVID-19. J. Thromb. Thrombolysis. 2021;51(3):584-6.	Cohort/9	810 - 401 cases - 409 controls	Mortality	- No significant difference
SZYMANSKI et al., 2021, USA.²¹21 Szymanski J, Mohrmann L, Carter J, Nelson R, Chekuri S, Assa A, et al. ABO blood type association with SARS-CoV-2 infection mortality: a single-center population in New York City. Transfusion. 2021;61(4):1064-70.	Cohort/7	4968	Mortality	- Increased mortality in blood group A
NALBANT et al., 2022, Turkey.¹⁹19 Nalbant A, Aydm A, Yaylac« S, Kaya T, Wermeulen CL, Cin-emre H. Association of ABO blood group and age with COVID-19 positive test. Revista da Associação Médica Brasileira. 2021;67:46-50.	Cohort/9	313 - 220 cases - 93 controls	Mortality	- No significant difference
AMOROSO et al., 2021, Italy.²⁰20 Amoroso A, Magistroni P, Vespasiano F, Bella A, Bellino S, Puoti F, et al. of Italian network. Regional transplant coordinating C. HLA and ABO Polymorphisms May Influence SARS-CoV-2 Infection and COVID-19 Severity. Transplantation. 2020.	Cohort/8	40,904 - 219 cases - 40,685 controls	Mortality	- No significant difference
MATZHOLD, et al., 2021, Austria.²⁷27 Matzhold EM, Berghold A, Bemelmans MKB, Banfi C, Stelzl E, Kessler HH, et al. Lewis and ABO histo-blood types and the secretor status of patients hospitalized with COVID-19 implicate a role for ABO antibodies in susceptibility to infection with SARS-CoV-2. Transfusion. 2021;61(9):2736-45.	Cohort/6	338	Mortality	- No significant difference
HERMEL et al., 2021, USA.⁵⁸58 Hermel DJ, Spierling Bagsic SR, Costantini CL, Mason JR, Gahvari ZJ, Saven A. ABO phenotype and clinical correlates of COVID-19 severity in hospitalized patients. Future Sei OA. 2021;7(8):FSO735.	Cross-sectional / 7	473	ICU admission and mortality	- No significant difference
AKTIMUR et al., 2020, Turkey.⁵¹51 Aktimur SH, Ahmet S, Yazicioglu B, Gunes AK, Serhat G The assessment of the relationship between ABO blood groups and Covid-19 infection. Int J Hematol Oncol. 2020;31(3):121-5.	Cross-sectional / 7	5379 -179 cases - 5200 controls	ICU admission and mortality	- No significant difference
YAYLACI et al., 2020, Turkey⁴⁷47 Yaylacî S, Dheir H, íssever K, Gene AB, Senocak D, Kocayigit H, et al. The effect of abo and rh blood group antigens on admission to intensive care unit and mortality in patients with COVID-19 infection. Revista da Associação Médica Brasileira. 2020;66:86-90.	Cross-sectional / 5	397	ICU admission and mortality	- No significant difference
PASANGHA et al., 2020, India.⁵⁵55 Pasangha E, Dhali A, D'Souza C, Umesh S. Are blood groups related to the distribution and severity of COVID-19? A cross-sectional study in a tertiary care hospital in South India. Qatar Med J.2021;2021(3):63.	Cross-sectional / 5	370	ICU admission, mechanical ventilation and mortality	- No significant difference
MULLINS, et al., 2021, USA.²⁸28 Mullins J, Al-Tarbsheh AH, Chieng H, Chaukiyal P, Ghalib S, Jain E, et al. The association of ABO blood type with the risk and severity of COVID-19 infection. Am J Blood Res. 2021;11 (1):53.	Cohort/ 5	227	ICU admission and mechanical ventilation	- No significant difference
GRECO et al., 2021, Italy.²⁹29 Greco S, Bella A, Bonsi B, Fabbri N, Califano A, Morrone S, et al. SARS-CoV-2 infection and H1N1 vaccination: does a relationship between the two factors really exist? A retrospective analysis of a territorial cohort in Ferrara, Italy. Eur Rev Med Pharmacol Sei. 2021: 2795-801.	Cohort/8	330	ICU admission and mortality	- Increased ICU admission in blood group AB
KABRAH et al., 2021, Saudi Arabia.⁵⁹59 Kabrah SM, Abuzerr SS, Baghdadi MA, Kabrah AM, Flemban AF, Bahwerth FS, et al. Susceptibility of ABO blood group to COVID-19 infections: clinico-hematological, radiological, and complications analysis. Medicine. 2021;100(52).	Cohort/7	285	ICU admission and mortality	- No significant difference
HOILAND et al., 2020, Canada.⁴⁴44 Hoiland RL, Fergusson NA, Mitra AR, Griesdale DE, Devine DV, Stukas S, et al. The association of ABO blood group with indices of disease severity and multiorgan dysfunction in COVID-19. Blood Adv. 2020;4(20):4981-9.	Cross-sectional / 7	95	Mechanical ventilation	- Increased need for mechanical ventilation in blood groups A and AB
HALIM et al., 2021, Blangadesh.⁵⁷57 Halim MR, Saha S, Haque IU, Jesmin S, Nishat RJ, Islam AA, et al. ABO blood group and outcomes in patients with COVID-19 admitted in the intensive care unit (ICU): a retrospective study in a tertiary-level hospital in Bangladesh. J Multidiscip Healthc. 2021;14:2429.	Cross-sectional / 6	771	Mechanical ventilation and mortality	- Increased mortality and need for mechanical ventilation in blood group A
GÖKERetal., 2020, Turkey⁴⁵45 Göker H, Karakulak EA, Demiroglu H, Ceylan ÇMA, Büyükasik Y, Inkaya AÇ, et al. The effects of blood group types on the risk of COVID-19 infection and its clinical outcome. Turk] Med Sei. 2020;50(4):679-83.	Cross-sectional / 7	2068 -186 cases -1882 controls	Mechanical ventilation, ICU admission and mortality	- No significant difference
TORRES-ALARCÓN et al., 2021, Mexico.³⁹39 Torres-Alarcón CG, García-Ruíz A, Cahete-Ibáhez CR, Morales-Pogoda II, Muhoz-Arce CM, BE Cid-Domínguez, et al. Blood system ABO antigens as risk factor for severity of SARS-CoV-2 infection. Gaceta médica de México. 2021;157(2):181-7.	Case control / 5	125 - 73 cases - 52 controls	Mechanical ventilation, ICU admission and mortality	- Increased mortality in blood group A
AL-YOUHA et al., 2020, Kuwait.³⁰30 Al-Youha SA, Alduaij W, Al-Serri A, Almazeedi SM, Al-Haddad M, Jamal MH, et al. The impact of ABO blood groups on clinical outcomes and susceptibility to COVID-19: a retrospective study in an unselected population. Transfusion. 2021 ;61 (5):1631-41.	Cohort / 7	3703,305 - 3305 cases - 3700,000 controls	Mechanical ventilation	- No significant difference
BADEDI, 2020, Saudi Arabia.²²22 Badedi M, Alnami A, Darraj H, Alrajhi A, Mutawwam D-A, Somaily M, et al. Clinical characteristics and ABO blood groups in COVID-19 patients, Saudi Arabia. Medicine. 2021;100(30).	Cohort / 7	404	Mechanical ventilation	- No significant difference
TAMAYO-VELASCO et al., 2021, Spain.²⁵25 Tamayo-Velasco A, Penarrubia Ponce MJ, Alvarez FJ, Gonzalo-Benito H, de la Fuente I, Perez-Gonzalez S, et al. Can the cytokine profile according to ABO blood groups be related to worse outcome in COVID-19 patients? yes, they can. Front Immunol. 2021: 4088.	Cohort / 6	136 -108 cases - 28 controls	Mechanical ventilation and mortality	- Increased mortality and need for mechanical ventilation in blood groups A, B and AB
ZIETZ et al., 2020, USA.¹⁵15 Zietz M, Zucker J, Tatonetti NP. Associations between blood type and COVID-19 infection, intubation, and death. Nat Commun. 2020;11(1):l-6.	Cohort / 8	14,112	Mechanical ventilation and mortality	- Increased mortality and need for mechanical ventilation in blood group AB
ISHAQetal., 2021, Pakistan.²⁶26 Ishaq U, Malik A, Malik J, Mehmood A, Qureshi A, Laique T, et al. Association of ABO blood group with COVID-19 severity, acute phase reactants and mortality. PLoS One. 2021;16(12): e0261432.	Cohort / 6	1067	Mechanical ventilation and mortality	- No significant difference

[1] *Corresponding author at: 1290, Rodolfo Teófilo, Fortaleza, CE, CEP: 60430-372, Brazi. E-mail address: paulo_r_med@yahoo.com.br (P.R. Nóbrega).

Brasil

Brasil

Correlation between ABO blood type, susceptibility to SARS-CoV-2 infection and COVID-19 disease severity: A systematic review

ABSTRACT

Objectives:

Methods:

Results:

Conclusion: