Burkina Faso is a malaria-endemic country, with a high incidence of G6PD deficiency (G6PDd), which recorded its first case of COVID-19 in March 2020. G6PDd leads to a decrease in the efficiency of erythrocytes to combat oxidative stress, while SARS-CoV-2 infection induces massive production of Reactive Oxygen Species (ROS) in patients. In the present review, we discuss a possible link between G6PDd and SARS-CoV-2 infection. The mean prevalence of G6PDd in Burkina Faso is estimated at 16.6% among males and 6.5% among females. A total of 21,128 cases of COVID-19 have been recorded in Burkina Faso with 387 deaths reported (with a mortality rate of 1.15% among diagnosed cases) as of August 30, 2022. To our knowledge, no association study between G6PDd and SARS-CoV-2 infection has been conducted to date in Burkina Faso. However, several case reports around the world have described elevated risks of hemolysis and thrombosis, and other complications among G6PD-deficient patients infected with SARS-CoV-2. The use of Hydroxychloroquine (HCQ) has also been deemed unsafe by some authors for the treatment of COVID-19 among patients with G6PDd. Although HCQ has been shown to be well tolerated in COVID-19 patients in Burkina Faso, the drug could induce hemolytic crises in people with G6PD deficiency. G6PD is important in regulating ROS and maintaining erythrocyte homeostasis. In view of its high prevalence in Burkina Faso, determination of the G6PD status is required in COVID-19 patients for adequate management such as identifying a subset of COVID-19 patients for whom close monitoring and supportive care may be essential and to restrict treatment with HCQ.
References
[1]
Modiano, D., Luoni, G., Sirima, B.S., Lanfrancotti, A., Petrarca, V., Cruciani, F., Simporé, J., Ciminelli, B.M., Foglietta, E., Grisanti, P., Bianco, I., Modiano, G. and Coluzzi, M. (2001) The Lower Susceptibility to Plasmodium falciparum Malaria of Fulani of Burkina Faso (West Africa) Is Associated with Low Frequencies of Classic Malaria-Resistance Genes. Transactions of the Royal Society of Tropical Medicine and Hygiene, 95, 149-152. https://doi.org/10.1016/S0035-9203(01)90141-5
[2]
Ouattara, A.K., Bisseye, C., Bazie, B.V., Diarra, B., Compaore, T.R., Djigma, F., Pietra, V., Moret, R. and Simpore, J. (2014) Glucose-6-Phosphate Dehydrogenase (G6PD) Deficiency Is Associated with Asymptomatic Malaria in a Rural Community in Burkina Faso. Asian Pacific Journal of Tropical Biomedicine, 4, 655-658. https://doi.org/10.12980/APJTB.4.2014APJTB-2014-0100
[3]
Ouattara, A.K., Yameogo, P., Diarra, B., Obiri-Yeboah, D., Yonli, A., Compaore, T.R., Soubeiga, S.T., Djigma, F.W. and Simpore, J. (2016) Molecular Heterogeneity of Glucose-6-Phosphate Dehydrogenase Deficiency in Burkina Faso: G-6-PD Betica Selma and Santamaria in People with Symptomatic Malaria in Ouagadougou. Mediterranean Journal of Hematology and Infectious Diseases, 8, e2016029. https://doi.org/10.4084/mjhid.2016.029
[4]
Ouattara, A.K., Yameogo, P., Traore, L., Diarra, B., Assih, M., Compaore, T.R., Obiri-Yeboah, D., Soubeiga, S.T., Djigma, F.W. and Simpore, J. (2017) Prevalence, Genetic Variants and Clinical Implications of G-6-PD Deficiency in Burkina Faso: A Systematic Review. BMC Medical Genetics, 18, Article No. 139. https://doi.org/10.1186/s12881-017-0496-2
[5]
Simpore, J., Ilboudo, D., Damintoti, K., Sawadogo, L., Maria, E., Binet, S., Nitiema, H., Ouedraogo, P., Pignatelli, S. and Nikiema, J.B. (2007) Glucose-6-Phosphate Dehydrogenase Deficiency and Sickle Cell Disease in Burkina Faso. Pakistan Journal of Biological Sciences, 10, 409-414. https://doi.org/10.3923/pjbs.2007.409.414
[6]
Luzzatto, L., Ally, M. and Notaro, R. (2020) Glucose-6-Phosphate Dehydrogenase Deficiency. Blood, 136, 1225-1240. https://doi.org/10.1182/blood.2019000944
[7]
Uyoga, S., Ndila, C.M., Macharia, A.W., Nyutu, G., Shah, S., Peshu, N., Clarke, G.M., Kwiatkowski, D.P., Rockett, K.A. and Williams, T.N. (2015) Glucose-6-Phosphate Dehydrogenase Deficiency and the Risk of Malaria and Other Diseases in Children in Kenya: A Case-Control and a Cohort Study. The Lancet Haematology, 2, E437-E444. https://doi.org/10.1016/S2352-3026(15)00152-0
[8]
Ndila, C.M., Uyoga, S., Macharia, A.W., Nyutu, G., Peshu, N., Ojal, J., Shebe, M., Awuondo, K.O., Mturi, N., Tsofa, B., Sepúlveda, N., Clark, T.G., Band, G., Clarke, G., Rowlands, K., et al. (2018) Human Candidate Gene Polymorphisms and Risk of Severe Malaria in Children in Kilifi, Kenya: A Case-Control Association Study. The Lancet Haematology, 5, E333-E345. https://doi.org/10.1016/S2352-3026(18)30107-8
[9]
Clarke, G.M., Rockett, K., Kivinen, K., Hubbart, C., Jeffreys, A.E., Rowlands, K., Jallow, M., Conway, D.J., Bojang, K.A., Pinder, M., Usen, S., Sisay-Joof, F., Sirugo, G., Toure, O., Thera, M.A., et al. (2017) Characterisation of the Opposing Effects of G6PD Deficiency on Cerebral Malaria and Severe Malarial Anaemia. eLife, 6, e15085.
[10]
INSD (2022) Burkina Faso—COVID 19 Rapport de Situation. Burkina Faso Open Data. https://burkinafaso.opendataforafrica.org//jovpdge/burkina-faso-covid-19-rapport-de-situation
[11]
WHO (2022) Burkina Faso: WHO Coronavirus Disease (COVID-19) Dashboard with Vaccination Data. https://covid19.who.int/region/afro/country/bf
[12]
Tegally, H., San, J.E., Cotten, M., Moir, M., Tegomoh, B., Mboowa, G., Martin, D.P., Baxter, C., Lambisia, A.W., Diallo, A., Amoako, D.G., Diagne, M.M., Sisay, A., Zekri, A.-R.N., Gueye, A.S., et al. (2022) The Evolving SARS-CoV-2 Epidemic in Africa: Insights from Rapidly Expanding Genomic Surveillance. Science, 378, eabq5358. https://doi.org/10.1126/science.abq5358
[13]
Sagna, T., Ouedraogo, P., Traore, L., Obiri-Yeboah, D., Yonli, A., Tapsoba, A., Tovo, F., Sorgho, A., Zongo, L., Nikiema, O., Ilboudo, D., Belemgnegre, M., Nadembega, C.W., Ouermi, D., Djigma, F.W., et al. (2022) Enigma of the High Prevalence of Anti-SARS-CoV-2 Antibodies in HIV-Positive People with No Symptoms of COVID-19 in Burkina Faso. Journal of Public Health in Africa, 13, Article No. 1778. https://doi.org/10.4081/jphia.2022.1778
[14]
Sagna, T., Ouedraogo, H., Zouré, A., Zida, S., Compaore, R., Kambire, D., Soubeiga, S., Ouedraogo, O., Djigma, F., Zongo, D., Tarnagda, G., Valea, D., Dabiré, C., Nikiema, A., Camara, M., et al. (2021) Le Laboratoire à l’épreuve de la pandémie de la COVID-19 au Burkina Faso: Quels défis pour la régularité de l’offre de diagnostic. Revue Malienne d’Infectiologie et de Microbiologie, 16, 32-37. https://doi.org/10.53597/remim.v16i1.1758
[15]
Zoure, A.A., Ouedraogo, H.G., Sagna, T., Compaore, T.R., Soubeiga, S.T., Cisse, K., Kambire, D., Ouedraogo, O., Zida, S. and Dabire, C. (2022) Molecular Diagnosis of COVID-19 in Burkina Faso: Successful Challenge. International Journal of Biological and Chemical Sciences, 16, 440-463. https://doi.org/10.4314/ijbcs.v16i1.37
[16]
Jamerson, B.D., Haryadi, T.H. and Bohannon, A. (2020) Glucose-6-Phosphate Dehydrogenase Deficiency: An Actionable Risk Factor for Patients with COVID-19? Archives of Medical Research, 51, 743-744. https://doi.org/10.1016/j.arcmed.2020.06.006
[17]
Jain, S.K., Parsanathan, R., Levine, S.N., Bocchini, J.A., Holick, M.F. and Vanchiere, J.A. (2020) The Potential Link between Inherited G6PD Deficiency, Oxidative Stress, and Vitamin D Deficiency and the Racial Inequities in Mortality Associated with COVID-19. Free Radical Biology and Medicine, 161, 84-91. https://doi.org/10.1016/j.freeradbiomed.2020.10.002
[18]
MESRSI (2020) Les données préliminaires de l’étude CHLORAZ indiquent un bénéfice du traitement avec la combinaison Hydroxychloroquine + Azythromicine chez les patients de la Covid-19 au Burkina Faso. https://www.mesrsi.gov.bf/fileadmin/user_upload/storage/COMMUNIQUE_DE_PRESS_RESULTATS_PRELIMINAIRES_DE_L_ETUDE_CHLORAZ.pdf
[19]
De Franceschi, L., Costa, E., Dima, F., Morandi, M. and Olivieri, O. (2020) Glucose-6-Phosphate Dehydrogenase Deficiency Associated Hemolysis in COVID-19 Patients Treated with Hydroxychloroquine/Chloroquine: New Case Reports Coming Out. European Journal of Internal Medicine, 80, 103. https://doi.org/10.1016/j.ejim.2020.08.015
[20]
Rouamba, T., Barry, H., Ouédraogo, E., Tahita, M.C., Yaméogo, N.V., Poda, A., Diendéré, A.E., Ouedraogo, A.S., Valea, I., Koné, A.M., Thiombiano, C., Traoré, I., Tarnagda, Z., Sawadogo, S.A., Gansané, Z., et al. (2021) Safety of Chloroquine or Hydroxychloroquine Plus Azithromycin for the Treatment of COVID-19 Patients in Burkina Faso: An Observational Prospective Cohort Study. Therapeutics and Clinical Risk Management, 17, 1187-1198. https://doi.org/10.2147/TCRM.S330813
[21]
Rouamba, T., Ouédraogo, E., Barry, H., Yaméogo, N.V., Sondo, A., Boly, R., Zoungrana, J., Ouédraogo, A.R., Tahita, M.C., Poda, A., Diendéré, A.E., Ouedraogo, A.S., Valea, I., Traoré, I., Tarnagda, Z., et al. (2022) Assessment of Recovery Time, Worsening, and Death among Inpatients and Outpatients with COVID-19, Treated with Hydroxychloroquine or Chloroquine plus Azithromycin Combination in Burkina Faso. International Journal of Infectious Diseases, 118, 224-229. https://doi.org/10.1016/j.ijid.2022.02.034
[22]
Stawicki, S.P., Jeanmonod, R., Miller, A.C., Paladino, L., Gaieski, D.F., Yaffee, A.Q., De Wulf, A., Grover, J., Papadimos, T.J., Bloem, C., Galwankar, S.C., Chauhan, V., Firstenberg, M.S., Di Somma, S., Jeanmonod, D., et al. (2020) The 2019-2020 Novel Coronavirus (Severe Acute Respiratory Syndrome Coronavirus 2) Pandemic: A Joint American College of Academic International Medicine-World Academic Council of Emergency Medicine Multidisciplinary COVID-19 Working Group Consensus Paper. Journal of Global Infectious Diseases, 12, 47-93. https://doi.org/10.4103/jgid.jgid_86_20
Gautret, P., Lagier, J.C., Parola, P., Hoang, V.T., Meddeb, L., Sevestre, J., Mailhe, M., Doudier, B., Aubry, C., Amrane, S., Seng, P., Hocquart, M., Eldin, C., Finance, J., Vieira, V.E., et al. (2020) Clinical and Microbiological Effect of a Combination of Hydroxychloroquine and Azithromycin in 80 COVID-19 Patients with at Least a Six-Day Follow up: A Pilot Observational Study. Travel Medicine and Infectious Disease, 34, Article ID: 101663. https://doi.org/10.1016/j.tmaid.2020.101663
[25]
Hache, G., Rolain, J.M., Gautret, P., Deharo, J.C., Brouqui, P., Raoult, D. and Honoré, S. (2021) Combination of Hydroxychloroquine Plus Azithromycin as Potential Treatment for COVID-19 Patients: Safety Profile, Drug Interactions, and Management of Toxicity. Microbial Drug Resistance, 27, 281-290. https://doi.org/10.1089/mdr.2020.0232
[26]
Baguiya, A., Poda, A., Cissé, K., Sondo, A., Ouedraogo, B. and Ouedraogo, A. (2021) Effect of Hydroxychloroquine or Chloroquine and Azithromycin on COVID-19 Patients’ Recovery and Mortality: Evidence from a Hospital Based Retrospective Cohort Study Conducted in Burkina Faso. Journal of Infectious Diseases and Epidemiology, 7, Article No. 192. https://doi.org/10.23937/2474-3658/1510192
[27]
Cappellini, M.D. and Fiorelli, G. (2008) Glucose-6-Phosphate Dehydrogenase Deficiency. Lancet, 371, 64-74. https://doi.org/10.1016/S0140-6736(08)60073-2
[28]
Howes, R.E., Dewi, M., Piel, F.B., Monteiro, W.M., Battle, K.E., Messina, J.P., Sakuntabhai, A., Satyagraha, A.W., Williams, T.N., Baird, J.K. and Hay, S.I. (2013) Spatial Distribution of G6PD Deficiency Variants across Malaria-Endemic Regions. Malaria Journal, 12, Article No. 418. https://doi.org/10.1186/1475-2875-12-418
[29]
Luzzatto, L. and Seneca, E. (2014) G6PD Deficiency: A Classic Example of Pharmacogenetics with On-Going Clinical Implications. British Journal of Haematology, 164, 469-480. https://doi.org/10.1111/bjh.12665
[30]
Ho, L. and John, R.M. (2015) Understanding and Managing Glucose-6-Phosphate Dehydrogenase Deficiency. The Journal for Nurse Practitioners, 11, 443-450. https://doi.org/10.1016/j.nurpra.2015.01.007
[31]
Luzzatto, L., Nannelli, C. and Notaro, R. (2016) Glucose-6-Phosphate Dehydrogenase Deficiency. Hematology/Oncology Clinics of North America, 30, 373-393. https://doi.org/10.1016/j.hoc.2015.11.006
[32]
Yang, H.C., Ma, T.H., Tjong, W.Y., Stern, A. and Chiu, D.T. (2021) G6PD Deficiency, Redox Homeostasis, and Viral Infections: Implications for SARS-CoV-2 (COVID-19). Free Radical Research, 55, 364-374. https://doi.org/10.1080/10715762.2020.1866757
[33]
Da Rocha, J.E.B., Othman, H., Tiemessen, C.T., Botha, G., Ramsay, M., Masimirembwa, C., Adebamowo, C., Choudhury, A., Brandenburg, J.T., Matshaba, M., Simo, G., Gamo, F.J. and Hazelhurst, S. (2021) G6PD Distribution in Sub-Saharan Africa and Potential Risks of Using Chloroquine/Hydroxychloroquine Based Treatments for COVID-19. The Pharmacogenomics Journal, 21, 649-656. https://doi.org/10.1038/s41397-021-00242-8
[34]
Pérez-Torres, I., Soto, M.E., Guarner-Lans, V., Manzano-Pech, L. and Soria-Castro, E. (2022) The Possible Role of Glucose-6-Phosphate Dehydrogenase in the SARS-CoV-2 Infection. Cells, 11, Article No. 1982. https://doi.org/10.3390/cells11131982
[35]
Aydemir, D. and Ulusu, N.N. (2020) Is Glucose-6-Phosphate Dehydrogenase Enzyme Deficiency a Factor in Coronavirus-19 (COVID-19) Infections and Deaths? Pathogens and Global Health, 114, 109-110. https://doi.org/10.1080/20477724.2020.1751388
[36]
Youssef, J.G., Zahiruddin, F., Youssef, G., Padmanabhan, S., Ensor, J., Pingali, S.R., Zu, Y., Sahay, S. and Iyer, S.P. (2021) G6PD Deficiency and Severity of COVID19 Pneumonia and Acute Respiratory Distress Syndrome: Tip of the Iceberg? Annals of Hematology, 100, 667-673. https://doi.org/10.1007/s00277-021-04395-1
[37]
Wu, Y.-H., Tseng, C.-P., Cheng, M.-L., Ho, H.-Y., Shih, S.-R. and Chiu, D.T.-Y. (2008) Glucose-6-Phosphate Dehydrogenase Deficiency Enhances Human Coronavirus 229E Infection. The Journal of Infectious Diseases, 197, 812-816. https://doi.org/10.1086/528377
[38]
Littera, R., Campagna, M., Deidda, S., Angioni, G., Cipri, S., Melis, M., Firinu, D., Santus, S., Lai, A., Porcella, R., Lai, S., Rassu, S., Scioscia, R., Meloni, F., Schirru, D., et al. (2020) Human Leukocyte Antigen Complex and Other Immunogenetic and Clinical Factors Influence Susceptibility or Protection to SARS-CoV-2 Infection and Severity of the Disease Course. The Sardinian Experience. Frontiers in Immunology, 11, Article 605688. https://doi.org/10.3389/fimmu.2020.605688
[39]
Beauverd, Y., Adam, Y., Assouline, B. and Samii, K. (2020) COVID-19 Infection and Treatment with Hydroxychloroquine Cause Severe Haemolysis Crisis in a Patient with Glucose-6-Phosphate Dehydrogenase Deficiency. European Journal of Haematology, 105, 357-359. https://doi.org/10.1111/ejh.13432
[40]
Palmer, K., Dick, J., French, W., Floro, L. and Ford, M. (2020) Methemoglobinemia in Patient with G6PD Deficiency and SARS-CoV-2 Infection. Emerging Infectious Diseases, 26, 2279-2281. https://doi.org/10.3201/eid2609.202353
[41]
Maillart, E., Leemans, S., Van Noten, H., Vandergraesen, T., Mahadeb, B., Salaouatchi, M.T., De Bels, D. and Clevenbergh, P. (2020) A Case Report of Serious Haemolysis in a Glucose-6-Phosphate Dehydrogenase-Deficient COVID-19 Patient Receiving Hydroxychloroquine. Infectious Diseases, 52, 659-661. https://doi.org/10.1080/23744235.2020.1774644
[42]
Yu, R., Chen, C.R., Evans, D., Qing, X., Gotesman, M., Chandramohan, G., Kallay, T., Lin, H.J. and Pedigo, T.P. (2022) Glucose-6-Phosphate Dehydrogenase Deficiency Presenting with Rhabdomyolysis in a Patient with Coronavirus Disease 2019 Pneumonia: A Case Report. Journal of Medical Case Reports, 16, Article No. 106. https://doi.org/10.1186/s13256-022-03322-w
[43]
Kumar, N., AbdulRahman, A., AlAwadhi, A.I. and AlQahtani, M. (2021) Is Glucose-6-Phosphatase Dehydrogenase Deficiency Associated with Severe Outcomes in Hospitalized COVID-19 Patients? Scientific Reports, 11, Article No. 19213. https://doi.org/10.1038/s41598-021-98712-3
[44]
Lupescu, A., Bissinger, R., Goebel, T., Salker, M.S., Alzoubi, K., Liu, G., Chirigiu, L., Mack, A.F., Qadri, S.M. and Lang, F. (2015) Enhanced Suicidal Erythrocyte Death Contributing to Anemia in the Elderly. Cellular Physiology and Biochemistry, 36, 773-783. https://doi.org/10.1159/000430137
[45]
Sasi, S., Yassin, M.A., Nair, A.P. and Al Maslamani, M.S. (2020) A Case of COVID-19 in a Patient with Asymptomatic Hemoglobin D Thalassemia and Glucose-6-Phosphate Dehydrogenase Deficiency. American Journal of Case Reports, 21, e925788. https://doi.org/10.12659/AJCR.925788
[46]
Klouda, C.B. and Stone, W.L. (2020) Oxidative Stress, Proton Fluxes, and Chloroquine/Hydroxychloroquine Treatment for COVID-19. Antioxidants, 9, Article No. 894. https://doi.org/10.3390/antiox9090894
[47]
Chaney, S., Basirat, A., McDermott, R., Keenan, N. and Moloney, E. (2020) COVID-19 and Hydroxychloroquine Side-Effects: Glucose 6-Phosphate Dehydrogenase Deficiency (G6PD) and Acute Haemolytic Anaemia. QJM: An International Journal of Medicine, 113, 890-891. https://doi.org/10.1093/qjmed/hcaa267
[48]
Zhang, P., Gao, X., Ishida, H., Amnuaysirikul, J., Weina, P.J., Grogl, M., O’Neil, M.T., Li, Q., Caridha, D., Ohrt, C., Hickman, M., Magill, A.J. and Ray, P. (2013) An In vivo Drug Screening Model Using Glucose-6-Phosphate Dehydrogenase Deficient Mice to Predict the Hemolytic Toxicity of 8-Aminoquinolines. The American Journal of Tropical Medicine and Hygiene, 88, 1138-1145. https://doi.org/10.4269/ajtmh.12-0682
[49]
Mohammad, S., Clowse, M.E.B., Eudy, A.M. and Criscione-Schreiber, L.G. (2018) Examination of Hydroxychloroquine Use and Hemolytic Anemia in G6PDH-Deficient Patients. Arthritis Care & Research, 70, 481-485. https://doi.org/10.1002/acr.23296
[50]
Ramirez de Oleo, I.E., Mejia Saldarriaga, M. and Johnson, B.K. (2022) Association of Hydroxychloroquine Use and Hemolytic Anemia in Patients with Low Levels of Glucose-6-Phosphate Dehydrogenase. Journal of Clinical Rheumatology, 28, e23-e25. https://doi.org/10.1097/RHU.0000000000001571
[51]
Schilling, W.H.K., Bancone, G. and White, N.J. (2020) No Evidence That Chloroquine or Hydroxychloroquine Induce Hemolysis in G6PD Deficiency. Blood Cells, Molecules, and Diseases, 85, Article ID: 102484. https://doi.org/10.1016/j.bcmd.2020.102484
[52]
Zuchelkowski, B.E., Wang, L., Gingras, S., Xu, Q., Yang, M., Triulzi, D., Page, G.P., Gordeuk, V.R., Kim-Shapiro, D.B., Lee, J.S. and Gladwin, M.T. (2020) Brief Report: Hydroxychloroquine Does Not Induce Hemolytic Anemia or Organ Damage in a “Humanized” G6PD A-Mouse Model. PLOS ONE, 15, e0240266. https://doi.org/10.1371/journal.pone.0240266
[53]
Kongkiatkamon, S. (2022) Acute Haemolysis Following COVID-19 Vaccination in a Thalassaemic Patient with G6PD Deficiency. British Journal of Haematology, 198, 221. https://doi.org/10.1111/bjh.18204
