Artemisinin derivative-containing therapies and abnormal hemoglobin: Do we need to adapt the treatment?

Eric A. Gbessi; Offianan A. Toure; Albert Gnondjui; Tossea S. Koui; Baba Coulibaly; Berenger A. Ako; Nguessan L. Tiacoh; Serge-Brice Assi; Ibrahima Sanogo; Didier-Paulin Sokouri; Ronan Jambou

doi:10.1051/parasite/2021063

All issues

Volume 28 (2021)

Parasite, 28 (2021) 67

References

Open Access

Research Article

Issue		Parasite Volume 28, 2021


Article Number		67
Number of page(s)		9
DOI		https://doi.org/10.1051/parasite/2021063
Published online		27 September 2021

Adjei GO, Goka BQ, Enweronu-Laryea CC, Rodrigues OP, Renner L, Sulley AM, Alifrangis M, Khalil I, Kurtzhals JA. 2014. A randomized trial of artesunate-amodiaquine versus artemether-lumefantrine in Ghanaian paediatric sickle cell and non-sickle cell disease patients with acute uncomplicated malaria. Malaria Journal, 13, 369. [PubMed] [Google Scholar]
Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Koné A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D. 2000. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood, 96, 2358–2363. [PubMed] [Google Scholar]
Allison AC. 1954. The distribution of the sickle-cell trait in East Africa and elsewhere, and its apparent relationship to the incidence of subtertian malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 48, 312–318. [PubMed] [Google Scholar]
Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois A-C, Khim N, Kim S, Duru V, Bouchier C, Ma L, Lim P, Leang R, Duong S, Sreng S, Suon S, Chuor CM, Bout DM, Ménard S, Rogers WO, Genton B, Fandeur T, Miotto O, Ringwald P, Le Bras J, Berry A, Barale J-C, Fairhurst RM, Benoit-Vical F, Mercereau-Puijalon O, Ménard D. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature, 505, 50–55. [PubMed] [Google Scholar]
Cui L, Su X. 2009. Discovery, mechanisms of action and combination therapy of artemisinin. Expert Review of Anti-Infective Therapy, 7, 999–1013. [PubMed] [Google Scholar]
Davis TME, Karunajeewa HA, Ilett KF. 2005. Artemisinin-based combination therapies for uncomplicated malaria. Medical Journal of Australia, 182, 181–185. [Google Scholar]
Fairhurst RM, Fujioka H, Hayton K, Collins KF, Wellems TE. 2003. Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state. Blood, 101, 3309–3315. [PubMed] [Google Scholar]
Flegg JA, Guerin PJ, White NJ, Stepniewska K. 2011. Standardizing the measurement of parasite clearance in falciparum malaria: the parasite clearance estimator. Malaria Journal, 10, 339. [PubMed] [Google Scholar]
Friedman MJ. 1979. Oxidant damage mediates variant red cell resistance to malaria. Nature, 280, 245–247. [PubMed] [Google Scholar]
Gonçalves BP, Sagara I, Coulibaly M, Wu Y, Assadou MH, Guindo A, Ellis RD, Diakite M, Gabriel E, Prevots DR, Doumbo OK, Duffy PE. 2017. Hemoglobin variants shape the distribution of malaria parasites in human populations and their transmission potential. Scientific Reports, 7, 14267. [PubMed] [Google Scholar]
Haldane JBS. 1949. The rate of mutations of human genes, in Malaria: Genetic and Evolutionary Aspects. Kluwer Academic Publishers: Boston. p. 169–174. [Google Scholar]
Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, Mumba D, Kekre M, Yavo W, Mead D, Bouyou-Akotet M, Apinjoh T, Golassa L, Randrianarivelojosia M, Andagalu B, Maiga-Ascofare O, Amambua-Ngwa A, Tindana P, Ghansah A, MacInnis B, Kwiatkowski D, Djimde AA. 2015. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. Journal of Infectious Diseases, 211, 1352–1355. [Google Scholar]
LaMonte G, Philip N, Reardon J, Lacsina JR, Majoros W, Chapman L, Thornburg CD, Telen MJ, Ohler U, Nicchitta CV, Haystead T, Chi J-T. 2012. Translocation of sickle cell erythrocyte MicroRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host & Microbe, 12, 187–199. [PubMed] [Google Scholar]
Modiano D, Luoni G, Sirima BS, Simporé J, Verra F, Konaté A, Rastrelli E, Olivieri A, Calissano C, Paganotti GM, D’Urbano L, Sanou I, Sawadogo A, Modiano G, Coluzzi M. 2001. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature, 414, 305–308. [PubMed] [Google Scholar]
Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM. 2008. Evidence of artemisinin-resistant malaria in Western Cambodia. New England Journal of Medicine, 359, 2619–2620. [Google Scholar]
Orjih AU. 1987. Increased accumulation of chloroquine and desethylchloroquine in homozygous sickle cells. Bulletin of the World Health Organization, 65, 51–55. [PubMed] [Google Scholar]
Prasartkaew S, Bunyaratvej A, Fucharoen S, Wasi P. 1986. Comparison of erythrocyte antioxidative enzyme activities between two types of haemoglobin H disease. Journal of Clinical Pathology, 39, 1299–1303. [PubMed] [Google Scholar]
Sugiarto SR, Moore BR, Makani J, Davis TME. 2018. Artemisinin therapy for malaria in hemoglobinopathies: A systematic review. Clinical Infectious Diseases, 66, 799–804. [Google Scholar]
Sun A, Dong Y, Chen M, Xu Y, Deng Y, Mao X, Wang J. 2016. Polymorphism analysis of Plasmodium falciparum K13 gene kelch domain associated with resistance to artemisinin in Yunnan Province. Chinese Journal of Parasitology & Parasitic Diseases, 34, 339–345. [Google Scholar]
Tossea SK, Adji EG, Coulibaly B, Ako BA, Coulibaly DN, Joly P, Assi S-B, Toure A, Jambou R. 2018. Cross sectional study on prevalence of sickle cell alleles S and C among patients with mild malaria in Ivory Coast. BMC Research Notes, 11, 215. [PubMed] [Google Scholar]
Toure OA, Assi SB, N’Guessan TL, Adji GE, Ako AB, Brou MJ, Ehouman MF, Gnamien LA, Coulibaly MA, Coulibaly B, Beourou S, Bassinka I, Soumahoro A, Kadjo F, Tano MA. 2014. Open-label, randomized, non-inferiority clinical trial of artesunate-amodiaquine versus artemether-lumefantrine fixed-dose combinations in children and adults with uncomplicated falciparum malaria in Côte d’Ivoire. Malaria Journal, 13, 439. [PubMed] [Google Scholar]
Toure OA, Landry NT, Valerie IBA, Brice AS, Emmanuel K, Adonis K, Stephane YS, Eric A, Viviane K-L, Gbessi AE, Sylvain B, Karil T, Berenger AAA, Albert G, Joseph D, Ronan J. 2018. Current efficacy of the first line uncomplicated malaria treatment in two sentinels sites of Côte d’Ivoire. International Journal of Clinical Research & Trials, 3, 124. [Google Scholar]
Trager W, Nagel RL, Roth EF, Friedman MJ. 1979. The role of hemoglobins C, S, and Nbalt in the inhibition of malaria parasite development in vitro. American Journal of Tropical Medicine and Hygiene, 28, 777–780. [Google Scholar]
Trent RJA. 2006. Diagnosis of the haemoglobinopathies. Clinical Biochemist Reviews, 27, 27–38. [Google Scholar]
Tun STT, Lubell Y, Dondorp AM, Fieldman T, Tun KM, Celhay O, Chan XH, Saralamba S, White LJ. 2017. Identifying artemisinin resistance from parasite clearance half-life data with a simple Shiny web application. PLoS One, 12, e0177840 [PubMed] [Google Scholar]
Vattanaviboon P, Wilairat P, Yuthavong Y. 1998. Binding of dihydroartemisinin to hemoglobin H: Role in drug accumulation and host-induced antimalarial ineffectiveness of α-thalassemic erythrocytes. Molecular Pharmacology, 53, 492–496. [PubMed] [Google Scholar]
White LJ, Flegg JA, Phyo AP, Wiladpai-ngern JH, Bethell D, Plowe C, Anderson T, Nkhoma S, Nair S, Tripura R, Stepniewska K, Pan-Ngum W, Silamut K, Cooper BS, Lubell Y, Ashley EA, Nguon C, Nosten F, White NJ, Dondorp AM. 2015. Defining the in vivo phenotype of artemisinin-resistant falciparum malaria: A modelling approach. PLoS Medicine, 12, e1001823. [PubMed] [Google Scholar]
WHO. 2006. Rapport du sécrétariat géneral de l’OMS sur les thalassémies et autres hémoglobinopaties. https://apps.who.int/gb/ebwha/pdf_files/EB118/B118_5-fr.pdf. [Google Scholar]
WHO. 2008. Global malaria control and elimination: report of a meeting on containment of artemisinin tolerance. Geneva: World Health Organization. [Google Scholar]
WHO. 2009. Methods for surveillance of antimalarial drug efficacy. Geneva: World Health Organization. [Google Scholar]
Willcox M, Björkman A, Brohult J. 1983. Falciparum malaria and β-thalassaemia trait in northern Liberia. Annals of Tropical Medicine & Parasitology, 77, 335–347. [Google Scholar]
Yuthavong Y, Butthep P, Bunyaratvej A, Fucharoen S. 1989. Decreased sensitivity of artesunate and chloroquine of Plasmodium falciparum infecting hemoglobin H and/or hemoglobin constant spring erythrocytes. Journal of Clinical Investigation, 83, 502–505. [Google Scholar]

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[1] Adjei GO, Goka BQ, Enweronu-Laryea CC, Rodrigues OP, Renner L, Sulley AM, Alifrangis M, Khalil I, Kurtzhals JA. 2014. A randomized trial of artesunate-amodiaquine versus artemether-lumefantrine in Ghanaian paediatric sickle cell and non-sickle cell disease patients with acute uncomplicated malaria. Malaria Journal, 13, 369. [PubMed] [Google Scholar]

[2] Agarwal A, Guindo A, Cissoko Y, Taylor JG, Coulibaly D, Koné A, Kayentao K, Djimde A, Plowe CV, Doumbo O, Wellems TE, Diallo D. 2000. Hemoglobin C associated with protection from severe malaria in the Dogon of Mali, a West African population with a low prevalence of hemoglobin S. Blood, 96, 2358–2363. [PubMed] [Google Scholar]

[3] Allison AC. 1954. The distribution of the sickle-cell trait in East Africa and elsewhere, and its apparent relationship to the incidence of subtertian malaria. Transactions of the Royal Society of Tropical Medicine and Hygiene, 48, 312–318. [PubMed] [Google Scholar]

[4] Ariey F, Witkowski B, Amaratunga C, Beghain J, Langlois A-C, Khim N, Kim S, Duru V, Bouchier C, Ma L, Lim P, Leang R, Duong S, Sreng S, Suon S, Chuor CM, Bout DM, Ménard S, Rogers WO, Genton B, Fandeur T, Miotto O, Ringwald P, Le Bras J, Berry A, Barale J-C, Fairhurst RM, Benoit-Vical F, Mercereau-Puijalon O, Ménard D. 2014. A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature, 505, 50–55. [PubMed] [Google Scholar]

[5] Cui L, Su X. 2009. Discovery, mechanisms of action and combination therapy of artemisinin. Expert Review of Anti-Infective Therapy, 7, 999–1013. [PubMed] [Google Scholar]

[6] Davis TME, Karunajeewa HA, Ilett KF. 2005. Artemisinin-based combination therapies for uncomplicated malaria. Medical Journal of Australia, 182, 181–185. [Google Scholar]

[7] Fairhurst RM, Fujioka H, Hayton K, Collins KF, Wellems TE. 2003. Aberrant development of Plasmodium falciparum in hemoglobin CC red cells: implications for the malaria protective effect of the homozygous state. Blood, 101, 3309–3315. [PubMed] [Google Scholar]

[8] Flegg JA, Guerin PJ, White NJ, Stepniewska K. 2011. Standardizing the measurement of parasite clearance in falciparum malaria: the parasite clearance estimator. Malaria Journal, 10, 339. [PubMed] [Google Scholar]

[9] Friedman MJ. 1979. Oxidant damage mediates variant red cell resistance to malaria. Nature, 280, 245–247. [PubMed] [Google Scholar]

[10] Gonçalves BP, Sagara I, Coulibaly M, Wu Y, Assadou MH, Guindo A, Ellis RD, Diakite M, Gabriel E, Prevots DR, Doumbo OK, Duffy PE. 2017. Hemoglobin variants shape the distribution of malaria parasites in human populations and their transmission potential. Scientific Reports, 7, 14267. [PubMed] [Google Scholar]

[11] Haldane JBS. 1949. The rate of mutations of human genes, in Malaria: Genetic and Evolutionary Aspects. Kluwer Academic Publishers: Boston. p. 169–174. [Google Scholar]

[12] Kamau E, Campino S, Amenga-Etego L, Drury E, Ishengoma D, Johnson K, Mumba D, Kekre M, Yavo W, Mead D, Bouyou-Akotet M, Apinjoh T, Golassa L, Randrianarivelojosia M, Andagalu B, Maiga-Ascofare O, Amambua-Ngwa A, Tindana P, Ghansah A, MacInnis B, Kwiatkowski D, Djimde AA. 2015. K13-propeller polymorphisms in Plasmodium falciparum parasites from sub-Saharan Africa. Journal of Infectious Diseases, 211, 1352–1355. [Google Scholar]

[13] LaMonte G, Philip N, Reardon J, Lacsina JR, Majoros W, Chapman L, Thornburg CD, Telen MJ, Ohler U, Nicchitta CV, Haystead T, Chi J-T. 2012. Translocation of sickle cell erythrocyte MicroRNAs into Plasmodium falciparum inhibits parasite translation and contributes to malaria resistance. Cell Host & Microbe, 12, 187–199. [PubMed] [Google Scholar]

[14] Modiano D, Luoni G, Sirima BS, Simporé J, Verra F, Konaté A, Rastrelli E, Olivieri A, Calissano C, Paganotti GM, D’Urbano L, Sanou I, Sawadogo A, Modiano G, Coluzzi M. 2001. Haemoglobin C protects against clinical Plasmodium falciparum malaria. Nature, 414, 305–308. [PubMed] [Google Scholar]

[15] Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM. 2008. Evidence of artemisinin-resistant malaria in Western Cambodia. New England Journal of Medicine, 359, 2619–2620. [Google Scholar]

[16] Orjih AU. 1987. Increased accumulation of chloroquine and desethylchloroquine in homozygous sickle cells. Bulletin of the World Health Organization, 65, 51–55. [PubMed] [Google Scholar]

[17] Prasartkaew S, Bunyaratvej A, Fucharoen S, Wasi P. 1986. Comparison of erythrocyte antioxidative enzyme activities between two types of haemoglobin H disease. Journal of Clinical Pathology, 39, 1299–1303. [PubMed] [Google Scholar]

[18] Sugiarto SR, Moore BR, Makani J, Davis TME. 2018. Artemisinin therapy for malaria in hemoglobinopathies: A systematic review. Clinical Infectious Diseases, 66, 799–804. [Google Scholar]

[19] Sun A, Dong Y, Chen M, Xu Y, Deng Y, Mao X, Wang J. 2016. Polymorphism analysis of Plasmodium falciparum K13 gene kelch domain associated with resistance to artemisinin in Yunnan Province. Chinese Journal of Parasitology & Parasitic Diseases, 34, 339–345. [Google Scholar]

[20] Tossea SK, Adji EG, Coulibaly B, Ako BA, Coulibaly DN, Joly P, Assi S-B, Toure A, Jambou R. 2018. Cross sectional study on prevalence of sickle cell alleles S and C among patients with mild malaria in Ivory Coast. BMC Research Notes, 11, 215. [PubMed] [Google Scholar]

[21] Toure OA, Assi SB, N’Guessan TL, Adji GE, Ako AB, Brou MJ, Ehouman MF, Gnamien LA, Coulibaly MA, Coulibaly B, Beourou S, Bassinka I, Soumahoro A, Kadjo F, Tano MA. 2014. Open-label, randomized, non-inferiority clinical trial of artesunate-amodiaquine versus artemether-lumefantrine fixed-dose combinations in children and adults with uncomplicated falciparum malaria in Côte d’Ivoire. Malaria Journal, 13, 439. [PubMed] [Google Scholar]

[22] Toure OA, Landry NT, Valerie IBA, Brice AS, Emmanuel K, Adonis K, Stephane YS, Eric A, Viviane K-L, Gbessi AE, Sylvain B, Karil T, Berenger AAA, Albert G, Joseph D, Ronan J. 2018. Current efficacy of the first line uncomplicated malaria treatment in two sentinels sites of Côte d’Ivoire. International Journal of Clinical Research & Trials, 3, 124. [Google Scholar]

[23] Trager W, Nagel RL, Roth EF, Friedman MJ. 1979. The role of hemoglobins C, S, and Nbalt in the inhibition of malaria parasite development in vitro. American Journal of Tropical Medicine and Hygiene, 28, 777–780. [Google Scholar]

[24] Trent RJA. 2006. Diagnosis of the haemoglobinopathies. Clinical Biochemist Reviews, 27, 27–38. [Google Scholar]

[25] Tun STT, Lubell Y, Dondorp AM, Fieldman T, Tun KM, Celhay O, Chan XH, Saralamba S, White LJ. 2017. Identifying artemisinin resistance from parasite clearance half-life data with a simple Shiny web application. PLoS One, 12, e0177840 [PubMed] [Google Scholar]

[26] Vattanaviboon P, Wilairat P, Yuthavong Y. 1998. Binding of dihydroartemisinin to hemoglobin H: Role in drug accumulation and host-induced antimalarial ineffectiveness of α-thalassemic erythrocytes. Molecular Pharmacology, 53, 492–496. [PubMed] [Google Scholar]

[27] White LJ, Flegg JA, Phyo AP, Wiladpai-ngern JH, Bethell D, Plowe C, Anderson T, Nkhoma S, Nair S, Tripura R, Stepniewska K, Pan-Ngum W, Silamut K, Cooper BS, Lubell Y, Ashley EA, Nguon C, Nosten F, White NJ, Dondorp AM. 2015. Defining the in vivo phenotype of artemisinin-resistant falciparum malaria: A modelling approach. PLoS Medicine, 12, e1001823. [PubMed] [Google Scholar]

[28] WHO. 2006. Rapport du sécrétariat géneral de l’OMS sur les thalassémies et autres hémoglobinopaties. https://apps.who.int/gb/ebwha/pdf_files/EB118/B118_5-fr.pdf. [Google Scholar]

[29] WHO. 2008. Global malaria control and elimination: report of a meeting on containment of artemisinin tolerance. Geneva: World Health Organization. [Google Scholar]

[30] WHO. 2009. Methods for surveillance of antimalarial drug efficacy. Geneva: World Health Organization. [Google Scholar]

[31] Willcox M, Björkman A, Brohult J. 1983. Falciparum malaria and β-thalassaemia trait in northern Liberia. Annals of Tropical Medicine & Parasitology, 77, 335–347. [Google Scholar]

[32] Yuthavong Y, Butthep P, Bunyaratvej A, Fucharoen S. 1989. Decreased sensitivity of artesunate and chloroquine of Plasmodium falciparum infecting hemoglobin H and/or hemoglobin constant spring erythrocytes. Journal of Clinical Investigation, 83, 502–505. [Google Scholar]