Addressing health equity for breastfeeding women: primaquine for Plasmodium vivax radical cure | Malaria Journal
WHO. World malaria report 2023. Geneva: World Health Organization; 2023. Accessed 8 Jan 2024.
WHO. Guidelines for malaria (version 7.1). Geneva: World Health Organization; 2023. Accessed 8 Jan 2024.
Nekkab N, Obadia T, Monteiro WM, Lacerda MVG, White M, Mueller I. Accelerating towards P. vivax elimination with a novel serological test-and-treat strategy: a modelling case study in Brazil. Lancet Reg Health Am. 2023;22: 100511.
Google Scholar
Douglas NM, Pontororing GJ, Lampah DA, Yeo TW, Kenangalem E, Poespoprodjo JR, et al. Mortality attributable to Plasmodium vivax malaria: a clinical audit from Papua, Indonesia. BMC Med. 2014;12:217.
Google Scholar
Lanca EF, Magalhaes BM, Vitor-Silva S, Siqueira AM, Benzecry SG, Alexandre MA, et al. Risk factors and characterization of Plasmodium vivax-associated admissions to pediatric intensive care units in the Brazilian Amazon. PLoS ONE. 2012;7: e35406.
Google Scholar
Poespoprodjo JR, Fobia W, Kenangalem E, Lampah DA, Hasanuddin A, Warikar N, et al. Vivax malaria: a major cause of morbidity in early infancy. Clin Infect Dis. 2009;48:1704–12.
Google Scholar
White NJ. Determinants of relapse periodicity in Plasmodium vivax malaria. Malar J. 2011;10:297.
Google Scholar
Corder RM, de Lima ACP, Khoury DS, Docken SS, Davenport MP, Ferreira MU. Quantifying and preventing Plasmodium vivax recurrences in primaquine-untreated pregnant women: an observational and modeling study in Brazil. PLoS Negl Trop Dis. 2020;14: e0008526.
Google Scholar
Commons RJ, Rajasekhar M, Edler P, Abreha T, Awab GR, Baird JK, et al. Effect of primaquine dose on the risk of recurrence in patients with uncomplicated Plasmodium vivax: a systematic review and individual patient data meta-analysis. Lancet Infect Dis. 2023;24:172–83.
Google Scholar
Soto AM, Gonzalez-Ceron L, Santillan-Valenzuela F, Parrales ME, Montoya A. Recurrent Plasmodium vivax cases of both short and long latency increased with transmission intensity and were distributed year-round in the most affected municipalities of the RACCN, Nicaragua, 2013–2018. Int J Environ Res Public Health. 2022;19:6195.
Google Scholar
Bancone G, Chu CS. G6PD variants and haemolytic sensitivity to primaquine and other drugs. Front Pharmacol. 2021;12: 638885.
Google Scholar
Rueangweerayut R, Bancone G, Harrell EJ, Beelen AP, Kongpatanakul S, Mohrle JJ, et al. Hemolytic potential of tafenoquine in female volunteers heterozygous for glucose-6-phosphate dehydrogenase (G6PD) deficiency (G6PD Mahidol variant) versus G6PD-normal volunteers. Am J Trop Med Hyg. 2017;97:702–11.
Google Scholar
Chu CS, Bancone G, Nosten F, White NJ, Luzzatto L. Primaquine-induced haemolysis in females heterozygous for G6PD deficiency. Malar J. 2018;17:101.
Google Scholar
GSK. KRINTAFEL prescribing information. Durham, GSK; 2023. Accessed 13 Mar 2024.
Sanofi-Aventis. Primaquine phosphate prescribing information. Bridgewater, Sanofi-Aventis; 2017. Accessed 13 Mar 2024.
Rajasekhar M, Simpson JA, Ley B, Edler P, Chu CS, Abreha T, et al. Primaquine dose and the risk of haemolysis in patients with uncomplicated Plasmodium vivax malaria: a systematic review and individual patient data meta-analysis. Lancet Infect Dis. 2023;24:184–95.
Google Scholar
Chu CS, Bancone G, Soe NL, Carrara VI, Gornsawun G, Nosten F. The impact of using primaquine without prior G6PD testing: a case series describing the obstacles to the medical management of haemolysis. Wellcome Open Res. 2019;4:25.
Google Scholar
Commons RJ, Simpson JA, Thriemer K, Chu CS, Douglas NM, Abreha T, et al. The haematological consequences of Plasmodium vivax malaria after chloroquine treatment with and without primaquine: a WorldWide Antimalarial Resistance Network systematic review and individual patient data meta-analysis. BMC Med. 2019;17:151.
Google Scholar
Yilma D, Groves ES, Brito-Sousa JD, Monteiro WM, Chu C, Thriemer K, et al. Severe hemolysis during primaquine radical cure of Plasmodium vivax malaria: two systematic reviews and individual patient data descriptive analyses. Am J Trop Med Hyg. 2023;109:761–9.
Google Scholar
Brito-Sousa JD, Santos TC, Avalos S, Fontecha G, Melo GC, Val F, et al. Clinical spectrum of primaquine-induced hemolysis in glucose-6-phosphate dehydrogenase deficiency: a 9-year hospitalization-based study from the Brazilian Amazon. Clin Infect Dis. 2019;69:1440–2.
Google Scholar
Pfeffer DA, Satyagraha AW, Sadhewa A, Alam MS, Bancone G, Boum Y 2nd, et al. Genetic variants of glucose-6-phosphate dehydrogenase and their associated enzyme activity: a systematic review and meta-analysis. Pathogens. 2022;11:1045.
Google Scholar
Howes RE, Piel FB, Patil AP, Nyangiri OA, Gething PW, Dewi M, et al. G6PD deficiency prevalence and estimates of affected populations in malaria endemic countries: a geostatistical model-based map. PLoS Med. 2012;9: e1001339.
Google Scholar
Gerth-Guyette E, Nguyen HT, Nowak S, Hoang NT, Mai DTT, Thi Sang V, et al. Assessing the operational feasibility of integrating point-of-care G6PD testing into Plasmodium vivax malaria management in Vietnam. Pathogens. 2023;12:689.
Google Scholar
Adhikari B, Tripura R, Dysoley L, Peto TJ, Callery JJ, Heng C, et al. Glucose-6-phosphate dehydrogenase (G6PD) measurement using biosensors by community-based village malaria workers and hospital laboratory staff in Cambodia: a quantitative study. Pathogens. 2023;12:400.
Google Scholar
Brito-Sousa JD, Peixoto HM, Devine A, Silva-Neto AV, Balieiro PCS, Sampaio VS, et al. Real-life quantitative G6PD screening in Plasmodium vivax patients in the Brazilian Amazon: a cost-effectiveness analysis. PLoS Negl Trop Dis. 2022;16: e0010325.
Google Scholar
Brito-Sousa JD, Murta F, Vitor-Silva S, Sampaio V, Mendes M, Souza B, et al. Quantitative G6PD deficiency screening in routine malaria diagnostic units in the Brazilian Amazon (SAFEPRIM): an operational mixed-methods study. Pathogens. 2022;11:1328.
Google Scholar
Brummaier T, Gilder ME, Gornsawun G, Chu CS, Bancone G, Pimanpanarak M, et al. Vivax malaria in pregnancy and lactation: a long way to health equity. Malar J. 2020;19:40.
Google Scholar
Gilder ME, Hanpithakphong W, Hoglund RM, Tarning J, Win HH, Hilda N, et al. Primaquine pharmacokinetics in lactating women and breastfed infant exposures. Clin Infect Dis. 2018;67:1000–7.
Google Scholar
Pan X, Abduljalil K, Almond LM, Pansari A, Yeo KR. Supplementing clinical lactation studies with PBPK modeling to inform drug therapy in lactating mothers: prediction of primaquine exposure as a case example. CPT Pharmacomet Syst Pharmacol. 2024;13:386–95.
Google Scholar
Watson J, Taylor WRJ, Bancone G, Chu CS, Jittamala P, White NJ. Implications of current therapeutic restrictions for primaquine and tafenoquine in the radical cure of vivax malaria. PLoS Negl Trop Dis. 2018;12: e0006440.
Google Scholar
Wattanakul T, Gilder ME, McGready R, Hanpithakpong W, Day NP, White N, et al. Population pharmacokinetic modelling of primaquine exposures in lactating women and breastfed infants. Nat Commun. 2024;14:3851.
Google Scholar
Price RN, Douglas NM. Expanding the use of primaquine for the radical cure of Plasmodium vivax. Clin Infect Dis. 2018;67:1008–9.
Google Scholar
Boel ME, Rijken MJ, Leenstra T, Phyo AP, Pimanpanarak M, Keereecharoen NL, et al. Malaria in the post-partum period; a prospective cohort study. PLoS ONE. 2013;8: e57890.
Google Scholar
Villegas L, McGready R, Htway M, Paw MK, Pimanpanarak M, Arunjerdja R, et al. Chloroquine prophylaxis against vivax malaria in pregnancy: a randomized, double-blind, placebo-controlled trial. Trop Med Int Health. 2007;12:209–18.
Google Scholar
Wolfe MS, Cordero JF. Safety of chloroquine in chemosuppression of malaria during pregnancy. Br Med J (Clin Res Ed). 1985;290:1466–7.
Google Scholar
Ogunbona FA, Onyeji CO, Bolaji OO, Torimiro SE. Excretion of chloroquine and desethylchloroquine in human milk. Br J Clin Pharmacol. 1987;23:473–6.
Google Scholar
Ahmed R, Poespoprodjo JR, Syafruddin D, Khairallah C, Pace C, Lukito T, et al. Efficacy and safety of intermittent preventive treatment and intermittent screening and treatment versus single screening and treatment with dihydroartemisinin–piperaquine for the control of malaria in pregnancy in Indonesia: a cluster-randomised, open-label, superiority trial. Lancet Infect Dis. 2019;19:973–87.
Google Scholar
World Health Organization. Breastfeeding recommendations. Geneva: WHO; 2023. Accessed 9 Jan 2024.
Akus M, Bartick M. Lactation safety recommendations and reliability compared in 10 medication resources. Ann Pharmacother. 2007;41:1352–60.
Google Scholar
Pincelli A, Neves PAR, Lourenco BH, Corder RM, Malta MB, Sampaio-Silva J, et al. The hidden burden of Plasmodium vivax malaria in pregnancy in the amazon: an observational study in Northwestern Brazil. Am J Trop Med Hyg. 2018;99:73–83.
Google Scholar
Phyo AP, Dahal P, Mayxay M, Ashley EA. Clinical impact of vivax malaria: a collection review. PLoS Med. 2022;19: e1003890.
Google Scholar
Bardaji A, Martinez-Espinosa FE, Arevalo-Herrera M, Padilla N, Kochar S, Ome-Kaius M, et al. Burden and impact of Plasmodium vivax in pregnancy: a multi-centre prospective observational study. PLoS Negl Trop Dis. 2017;11: e0005606.
Google Scholar
Boltena MT, El-Khatib Z, Sahlemichael Kebede A, Asamoah BO, Tadesse Boltena A, Yeshambaw M, et al. Comorbidity of geo-helminthes among malaria outpatients of the health facilities in Ethiopia: systematic review and meta-analysis. Int J Environ Res Public Health. 2021;18:862.
Google Scholar
Cardona-Arias JA, Carmona-Fonseca J. Congenital malaria: frequency and epidemiology in Colombia, 2009–2020. PLoS ONE. 2022;17: e0263451.
Google Scholar
Dombrowski JG, Barateiro A, Peixoto EPM, Barros A, Souza RM, Clark TG, et al. Adverse pregnancy outcomes are associated with Plasmodium vivax malaria in a prospective cohort of women from the Brazilian Amazon. PLoS Negl Trop Dis. 2021;15: e0009390.
Google Scholar
Botto-Menezes C, Silva Dos Santos MC, Lopes Simplicio J, Menezes de Medeiros J, Barroso Gomes KC, de Carvalho Costa IC, et al. Plasmodium vivax malaria in pregnant women in the Brazilian amazon and the risk factors associated with prematurity and low birth weight: a descriptive study. PLoS ONE. 2015;10: e0144399.
Google Scholar
Chandrashekhar VN, Punnath K, Dayanand KK, Kakkilaya SB, Jayadev P, Kumari SN, et al. Impact of oxidative stress in response to malarial infection during pregnancy: complications, histological changes, and pregnancy outcomes. Trop Parasitol. 2022;12:21–33.
Google Scholar
Wells TN, Burrows JN, Baird JK. Targeting the hypnozoite reservoir of Plasmodium vivax: the hidden obstacle to malaria elimination. Trends Parasitol. 2010;26:145–51.
Google Scholar
Ahmad SS, Rahi M, Sharma A. Relapses of Plasmodium vivax malaria threaten disease elimination: time to deploy tafenoquine in India? BMJ Glob Health. 2021;6: e004558.
Google Scholar
John GK, Douglas NM, von Seidlein L, Nosten F, Baird JK, White NJ, et al. Primaquine radical cure of Plasmodium vivax: a critical review of the literature. Malar J. 2012;11:280.
Google Scholar
Milligan R, Daher A, Villanueva G, Bergman H, Graves PM. Primaquine alternative dosing schedules for preventing malaria relapse in people with Plasmodium vivax. Cochrane Database Syst Rev. 2020;8:CD012656.
Google Scholar
Walker CR, Hickson RI, Chang E, Ngor P, Sovannaroth S, Simpson JA, et al. A model for malaria treatment evaluation in the presence of multiple species. Epidemics. 2023;44: 100687.
Google Scholar
Kim S, Byun JH, Park A, Jung IH. A mathematical model for assessing the effectiveness of controlling relapse in Plasmodium vivax malaria endemic in the Republic of Korea. PLoS ONE. 2020;15: e0227919.
Google Scholar
Obadia T, Nekkab N, Robinson LJ, Drakeley C, Mueller I, White MT. Developing sero-diagnostic tests to facilitate Plasmodium vivax serological test-and-treat approaches: modeling the balance between public health impact and overtreatment. BMC Med. 2022;20:98.
Google Scholar
Elmes NJ, Bennett SM, Abdalla H, Carthew TL, Edstein MD. Lack of sex effect on the pharmacokinetics of primaquine. Am J Trop Med Hyg. 2006;74:951–2.
Google Scholar
Ward SA, Mihaly GW, Edwards G, Looareesuwan S, Phillips RE, Chanthavanich P, et al. Pharmacokinetics of primaquine in man. II. Comparison of acute vs chronic dosage in Thai subjects. Br J Clin Pharmacol. 1985;19:751–5.
Google Scholar
Mihaly GW, Ward SA, Edwards G, Nicholl DD, Orme ML, Breckenridge AM. Pharmacokinetics of primaquine in man. I. Studies of the absolute bioavailability and effects of dose size. Br J Clin Pharmacol. 1985;19:745–50.
Google Scholar
Mihaly GW, Ward SA, Edwards G, Orme ML, Breckenridge AM. Pharmacokinetics of primaquine in man: identification of the carboxylic acid derivative as a major plasma metabolite. Br J Clin Pharmacol. 1984;17:441–6.
Google Scholar
Mukaka M, Onyamboko MA, Olupot-Olupot P, Peerawaranun P, Suwannasin K, Pagornrat W, et al. Pharmacokinetics of single low dose primaquine in Ugandan and Congolese children with falciparum malaria. EBioMedicine. 2023;96: 104805.
Google Scholar
Bennett P. Use of the monographs on drugs. In: Bennett P, editor. Drugs and human lactation: a comprehensive guide to the content and consequences of drugs, micronutrients, radiopharmaceuticals, and environmental and occupational chemicals in human milk. 2nd ed. Amsterdam: Elsevier; 1996. p. 67–74.
Ojara FW, Kawuma AN, Waitt C. A systematic review on maternal-to-infant transfer of drugs through breast milk during the treatment of malaria, tuberculosis, and neglected tropical diseases. PLoS Negl Trop Dis. 2023;17: e0011449.
Google Scholar
Bancone G, Chowwiwat N, Somsakchaicharoen R, Poodpanya L, Moo PK, Gornsawun G, et al. Single low dose primaquine (0.25 mg/kg) does not cause clinically significant haemolysis in G6PD deficient subjects. PLoS ONE. 2016;11: e0151898.
Google Scholar
Abduljalil K, Pansari A, Ning J, Jamei M. Prediction of drug concentrations in milk during breastfeeding, integrating predictive algorithms within a physiologically-based pharmacokinetic model. CPT Pharmacomet Syst Pharmacol. 2021;10:878–89.
Google Scholar
Allegaert K, Abbasi MY, Annaert P, Olafuyi O. Current and future physiologically based pharmacokinetic (PBPK) modeling approaches to optimize pharmacotherapy in preterm neonates. Expert Opin Drug Metab Toxicol. 2022;18:301–12.
Google Scholar
Nauwelaerts N, Macente J, Deferm N, Bonan RH, Huang MC, Van Neste M, et al. Generic workflow to predict medicine concentrations in human milk using physiologically-based pharmacokinetic (PBPK) modelling—a contribution from the ConcePTION project. Pharmaceutics. 2023;15:1469.
Google Scholar
Pressly MA, Schmidt S, Guinn D, Liu Z, Ceresa C, Samuels S, et al. Informing a comprehensive risk assessment of infant drug exposure from human milk: application of a physiologically based pharmacokinetic lactation model for sotalol. J Clin Pharmacol. 2023;63(Suppl 1):S106–16.
Google Scholar
Van Neste M, Bogaerts A, Nauwelaerts N, Macente J, Smits A, Annaert P, et al. Challenges related to acquisition of physiological data for physiologically based pharmacokinetic (PBPK) models in postpartum, lactating women and breastfed infants—a Contribution from the ConcePTION Project. Pharmaceutics. 2023;15:2618.
Google Scholar
Damoiseaux D, Amant F, Beijnen JH, Barnett S, Veal GJ, Huitema ADR, et al. Physiologically-based pharmacokinetic model to predict doxorubicin and paclitaxel exposure in infants through breast milk. CPT Pharmacomet Syst Pharmacol. 2023;12:1931–44.
Google Scholar
Yeung CHT, Autmizguine J, Dalvi P, Denoncourt A, Ito S, Katz P, et al. Maternal ezetimibe concentrations measured in breast milk and its use in breastfeeding infant exposure predictions. Clin Pharmacokinet. 2024;63:317–32.
Google Scholar
Cardoso E, Guidi M, Nauwelaerts N, Nordeng H, Teil M, Allegaert K, et al. Safety of medicines during breastfeeding—from case report to modeling: a contribution from the ConcePTION project. Expert Opin Drug Metab Toxicol. 2023;19:269–83.
Google Scholar
Guinn D, Pressly MA, Liu Z, Ceresa C, Samuels S, Wang YM, et al. Exploring the knowledge gaps in infant drug exposure from human milk: a clinical pharmacology perspective. J Clin Pharmacol. 2023;63:273–6.
Google Scholar
Pan X, Rowland YK. Physiologically based pharmacokinetic modeling to determine the impact of CYP2B6 genotype on efavirenz exposure in children, mothers and breastfeeding infants. Clin Pharmacol Ther. 2023;114:182–91.
Google Scholar
Center for Drug Evaluation and Research. Clinical lactation studies: considerations for study design. Rockville: United States Food and Drug Administration; 2019. Accessed 8 Apr 2024.
Zhang X, Yang Y, Grimstein M, Fan J, Grillo JA, Huang SM, et al. Application of PBPK modeling and simulation for regulatory decision making and its impact on US prescribing information: an update on the 2018–2019 submissions to the US FDA’s Office of Clinical Pharmacology. J Clin Pharmacol. 2020;60(Suppl 1):S160–78.
Google Scholar
Johnson TN, Small BG, Rowland YK. Increasing application of pediatric physiologically based pharmacokinetic models across academic and industry organizations. CPT Pharmacomet Syst Pharmacol. 2022;11:373–83.
Google Scholar
Lin W, Chen Y, Unadkat JD, Zhang X, Wu D, Heimbach T. Applications, challenges, and outlook for PBPK modeling and simulation: a regulatory, industrial and academic perspective. Pharm Res. 2022;39:1701–31.
Google Scholar
European Medicines Agency. Guideline on the reporting of physiologically based pharmacokinetic (PBPK) modelling and simulation. London, European Medicines Agency; 2018. Accessed 14 Mar 2024.
Kuemmel C, Yang Y, Zhang X, Florian J, Zhu H, Tegenge M, et al. Consideration of a credibility assessment framework in model-informed drug development: potential application to physiologically-based pharmacokinetic modeling and simulation. CPT Pharmacomet Syst Pharmacol. 2020;9:21–8.
Google Scholar
Brozek JL, Canelo-Aybar C, Akl EA, Bowen JM, Bucher J, Chiu WA, et al. GRADE guidelines 30: the GRADE approach to assessing the certainty of modeled evidence—an overview in the context of health decision-making. J Clin Epidemiol. 2021;129:138–50.
Google Scholar
Devine A, Battle KE, Meagher N, Howes RE, Dini S, Gething PW, et al. Global economic costs due to vivax malaria and the potential impact of its radical cure: a modelling study. PLoS Med. 2021;18: e1003614.
Google Scholar
White MT, Yeung S, Patouillard E, Cibulskis R. Costs and cost-effectiveness of Plasmodium vivax control. Am J Trop Med Hyg. 2016;95:52–61.
Google Scholar
El Gaaloul M, Tornesi B, Lebus F, Reddy D, Kaszubska W. Re-orienting anti-malarial drug development to better serve pregnant women. Malar J. 2022;21:121.
Google Scholar
Alexe A, Garg A, Kovacs B, Abramova N, Apara O, Eisele O, et al. Regulations governing medicines for maternal and neonatal health: a landscape assessment. Ther Innov Regul Sci. 2024;58:242–57.
Google Scholar
Weld ED, Bailey TC, Waitt C. Ethical issues in therapeutic use and research in pregnant and breastfeeding women. Br J Clin Pharmacol. 2022;88:7–21.
Google Scholar
Illamola SM, Bucci-Rechtweg C, Costantine MM, Tsilou E, Sherwin CM, Zajicek A. Inclusion of pregnant and breastfeeding women in research—efforts and initiatives. Br J Clin Pharmacol. 2018;84:215–22.
Google Scholar
Jorgensen SCJ, Miljanic S, Tabbara N, Somanader D, Leung F, De Castro C, et al. Inclusion of pregnant and breastfeeding women in nonobstetrical randomized controlled trials. Am J Obstet Gynecol MFM. 2022;4: 100700.
Google Scholar
link
-1728475433994.jpg "Doctor Lists Tips For Protecting Your Eyes During Work From Home")
