Contrasting epidemiology and genetic variation of Plasmodium vivax infecting Duffy-negative individuals across Africa

Lo, Eugenia; Russo, Gianluca; Pestana, Kareen; Kepple, Daniel; Abagero, Beka Raya; Dongho, Ghyslaine Bruna Djeunang; Gunalan, Karthigayan; Miller, Louis H.; Hamid, Muzamil Mahdi Abdel; Yewhalaw, Delenasaw; Paganotti, Giacomo Maria

doi:10.1016/j.ijid.2021.05.009

Cited by 24 publications

(51 citation statements)

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“…The last one gives rise to Duffy-negative phenotypes [ 9 , 10 ] and was thought to confer innate resistance to blood-stage infection with P. vivax and clinical malaria [ 11 ]. Recently, however, the widespread detection of P. vivax across individuals lacking Duffy antigen in many African countries [ 9 , 12 – 17 ] including Ethiopia [ 13 , 18 , 19 ] further complicates the current understanding of vivax malaria epidemiology in the region.…”

Section: Introductionmentioning

confidence: 99%

Vivax malaria in Duffy-negative patients shows invariably low asexual parasitaemia: implication towards malaria control in Ethiopia

Abate

Bouyssou

Mabilotte

et al. 2022

Malar J

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Background The increase in detections of Plasmodium vivax infection in Duffy-negative individuals in Africa has challenged the dogma establishing the unique P. vivax Duffy Binding Protein-Duffy antigen receptor for chemokines (PvDBP-DARC) pathway used by P. vivax merozoites to invade reticulocytes. Information on the impact of Duffy antigen polymorphisms on the epidemiology of P. vivax malaria remains elusive. The objective of this study was to determine the distribution of asexual parasitaemia of P. vivax according to the Duffy antigen polymorphisms in Ethiopia. Methods DNA was extracted from dried blood spots (DBS) collected from prospectively recruited 138 P. vivax-infected patients from health centres. The identification and estimation of P. vivax asexual parasitaemia were performed by microscopic examination and quantitative real-time polymerase chain reaction (PCR). Duffy genotyping was conducted by DNA sequencing in a total of 138 P.vivax infected samples. Results The proportion of Duffy-negatives (FY*BES/FY*BES) in P. vivax infected patients was 2.9% (4/138). Duffy genotype FY*B/FY*BES (48.6%) was the most common, followed by FY*A/FY*BES genotype (25.4%). In one patient, the FY*02 W.01/FY*02 N.01 genotype conferring a weak expression of the Fyb antigen was observed. All P.vivax infected Duffy-negative patients showed low asexual parasitaemia (≤ 110 parasites/µL). The median P. vivax parasitaemia in Duffy-negative patients (53 parasites/µL) was significantly lower than those found in homozygous and heterozygous individuals (P < 0.0001). Conclusion Plasmodium vivax in Duffy-negative patients shows invariably low asexual parasitaemia. This finding suggests that the pathway used by P. vivax to invade Duffy-negative reticulocytes is much less efficient than that used in Duffy-positives. Moreover, the low asexual parasitaemia observed in Duffy-negative individuals could constitute an ‘undetected silent reservoir', thus likely delaying the elimination of vivax malaria in Ethiopia.

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Section: Introductionmentioning

confidence: 99%

Vivax malaria in Duffy-negative patients shows invariably low asexual parasitaemia: implication towards malaria control in Ethiopia

Abate

Bouyssou

Mabilotte

et al. 2022

Malar J

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“…These results indicated that the highest prevalence of P. vivax infection among Duffy-negative individuals was identified in a Southern African study (Botswana, 86%, 95% CI 65%–95%) 27 , followed by Mid Africa (61%, 95% CI 6%–115%, I 2 = 99.59%, three studies 19 , 23 , 39 ), and North Africa (13%, 95% CI 9%–18%, I 2 = 100%, two studies 18 , 27 ). However, a low prevalence was reported in an East African study [6%, 95% CI 3%–9%, I 2 = 83.96%, five studies (six study areas) 25 , 27 , 29 , 41 , 43 ], followed by West Africa (4%, 95% CI 1%–8%, I 2 = 96.79%, two studies 24 , 42 ). But the lowest prevalence was reported in a South American study (Brazil, 1%, 95% CI 0%–2%, I 2 = 99.8%, two studies 20 , 21 ) (Fig.…”

Section: Resultsmentioning

confidence: 72%

“…Three studies 20 , 21 , 31 were conducted in South America (2/27, 7.4%) and Asia (1/27, 3.7%). Of the 24 African studies, six were conducted in East Africa (Ethiopia 28 , 43 , Madagascar 25 , 29 , Kenya 40 , and Ethiopia 41 ), seven in Mid Africa (Democratic Republic of Congo 19 , Cameroon 22 , 23 , 32 , 33 , 39 , Angola, and Equatorial Guinea 30 ), seven in West Africa (Mauritania 24 , 42 , Nigeria 36 , 37 , Senegal 34 , Mali 35 , and Benin 38 ), two in North Africa (Sudan 17 , 18 ), one in North and East Africa (Ethiopia and Sudan 26 ), and one in Ethiopia/Botswana/Sudan 27 . Twenty-two articles were cross-sectional studies (22/27, 81.5%), two were case-controls 12 , 40 , and one was a cohort study 35 .…”

Section: Resultsmentioning

confidence: 99%

“…Fourteen studies 18 – 21 , 23 – 25 , 27 – 29 , 39 , 41 – 43 , conducted in 16 areas and reporting P. vivax infection prevalence among Duffy-negative individuals, were included in the pooled prevalence meta-analysis. These results showed that the pooled prevalence was 25% (95% CI − 3%–53%, I 2 = 99.96%, Fig.…”

Section: Resultsmentioning

confidence: 99%

“…These finding confirmed data from previous studies and supported the hypothesis that Duffy-negativity was no longer protective against P. vivax infection. Nevertheless, a high prevalence of infection among Duffy-negative individuals was observed in West Africa 34 – 38 ), Mid Africa 19 , 22 , 23 , 30 , 32 , 33 , 39 ), North Africa 17 , 18 , 27 , East Africa 40 , and Southern Africa 27 . Our meta-analysis results showed that Duffy-negativity was protective against P. vivax infection in individuals from East Africa 25 , 28 , 29 , 41 , although several reports have documented about the infection of P. vivax in Duffy- negative individuals.…”

Section: Discussionmentioning

confidence: 98%

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Prevalence and risk of Plasmodium vivax infection among Duffy-negative individuals: a systematic review and meta-analysis

Wilairatana

Masangkay

Kotepui

et al. 2022

Sci Rep

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A better understanding of the occurrence and risk of Plasmodium vivax infection among Duffy-negative individuals is required to guide further research on these infections across Africa. To address this, we used a meta-analysis approach to investigate the prevalence of P. vivax infection among Duffy-negative individuals and assessed the risk of infection in these individuals when compared with Duffy-positive individuals. This study was registered with The International Prospective Register of Systematic Reviews website (ID: CRD42021240202) and followed Preferred Reporting Items for Systematic review and Meta-Analyses guidelines. Literature searches were conducted using medical subject headings to retrieve relevant studies in Medline, Web of Science, and Scopus, from February 22, 2021 to January 31, 2022. Selected studies were methodologically evaluated using the Joanna Briggs Institute (JBI) Critical Appraisal Tools to assess the quality of cross-sectional, case–control, and cohort studies. The pooled prevalence of P. vivax infection among Duffy-negative individuals and the odds ratio (OR) of infection among these individuals when compared with Duffy-positive individuals was estimated using a random-effects model. Results from individual studies were represented in forest plots. Heterogeneity among studies was assessed using Cochrane Q and I2 statistics. We also performed subgroup analysis of patient demographics and other relevant variables. Publication bias among studies was assessed using funnel plot asymmetry and the Egger’s test. Of 1593 retrieved articles, 27 met eligibility criteria and were included for analysis. Of these, 24 (88.9%) reported P. vivax infection among Duffy-negative individuals in Africa, including Cameroon, Ethiopia, Sudan, Botswana, Nigeria, Madagascar, Angola, Benin, Kenya, Mali, Mauritania, Democratic Republic of the Congo, and Senegal; while three reported occurrences in South America (Brazil) and Asia (Iran). Among studies, 11 reported that all P. vivax infection cases occurred in Duffy-negative individuals (100%). Also, a meta-analysis on 14 studies showed that the pooled prevalence of P. vivax infection among Duffy-negative individuals was 25% (95% confidence interval (CI) − 3%–53%, I2 = 99.96%). A meta-analysis of 11 studies demonstrated a decreased odds of P. vivax infection among Duffy-negative individuals (p = 0.009, pooled OR 0.46, 95% CI 0.26–0.82, I2 = 80.8%). We confirmed that P. vivax infected Duffy-negative individuals over a wide prevalence range from 0 to 100% depending on geographical area. Future investigations on P. vivax infection in these individuals must determine if Duffy-negativity remains a protective factor for P. vivax infection.

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Current Status of Malaria Control and Elimination in Africa: Epidemiology, Diagnosis, Treatment, Progress and Challenges

Li,

Docile,

Fisher

et al. 2024

J Epidemiol Glob Health

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The African continent carries the greatest malaria burden in the world. Falciparum malaria especially has long been the leading cause of death in Africa. Climate, economic factors, geographical location, human intervention and unstable security are factors influencing malaria transmission. Due to repeated infections and early interventions, the proportion of clinically atypical malaria or asymptomatic plasmodium carriers has increased significantly, which easily lead to misdiagnosis and missed diagnosis. African countries have made certain progress in malaria control and elimination, including rapid diagnosis of malaria, promotion of mosquito nets and insecticides, intermittent prophylactic treatment in high-risk groups, artemisinin based combination therapies, and the development of vaccines. Between 2000 and 2022, there has been a 40% decrease in malaria incidence and a 60% reduction in mortality rate in the WHO African Region. However, many challenges are emerging in the fight against malaria in Africa, such as climate change, poverty, substandard health services and coverage, increased outdoor transmission and the emergence of new vectors, and the growing threat of resistance to antimalarial drugs and insecticides. Joint prevention and treatment, identifying molecular determinants of resistance, new drug development, expanding seasonal malaria chemo-prevention intervention population, and promoting the vaccination of RTS, S/AS01 and R21/Matrix-M may help to solve the dilemma. China’s experience in eliminating malaria is conducive to Africa’s malaria prevention and control, and China-Africa cooperation needs to be constantly deepened and advanced. Our review aims to help the global public develop a comprehensive understanding of malaria in Africa, thereby contributing to malaria control and elimination.

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Contrasting epidemiology and genetic variation of Plasmodium vivax infecting Duffy-negative individuals across Africa

Cited by 24 publications

References 50 publications

Vivax malaria in Duffy-negative patients shows invariably low asexual parasitaemia: implication towards malaria control in Ethiopia

Vivax malaria in Duffy-negative patients shows invariably low asexual parasitaemia: implication towards malaria control in Ethiopia

Prevalence and risk of Plasmodium vivax infection among Duffy-negative individuals: a systematic review and meta-analysis

Current Status of Malaria Control and Elimination in Africa: Epidemiology, Diagnosis, Treatment, Progress and Challenges

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