Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density

Bradley, John; Stone, Will; Da, Dari F.; Morlais, Isabelle; Dicko, Alassane; Cohuet, Anna; Guelbeogo, Wamdaogo M.; Mahamar, Almahamoudou; Nsango, Sandrine E.; Soumaré, Harouna M; Diawara, Halimatou; Lanke, Kjerstin; Graumans, Wouter; Siebelink-Stoter, Rianne; Vegte‐Bolmer, Marga van de; Chen, Ingrid; Tiono, Alfred B.; Gonçalves, Bronner P.; Gosling, Roland; Sauerwein, Robert W.; Drakeley, Chris; Churcher, Thomas S.; Bousema, Teun

doi:10.7554/elife.34463

Cited by 108 publications

(155 citation statements)

References 35 publications

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“…Whether the differences between studies result from variation in parasite thermal sensitivity between strains, or other factors, is not known. Our data, together with those of Bradley et al 52 and Pathak et al . 53 , suggest variation in gametocyte densities between feeds/hosts could mediate the effects of temperature on parasite establishment (i.e.…”

Section: Discussionsupporting

confidence: 90%

The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria

Suh

Grossman

Waite

et al. 2019

Preprint

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AbstractInsecticide-treated bed nets reduce malaria transmission by limiting contact between mosquito vectors and human hosts when mosquitoes feed during the night. However, malaria vectors can also feed in the early evening and in the morning when people are not protected. Here, we explored how timing of blood feeding interacts with environmental temperature to influence the capacity of Anopheles mosquitoes to transmit the human malaria parasite, Plasmodium falciparum. We found no effect of biting time itself on the proportion of mosquitoes that became infectious (vector competence) at constant temperature. However, when mosquitoes were maintained under more realistic fluctuating temperatures there was a significant increase in competence for mosquitoes feeding in the evening, and a significant reduction in competence for those feeding in the morning, relative to those feeding at midnight. These effects appear to be due to thermal sensitivity of malaria parasites during the initial stages of parasite development within the mosquito, and the fact that mosquitoes feeding in the evening experience cooling temperatures during the night, whereas mosquitoes feeding in the morning quickly experience warming temperatures that are inhibitory to parasite establishment. A transmission dynamics model illustrates that such differences in competence could have important implications for disease endemicity, the extent of transmission that persists in the presence of bed nets, and the epidemiological impact of behavioural resistance. These results indicate the interaction of temperature and feeding behaviour to be a major ecological determinant of the vectorial capacity of malaria mosquitoes.

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Section: Discussionsupporting

confidence: 90%

The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria

Suh

Grossman

Waite

et al. 2019

Preprint

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“…For this purpose, significant efforts have been made to develop new molecular tools to detect and estimate more precisely the gametocyte densities for both males and females. It is interesting to note that these methods have also significantly improved the prediction of mosquito infection rates (19). Nevertheless, a significant level of uncertainty remains.…”

Section: Discussionmentioning

confidence: 99%

“…A mosquito blood meal represents a volume of 1.5 to 4μl on average (17, 18) and it needs to contain at least one gametocyte (sexual stage) of both sexes to result in malaria infection. Although the shape of the relationship between gametocyte densities measured in the human blood and the probability or the intensity of mosquito infection is not always clear, the likelihood of mosquito infection seems to be mainly dictated by gametocyte density (19, 20). Therefore, the number of gametocytes in human blood is frequently used as an indicator of human-to-mosquito transmission potential (21–23).…”

Section: Introductionmentioning

confidence: 99%

“…Robust estimation of gametocyte density is therefore essential to the identification of the human infection reservoir. Although, sensitive molecular techniques have been developed to significantly improve the detection, quantification and possibly sex determination of gametocytes (19, 21, 24–26), the temporal and spatial dynamics of gametocyte distribution and infectivity in vertebrate hosts remain relatively neglected. Gametocyte density are mostly estimated from a single blood sample from a single body location (e.g.…”

Section: Introductionmentioning

confidence: 99%

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Opening Pandora’s Box: Distribution of Plasmodium gametocytes in bloodstream

Pigeault¹,

Isaïa²,

Yerbanga

et al. 2019

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10Malaria, a vector borne disease caused by Plasmodium spp., remains a major global cause of 11 morbidity and mortality. Optimization of the disease control strategies requires a thorough 12 understanding of the fundamental processes underlying parasite transmission. Although the 13 number of transmissible stages of Plasmodium (gametocyte) in human blood is frequently 14 used as an indicator of human-to-mosquito transmission potential, this relationship is not 15 always clear. Important efforts have been made to develop molecular tools to fine-tune 16 gametocyte densities estimation and therefore improve the prediction of mosquito infection 17 rates, but a significant level of uncertainty around this estimate remains. Here we show with 18 both human and avian malaria system that the within-vertebrate host distribution of 19 gametocytes could explain much of this uncertainty. By comparing gametocyte densities in 20 bloodstream between different body parts, we found a difference by nearly 50% in humans 21 and by more than 15% in birds. An estimation of gametocyte density from only one blood 22 sample, as is usually the case, could therefore drastically over-or underestimated the 23 infectivity of gametocyte carriers. This might have important consequences on the 24 epidemiology of the disease since we show, using the avian malaria system, that this variation 25 influences the transmission of the parasite to the mosquito vector. In the light of our results, 26 we argue that it is essential to consider the heterogeneous distribution of gametocyte to 27 improve human diagnosis, identify infectious reservoirs and to test new malaria control 28 strategies. 29 30

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“…[27, 28], and so, attempts to fertilise senesced females may "waste" males [29]. In this scenario, 257 parasite evolution is shaped by processes operating in the vector.…”

Section: Onwards Transmission Is Determined By Time-of-day Of Both Pamentioning

confidence: 99%

Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes

Schneider

Rund

Smith

et al. 2018

Preprint

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18That periodicity in the biting activity of mosquito vectors explains why malaria parasites have 19 evolved rhythms in cycles of asexual replication in the host's blood was proposed almost 50 years 20ago. Yet, tests of this hypothesis have proved inconclusive. Using the rodent malaria Plasmodium 21 chabaudi, we examine rhythms in the density and infectivity of transmission forms (gametocytes) 22 in the host's blood, parasite development inside mosquitoes, and onwards transmission. 23Moreover, we control for the confounding effects of rhythms in mosquito susceptibility. We reveal 24 that at night, gametocytes are twice as infective to mosquitoes, despite being less numerous in 25 the blood. This enhanced infectiousness at night interacts with mosquito rhythms to increase 26 sporozoite burdens by almost four-fold when mosquitoes feed during their day. Thus, daytime 27 blood-feeding (e.g. driven by the use of bed nets) may render gametocytes less infective, but this 28 is compensated for by the greater susceptibility of mosquitoes. 29 2 30

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Predicting the likelihood and intensity of mosquito infection from sex specific Plasmodium falciparum gametocyte density

Cited by 108 publications

References 35 publications

The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria

The influence of feeding behaviour and temperature on the capacity of mosquitoes to transmit malaria

Opening Pandora’s Box: Distribution of Plasmodium gametocytes in bloodstream

Adaptive periodicity in the infectivity of malaria gametocytes to mosquitoes

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