Multiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential.

Multiple blood feeding in mosquitoes shortens the Plasmodium falciparum incubation period and increases malaria transmission potential.
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DOI:
10.1371/journal.ppat.1009131
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发表时间:
2020-12
期刊:
影响因子:
6.7
通讯作者:
Catteruccia F
Catteruccia F
中科院分区:
医学1区
文献类型:
--
作者:
Shaw WR;Holmdahl IE;Itoe MA;Werling K;Marquette M;Paton DG;Singh N;Buckee CO;Childs LM;Catteruccia F

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许多蚊子物种,包括主要的疟疾媒介冈比亚按蚊,在其生命周期中自然经历吸血,卵发育和产卵的多个生殖周期。当蚊子实验性感染疟疾寄生虫时,这种复杂的蚊子行为经常被忽视,限制了我们准确描述传播潜在影响的能力。在这里,我们研究如何恶性疟原虫的发展和传播潜力受到影响时,感染的蚊子饲料额外的时间。我们测量了恶性疟原虫卵囊的大小,并进行了子孢子时间过程分析,以确定寄生虫的外源性潜伏期(EIP),即寄生虫达到感染性子孢子阶段所需的时间,在An。冈比亚雌性吸血一次或两次。感染后3天的额外血液喂养显著加速卵囊生长速率,导致唾液腺中子孢子的早期积累,从而缩短EIP(减少2.3 ± 0.4天)。此外,寄生虫的生长在生殖能力降低的转基因蚊子中进一步加速,这模拟了目前在种群抑制基因驱动中提出的遗传修饰。我们将我们缩短的EIP值纳入传输潜力的衡量标准,即基本再生数R 0,并发现撒哈拉以南非洲的平均R 0比使用传统EIP测量时更高(范围:10.1%-12.1%)。这些数据表明,消灭疟疾可能更具挑战性,年轻的蚊子或生殖能力下降的蚊子可能比目前认为的更容易感染。我们的研究结果对当前和未来的蚊子控制干预措施具有深远的影响。在自然环境中,雌性冈比亚按蚊是主要的疟疾传播媒介,在其一生中会多次吸血。在这里,我们证明了一个额外的血液饲料加速恶性疟原虫疟疾寄生虫在这种蚊子的增长。将这些数据转化为撒哈拉以南非洲地区的数学模型表明,疟疾传播的潜力可能比以前认为的要高,这使得消除疾病更加困难。此外,我们表明,控制策略,操纵蚊子繁殖的目的是抑制按蚊种群可能无意中有利于疟疾传播。我们的数据还表明,寄生虫可以通过较年轻的蚊子传播,这些蚊子对杀虫剂的杀灭不太敏感,这对基于杀虫剂的策略的成功具有负面影响。
Many mosquito species, including the major malaria vector Anopheles gambiae, naturally undergo multiple reproductive cycles of blood feeding, egg development and egg laying in their lifespan. Such complex mosquito behavior is regularly overlooked when mosquitoes are experimentally infected with malaria parasites, limiting our ability to accurately describe potential effects on transmission. Here, we examine how Plasmodium falciparum development and transmission potential is impacted when infected mosquitoes feed an additional time. We measured P. falciparum oocyst size and performed sporozoite time course analyses to determine the parasite’s extrinsic incubation period (EIP), i.e. the time required by parasites to reach infectious sporozoite stages, in An. gambiae females blood fed either once or twice. An additional blood feed at 3 days post infection drastically accelerates oocyst growth rates, causing earlier sporozoite accumulation in the salivary glands, thereby shortening the EIP (reduction of 2.3 ± 0.4 days). Moreover, parasite growth is further accelerated in transgenic mosquitoes with reduced reproductive capacity, which mimic genetic modifications currently proposed in population suppression gene drives. We incorporate our shortened EIP values into a measure of transmission potential, the basic reproduction number R0, and find the average R0 is higher (range: 10.1%–12.1% increase) across sub-Saharan Africa than when using traditional EIP measurements. These data suggest that malaria elimination may be substantially more challenging and that younger mosquitoes or those with reduced reproductive ability may provide a larger contribution to infection than currently believed. Our findings have profound implications for current and future mosquito control interventions. In natural settings the female Anopheles gambiae mosquito, the major malaria vector, blood feeds multiple times in her lifespan. Here we demonstrate that an additional blood feed accelerates the growth of Plasmodium falciparum malaria parasites in this mosquito. Incorporating these data into a mathematical model across sub-Saharan Africa reveals that malaria transmission potential is likely to be higher than previously thought, making disease elimination more difficult. Additionally, we show that control strategies that manipulate mosquito reproduction with the aim of suppressing Anopheles populations may inadvertently favor malaria transmission. Our data also suggest that parasites can be transmitted by younger mosquitoes, which are less susceptible to insecticide killing, with negative implications for the success of insecticide-based strategies.
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