High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host

Pichon, G.; Awono-Ambene, Herman Parfait; Robert, Vincent

doi:10.1017/s0031182099006277

Cited by 71 publications

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“…Pinchon et al (26) found high heterogeneity in the number of Plasmodium falciparum gametocytes in the blood meal of mosquitoes feeding on the same host and an overdispersed distribution of gametocytes ingested by mosquitoes. Similarly, feeding behavior and spirochete maintenance may vary in ticks feeding on the same host in a way that generates an aggregated distribution of spirochete loads.…”

Section: Discussionmentioning

confidence: 99%

Real-Time PCR for Simultaneous Detection and Quantification of Borrelia burgdorferi in Field-Collected Ixodes scapularis Ticks from the Northeastern United States

Wang¹,

Liveris²,

Brei

et al. 2003

Appl Environ Microbiol

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The density of spirochetes in field-collected or experimentally infected ticks is estimated mainly by assays based on microscopy. In this study, A high degree of spirochete aggregation among infected ticks (variance-to-mean ratio of 24,877; moment estimate of k ‫؍‬ 0.279) was observed. From the frequency distribution data and previously published transmission studies, we estimated that a minimum of 300 organisms may be required in a host-seeking nymphal tick to be able to transmit infection to mice while feeding on mice. These data indicate that real-time qPCR is a reliable approach for simultaneous detection and quantification of B. burgdorferi infection in field-collected ticks and can be used for ecological and epidemiological surveillance of Lyme disease spirochetes.Hard ticks (Ixodidae) in the Ixodes persulcatus complex, such as Ixodes scapularis and Ixodes pacificus in North America, Ixodes ricinus in Europe, and Ixodes persulcatus in far eastern Russia and Asia, are the principal vectors of the Lyme disease spirochete, Borrelia burgdorferi, and several other tick-borne pathogens (2, 25). The incidence of human Lyme disease in areas where it is endemic is correlated with the abundance and prevalence of Ixodes ticks infected with B. burgdorferi (34). Moreover, studies of laboratory animals have suggested that the efficiency of host infection is determined in part by the number of spirochetes inoculated using a needle or deposited by the tick at the time of feeding (21, 27). Thus, monitoring B. burgdorferi density in host-seeking ticks will provide more accurate data for assessment of population risk of Lyme disease and the potential variability of disease manifestations after tick bites.Currently, the number of spirochetes in field-collected or experimentally infected Ixodes ticks is estimated mainly by microscopy-based assays in which the spirochetes are counted directly on tick midgut smears stained with fluorescently labeled specific antibodies (8, 9, 27) or on silver-stained histological sections of ticks (11,14). For specific detection of B. burgdorferi in field-collected adult I. scapularis ticks and monitoring of the spirochete kinetics during the tick life cycle, an OspA antigen-capture enzyme-linked immunosorbent assay (ELISA) was also developed (3-5). These methods are laborintensive, which limits the number of ticks that can be analyzed. Moreover, the sensitivities of these methods are relatively low, e.g., a lower detection limit of approximately 150 spirochetes was reported for the antigen-capture ELISA (5).Real-time PCR has features that allow for rapid detection of infectious pathogens in environmental or experimentally infected animal tissues and clinical specimens (38). The technique has recently been employed to detect the presence of B. burgdorferi DNA in I. ricinus ticks from Switzerland (15), to quantify the spirochete loads in experimentally infected animal tissues (23,24,35), and to differentiate the three B. burgdorferi sensu lato species that are pathogenic to humans in Europe (22,2...

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Section: Discussionmentioning

confidence: 99%

Real-Time PCR for Simultaneous Detection and Quantification of Borrelia burgdorferi in Field-Collected Ixodes scapularis Ticks from the Northeastern United States

Wang¹,

Liveris²,

Brei

et al. 2003

Appl Environ Microbiol

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“…This makes the observed efficiency of transmission at low gametocyte concentrations even more intriguing. Unknown mechanisms may facilitate an aggregation of gametocytes that favors the encounter of males and females (352). One of these mechanisms may be a transmission-enhancing effect of antigametocyte antibodies (152,195,349), possibly directed against currently unknown antigens (459, 491).…”

Section: Gametocyte Density and Mosquito Infection Ratesmentioning

confidence: 99%

“…It is conceivable that infective gametocytes actively seek subdermal sites to enhance their transmission potential. Subdermal clustering has been hypothesized to be related to the crescent shape of P. falciparum gametocyte-infected erythrocytes (304), and clustering of gametocytes in mosquito blood meals suggests some additional mechanism for aggregation (352). A unique study from 1952 is often cited in this respect and provides direct, albeit incomplete, evidence for preferential sequestration in the subdermal capillaries.…”

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confidence: 99%

Epidemiology and Infectivity of Plasmodium falciparum and Plasmodium vivax Gametocytes in Relation to Malaria Control and Elimination

2011

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SUMMARY Malaria remains a major cause of morbidity and mortality in the tropics, with Plasmodium falciparum responsible for the majority of the disease burden and P. vivax being the geographically most widely distributed cause of malaria. Gametocytes are the sexual-stage parasites that infect Anopheles mosquitoes and mediate the onward transmission of the disease. Gametocytes are poorly studied despite this crucial role, but with a recent resurgence of interest in malaria elimination, the study of gametocytes is in vogue. This review highlights the current state of knowledge with regard to the development and longevity of P. falciparum and P. vivax gametocytes in the human host and the factors influencing their distribution within endemic populations. The evidence for immune responses, antimalarial drugs, and drug resistance influencing infectiousness to mosquitoes is reviewed. We discuss how the application of molecular techniques has led to the identification of submicroscopic gametocyte carriage and to a reassessment of the human infectious reservoir. These components are drawn together to show how control measures that aim to reduce malaria transmission, such as mass drug administration and a transmission-blocking vaccine, might better be deployed.

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“…High gametocyte densities do not necessarily result in mosquito infection (Graves et al 1988;Gamage-Mendis et al 1991;Schneider et al 2007), whereas individuals with low densities that carry no observable gametocytes have been found to be infectious (Jeffery and Eyles 1955;Muirhead-Thomson 1998;Coleman et al 2004;Schneider et al 2007). This heterogeneity in mosquito infection may result in part from sampling bias: Samples are generally collected via venipuncture but there may be a specified localization or clustering of gametocytes in the human vasculature during a blood meal (Pichon et al 2000). Similarly, in P. vivax infections, the relationship between gametocyte density and mosquito infection is poorly defined which is attributed to limited sensitivity of microscopy to detect and differentiate gametocyte stages (Gamage-Mendis et al 1991;Bharti et al 2006).…”

Section: Relationship Between Gametocyte Density and Infectiousness Tmentioning

confidence: 99%

Biology of Malaria Transmission

Meibalan

Marti

2016

Cold Spring Harb Perspect Med

135

137

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Understanding transmission biology at an individual level is a key component of intervention strategies that target the spread of malaria parasites from human to mosquito. Gametocytes are specialized sexual stages of the malaria parasite life cycle developed during evolution to achieve crucial steps in transmission. As sexual differentiation and transmission are tightly linked, a deeper understanding of molecular and cellular events defining this relationship is essential to combat malaria. Recent advances in the field are gradually revealing mechanisms underlying sexual commitment, gametocyte sequestration, and dynamics of transmissible stages; however, key questions on fundamental gametocyte biology still remain. Moreover, species-specific variation between Plasmodium falciparum and Plasmodium vivax transmission dynamics pose another significant challenge for worldwide malaria elimination efforts. Here, we review the biology of transmission stages, highlighting numerous factors influencing development and dynamics of gametocytes within the host and determinants of human infectiousness. C urrent measures for malaria elimination have been inspired by the Global Malaria Eradication Program (GMEP), which operated under the World Health Organization (WHO) between 1955 and 1969. The strategy of GMEP was largely based on dichlorodiphenyltrichloroethane (DDT)-based indoor residual spraying (DDT-IRS) complemented with mass drug administration (Pampana 1969). Although GMEP was able to eliminate malaria from many regions of the world, it was eventually abandoned because of technical challenges, increasing spread of both insecticide resistance and drug-resistant parasite strains, and lack of continuous political support (Najera et al. 2011 ual parasites and early transmission stages, whereas mature infectious transmission stages are unaffected. To block transmission, ACT is often combined with the only transmissionblocking drug on the market, Primaquine. However, recent emergence of artemisinin resistance in Southeast Asia asks for urgent evaluation of alternative treatment strategies (Noedl et al. 2008;Dondorp et al. 2009;Mbengue et al. 2015;Straimer et al. 2015).Of the five Plasmodium species known to cause malaria in humans, Plasmodium falciparum is lethal and responsible for severe disease pathology and the majority of deaths due to malaria, especially in sub-Saharan Africa. Plasmodium vivax typically causes milder infections than P. falciparum but has a much greater geographical distribution (Gething et al. 2012). The clinical symptoms of malaria are largely a result of the replication of asexual stages in human blood, but transmission to mosquitoes is only achieved through the development of sexual stages, termed gametocytes. To abrogate transmission of P. falciparum, we must be able to clear asexual and sexual stages from the human host, eventually rendering an individual noninfectious to mosquitoes. However, in the case of P. vivax, elimination is highly challenging because of the relapse of dormant liver-stage h...

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High heterogeneity in the number of Plasmodium falciparum gametocytes in the bloodmeal of mosquitoes fed on the same host

Cited by 71 publications

References 0 publications

Real-Time PCR for Simultaneous Detection and Quantification of Borrelia burgdorferi in Field-Collected Ixodes scapularis Ticks from the Northeastern United States

Real-Time PCR for Simultaneous Detection and Quantification of Borrelia burgdorferi in Field-Collected Ixodes scapularis Ticks from the Northeastern United States

Epidemiology and Infectivity of Plasmodium falciparum and Plasmodium vivax Gametocytes in Relation to Malaria Control and Elimination

Biology of Malaria Transmission

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