Effect of irradiation on the survival and susceptibility of female Anopheles arabiensis to natural isolates of Plasmodium falciparum

Abstract

Background: The sterile insect technique (SIT) is a vector control strategy relying on the mass release of sterile males into wild vector populations. Current sex separation techniques are not fully efficient and could lead to the release of a small proportion of females. It is therefore important to evaluate the effect of irradiation on the ability of released females to transmit pathogens. This study aimed to assess the effect of irradiation on the survival and competence of Anopheles arabiensis females for Plasmodium falciparum in laboratory conditions. Methods: Pupae were irradiated at 95 Gy of gamma-rays, and emerging females were challenged with one of 14 natural isolates of P. falciparum. Seven days post-blood meal (dpbm), irradiated and unirradiated-control females were dissected to assess the presence of oocysts, using 8 parasite isolates. On 14 dpbm, sporozoite dissemination in the head/thorax was also examined, using 10 parasites isolates including 4 in common with the 7 dpbm dissection (oocyst data). The survivorship of irradiated and unirradiated-control mosquitoes was monitored. Results: Overall, irradiation reduced the proportion of mosquitoes infected with the oocyst stages by 17% but this effect was highly inconsistent among parasite isolates. Secondly, there was no significant effect of irradiation on the number of developing oocysts. Thirdly, there was no significant difference in both the sporozoite infection rate and load between the irradiated and unirradiated-control mosquitoes. Fourthly, irradiation had varying effects on female survival with either a negative effect or no effect. Conclusions: The effect of irradiation on mosquito competence strongly varied among parasite isolates. Because of such isolate variability and, the fact that different parasite isolates were used to collect oocyst and sporozoite data, the irradiation-mediated reduction of oocyst prevalence was not confirmed for the sporozoite stages. Our data indicate that irradiated female An. arabiensis could contribute to malaria transmission, and highlight the need for perfect sexing tools, which would prevent the release of females as part of SIT programmes.

Effects of radiation on the fitness, sterility and arbovirus susceptibility of a Wolbachia‐free Aedes albopictus strain for use in the sterile insect technique

“…3(c),(d)), indicating that irradiation did not change the virus susceptibility of GT females. Similar results have been reported showing that irradiation did not increase susceptibility to pathogens such as dengue and chikungunya virus 46,53 or Plasmodium falciparum 54 . It must be noted that the irradiation exposures were performed at the pupal stage in both studies.…”

Impact of Irradiation on Vector Competence of Aedes aegypti and Aedes albopictus (Diptera: Culicidae) for Dengue and Chikungunya Viruses

“…Because irradiation may adversely influence the quality of the insect to be released through mutations in the somatic cells, it is essential to select the optimum radiation dose that effectively sterilizes the insect without adversely affecting the insect's competitiveness (Bakri et al, 2005;Parker et al, 2021). Dose-dependent radiation damage to the insect's mid-gut has been previously identified as the main factor affecting changes in the infection levels and in the alteration in the gut bacterial communities (Lauzon and Potter, 2012;Woruba et al, 2019;Guissou et al, 2020). The structural damages observed in the mid-gut tissues of irradiated flies lead to metabolic and physiological abnormalities (Lauzon and Potter, 2012) and could be related to the increased dissemination efficiency observed in irradiated female mosquitoes in this study.…”

“…Virus transmission by arthropods is a complex process (vector competence) controlled by biological intrinsic barriers in the vectors, including barriers affecting virus amplification in the mid-gut cells, dissemination in the insect's body fluid (hemolymph), and finally, infection and amplification in the salivary glands as the last stage before transmission to a new host. Ionizing radiation can influence the competence of different mosquitoes for pathogens and viruses through alterations of their immune response, and therefore, their ability to effectively transmit these arboviruses (Guissou et al, 2020). Radiation can also seriously alter symbiotic gut microbiota which is linked to the insect ecological fitness (Cai et al, 2018) and can affect immune responses that can influence vector competence for human pathogens (Dennison et al, 2014).…”

Contrasting effects of the alkaloid ricinine on the capacity of Anopheles gambiae and Anopheles coluzzii to transmit Plasmodium falciparum

“…gambiae or An. coluzzii , depending on availability, see below) were fed with blood drawn from naturally P. falciparum gametocyte-infected patients recruited among 5–12-year-old school children in villages surrounding Bobo-Dioulasso, Burkina Faso, using Direct membrane feeding assays (DMFA) as previously described [ 18 , 27 ]. Briefly, thick blood smears were taken from each volunteer, air-dried, Giemsa-stained and examined by microscopy for the presence of P. falciparum at the IRSS laboratory in Bobo-Dioulasso.…”

“…Oocyst rupture in the mosquito midgut and sporozoite invasion of salivary glands are highly asynchronous. While some oocysts are intact and keep developing on 9–12 dpbm, others have already ruptured and released their sporozoites [ 26 , 27 ]. To explore possible differences in the timing of sporozoite dissemination in mosquito salivary glands between ricinine-fed and control females, three metrics were measured [ 26 , 27 ]: The proportion of infected mosquitoes with ruptured oocysts on 10–12 dpbm; the number of mosquitoes with at least one ruptured oocyst in their midguts out of the total number of infected mosquitoes (i.e.…”