Widespread zoophagy and detection of Plasmodium spp. in Anopheles mosquitoes in southeastern Madagascar

Abstract

Background Malaria is a top cause of mortality on the island nation of Madagascar, where many rural communities rely on subsistence agriculture and livestock production. Understanding feeding behaviours of Anopheles in this landscape is crucial for optimizing malaria control and prevention strategies. Previous studies in southeastern Madagascar have shown that Anopheles mosquitoes are more frequently captured within 50 m of livestock. However, it remains unknown whether these mosquitoes preferentially feed on livestock. Here, mosquito blood meal sources and Plasmodium sporozoite rates were determined to evaluate patterns of feeding behaviour in Anopheles spp. and malaria transmission in southeastern Madagascar. Methods Across a habitat gradient in southeastern Madagascar 7762 female Anopheles spp. mosquitoes were collected. Of the captured mosquitoes, 492 were visibly blood fed and morphologically identifiable, and a direct enzyme-linked immunosorbent assay (ELISA) was used to test for swine, cattle, chicken, human, and dog blood among these specimens. Host species identification was confirmed for multiple blood meals using PCR along with Sanger sequencing. Additionally, 1,607 Anopheles spp. were screened for the presence of Plasmodium falciparum, P. vivax-210, and P. vivax 247 circumsporozoites (cs) by ELISA. Results Cattle and swine accounted, respectively, for 51% and 41% of all blood meals, with the remaining 8% split between domesticated animals and humans. Of the 1,607 Anopheles spp. screened for Plasmodium falciparum, Plasmodium vivax 210, and Plasmodium vivax 247 cs-protein, 45 tested positive, the most prevalent being P. vivax 247, followed by P. vivax 210 and P. falciparum. Both variants of P. vivax were observed in secondary vectors, including Anopheles squamosus/cydippis, Anopheles coustani, and unknown Anopheles spp. Furthermore, evidence of coinfection of P. falciparum and P. vivax 210 in Anopheles gambiae sensu lato (s.l.) was found. Conclusions Here, feeding behaviour of Anopheles spp. mosquitoes in southeastern Madagascar was evaluated, in a livestock rich landscape. These findings suggest largely zoophagic feeding behaviors of Anopheles spp., including An. gambiae s.l. and presence of both P. vivax and P. falciparum sporozoites in Anopheles spp. A discordance between P. vivax reports in mosquitoes and humans exists, suggesting high prevalence of P. vivax circulating in vectors in the ecosystem despite low reports of clinical vivax malaria in humans in Madagascar. Vector surveillance of P. vivax may be relevant to malaria control and elimination efforts in Madagascar. At present, the high proportion of livestock blood meals in Madagascar may play a role in buffering (zooprophylaxis) or amplifying (zoopotentiation) the impacts of malaria. With malaria vector control efforts focused on indoor feeding behaviours, complementary approaches, such as endectocide-aided vector control in livestock may be an effective strategy for malaria reduction in Madagascar.

Blood meal profile and positivity rate with malaria parasites among different malaria vectors in Sudan

“…The low prevalence of fed females (12.9%) reported in this study compared to gravid females (49.1%), supports the assumption that mosquito collection for blood meal analysis is mainly affected by the resting position especially after taking the blood meal [ 42 ]. Recently, a study conducted by Finney et al indicated that most of the human blood meals were from Anopheles mosquitoes trapped outdoors, while many livestock blood meals were from Anopheles mosquitoes trapped indoors [ 44 ].…”

“…These results disagree with a previous report from Burkina Faso, where human blood meal source was more than 80% [ 47 ]. However, this variation can be as a result of host availability in that specific region [ 44 ].…”

“…Although, this assumption is not fully supported by this study, either through animal screening or sporozoite detection in the salivary glands of the infected vector. However, it can hint to the need for a wide animal screening especially during the non-transmission seasons of malaria [ 44 ]. These results should be interpreted with caution.…”

A Follow-Up to the Geographical Distribution of Anopheles Species in Malaria-Endemic and Non-Endemic Areas of Honduras

“…Several authors have reported mosquitoes infected by Plasmodium spp. in Africa [ 59 , 60 , 61 , 62 ] and the Amazon Basin in South America [ 47 , 51 , 55 ] where higher rates of transmission have been reported. The absence of infected mosquitoes was not unexpected due to the low number of malaria cases reported in Gracias a Dios, Bay Islands, and El Paraíso, during the years of collection (average of 380, 7, and 18 cases per year, respectively), and the absence of malaria cases in Cortés and Comayagua.…”

Plasmodium vivax: the potential obstacles it presents to malaria elimination and eradication

“…In addition, many P. vivax vectors are early biters and outdoor feeders and exhibit outdoor-resting patterns [ 68 ]. These characteristics are supposed to make it easier to get through control measures such as insecticide-treated nets (ITNs) or indoor residual spray (IRS).…”