Comparison of infectivity of Plasmodium vivax to wild-caught and laboratory-adapted (colonized) Anopheles arabiensis mosquitoes in Ethiopia

Chali, Wakweya; Ashine, Temesgen; Hailemeskel, Elifaged; Gashaw, Abrham; Tafesse, Temesgen; Lanke, Kjerstin; Esayas, Endashaw; Kedir, Soriya; Shumie, Girma; Behaksra, Sinknesh Wolde; Bradley, John; Yewhalaw, Delenasaw; Mamo, Hassen; Petros, Beyene; Drakeley, Chris; Gadisa, Endalamaw; Bousema, Teun; Tadesse, Fitsum G.

doi:10.1186/s13071-020-3998-2

Cited by 8 publications

(12 citation statements)

References 57 publications

(79 reference statements)

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“…Several factors are known to influence the variation in mosquito infection, including gametocytes density [ 44 ] and the presence of host immunity [ 45 ]. A positive association between gametocyte density and infectivity has been discovered in several other studies [ 9 , 43 , 46 ] but was not observed in the present study. This finding may reflect the presence of transmission-blocking components in the blood of Indian patients.…”

Section: Discussioncontrasting

confidence: 56%

“…stephensi with Plasmodium parasite blood [ 42 ]. The higher feeding efficiency of the colony compared with wild mosquitoes has also been reported for Anopheles arabiensis , and a longer starvation period is also preferred for wild-caught mosquitoes [ 43 ]. This finding guides the use of laboratory-colonized mosquitoes in feeding experiments, which offers a significant advantage over the use of wild mosquitoes in terms of logistics, ease of maintenance and handling, and scaling-up flexibility and reproducibility of the assays [ 12 ].…”

Section: Discussionmentioning

confidence: 99%

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Optimization of Plasmodium vivax sporozoite production from Anopheles stephensi in South West India

Mohanty

Souza

Harjai

et al. 2021

Malar J

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Background Efforts to study the biology of Plasmodium vivax liver stages, particularly the latent hypnozoites, have been hampered by the limited availability of P. vivax sporozoites. Anopheles stephensi is a major urban malaria vector in Goa and elsewhere in South Asia. Using P. vivax patient blood samples, a series of standard membrane-feeding experiments were performed with An. stephensi under the US NIH International Center of Excellence for Malaria Research (ICEMR) for Malaria Evolution in South Asia (MESA). The goal was to understand the dynamics of parasite development in mosquitoes as well as the production of P. vivax sporozoites. To obtain a robust supply of P. vivax sporozoites, mosquito-rearing and mosquito membrane-feeding techniques were optimized, which are described here. Methods Membrane-feeding experiments were conducted using both wild and laboratory-colonized An. stephensi mosquitoes and patient-derived P. vivax collected at the Goa Medical College and Hospital. Parasite development to midgut oocysts and salivary gland sporozoites was assessed on days 7 and 14 post-feeding, respectively. The optimal conditions for mosquito rearing and feeding were evaluated to produce high-quality mosquitoes and to yield a high sporozoite rate, respectively. Results Laboratory-colonized mosquitoes could be starved for a shorter time before successful blood feeding compared with wild-caught mosquitoes. Optimizing the mosquito-rearing methods significantly increased mosquito survival. For mosquito feeding, replacing patient plasma with naïve serum increased sporozoite production > two-fold. With these changes, the sporozoite infection rate was high (> 85%) and resulted in an average of ~ 22,000 sporozoites per mosquito. Some mosquitoes reached up to 73,000 sporozoites. Sporozoite production could not be predicted from gametocyte density but could be predicted by measuring oocyst infection and oocyst load. Conclusions Optimized conditions for the production of high-quality P. vivax sporozoite-infected An. stephensi were established at a field site in South West India. This report describes techniques for producing a ready resource of P. vivax sporozoites. The improved protocols can help in future research on the biology of P. vivax liver stages, including hypnozoites, in India, as well as the development of anti-relapse interventions for vivax malaria.

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Section: Discussioncontrasting

confidence: 56%

Section: Discussionmentioning

confidence: 99%

Optimization of Plasmodium vivax sporozoite production from Anopheles stephensi in South West India

Mohanty

Souza

Harjai

et al. 2021

Malar J

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“…The use of human blood samples naturally infected with P. vivax in mosquito-feeding assays allowed us to mimic natural infection events as they would occur in nature, making results of this study pertinent to the interpretation of data from field-collected Anopheles [ 29 ] using these methods for Plasmodium detection . The collection method of wild Anopheles and site-specific endemicity are important considerations in the interpretation of PCR-derived infection rates.…”

Section: Discussionmentioning

confidence: 99%

A comparison of PCR and ELISA methods to detect different stages of Plasmodium vivax in Anopheles arabiensis

et al. 2021

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Background In characterizing malaria epidemiology, measuring mosquito infectiousness informs the entomological inoculation rate, an important metric of malaria transmission. PCR-based methods have been touted as more sensitive than the current “gold-standard” circumsporozoite (CSP) ELISA. Wider application of PCR-based methods has been limited by lack of specificity for the infectious sporozoite stage. We compared a PCR method for detecting the parasite’s mitochondrial (mt) cytochrome oxidase I (COX-I) gene with ELISA for detecting circumsporozoite protein for identification of different life stages of the parasite during development within a mosquito. Methods A PCR-based method targeting the Plasmodium mt COX-I gene was compared with the CSP ELISA method to assess infectivity in Anopheles arabiensis colony mosquitoes fed on blood from patients infected with Plasmodium vivax. Mosquitoes were tested at six post-infection time points (days 0.5, 1, 6, 9, 12, 15). The head and thorax and the abdomen for each specimen were tested separately with each method. Agreement between methods at each infection stage was measured using Cohen’s kappa measure of test association. Results Infection status of mosquitoes was assessed in approximately 90 head/thorax and 90 abdomen segments at each time point; in total, 538 head/thorax and 534 abdomen segments were tested. In mosquitoes bisected after 0.5, 1, and 6 days post-infection (dpi), the mt COX-I PCR detected Plasmodium DNA in both the abdomen (88, 78, and 67%, respectively) and head/thorax segments (69, 60, and 44%, respectively), whilst CSP ELISA detected sporozoites in only one abdomen on day 6 post-infection. PCR was also more sensitive than ELISA for detection of Plasmodium in mosquitoes bisected after 9, 12, and 15 dpi in both the head and thorax and abdomen. There was fair agreement between methods for time points 9–15 dpi (κ = 0.312, 95% CI: 0.230–0.394). Conclusions The mt COX-I PCR is a highly sensitive, robust method for detecting Plasmodium DNA in mosquitoes, but its limited Plasmodium life-stage specificity cannot be overcome by bisection of the head and thorax from the abdomen prior to PCR. Thus, the mt COX-I PCR is a poor candidate for identifying infectious mosquitoes. Graphical Abstract

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“…The use of human blood samples naturally infected with P. vivax in mosquito-feeding assays allowed us to mimic natural infection events as they would occur in nature, making results of this study pertinent to the interpretation of data from eld-collected Anopheles [29] using these methods for Plasmodium detection. The collection method of wild Anopheles and site-speci c endemicity are important considerations in the interpretation of PCR-derived infection rate.…”

Section: Discussionmentioning

confidence: 99%

A Comparison of PCR and ELISA Methods to Detect Different Stages of Plasmodium Vivax in Anopheles Arabiensis.

Hendershot

Esayas

Sutcliffe³

et al. 2021

Preprint

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Background: In characterizing malaria epidemiology, measuring mosquito infectiousness informs the entomological inoculation rate, an important metric of malaria transmission. PCR-based methods have been touted as more sensitive than the current “gold-standard” circumsporozoite (CSP) ELISA. Wider application of PCR-based methods has been limited by lack of specificity for the infectious sporozoite stage. We compared a PCR method for detecting the parasite’s cytochrome oxidase I (COX-I) gene with ELISA for detecting circumsporozoite protein for identification of different life stages of the parasite during development within a mosquito. Methods: A PCR-based method targeting the Plasmodium COX-I gene was compared with the CSP ELISA method to assess infectivity in Anopheles arabiensis colony mosquitoes fed on blood from patients infected with Plasmodium vivax. Mosquitoes were tested at six post-infection timepoints (days 0.5, 1, 6, 9, 12, 15). Head and thoraces, and abdomens for each specimen were tested separately with both methods. Agreement between methods at each infection stage was measured using Cohen’s Kappa measure of test association.Results: Infection status of mosquitoes was assessed in approximately 90 head and thoraces and 90 abdomens at each time point; in total 538 head and thoraces and 534 abdomens were tested. In mosquitoes bisected after 0.5, 1-, and 6-days post-infection, the COX-I PCR detected Plasmodium DNA in both the abdomens (88%, 78%, and 67%, respectively) and head and thoraces (69%, 60%, and 44%, respectively) whilst CSP-ELISA detect sporozoites in only 1 abdomen on day 6 post-infection. PCR was also more sensitive than ELISA for detection of Plasmodium in mosquitoes bisected after 9-, 12-, and 15-days post-infection in both the head and thoraces and abdomens. There was fair agreement between both methods for time points 9 -15 days post-infection (κ = 0.312, 95% CI: 0.230 – 0.394). Conclusion: The COX-I PCR is a highly sensitive, robust method for detecting Plasmodium DNA in mosquitoes, but its limited Plasmodium life-stage specificity cannot be overcome by bisection of the head and thorax from the abdomen prior to PCR. Thus, the COX-I PCR is a poor candidate for identifying infectious mosquitoes.

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Comparison of infectivity of Plasmodium vivax to wild-caught and laboratory-adapted (colonized) Anopheles arabiensis mosquitoes in Ethiopia

Cited by 8 publications

References 57 publications

Optimization of Plasmodium vivax sporozoite production from Anopheles stephensi in South West India

Optimization of Plasmodium vivax sporozoite production from Anopheles stephensi in South West India

A comparison of PCR and ELISA methods to detect different stages of Plasmodium vivax in Anopheles arabiensis

A Comparison of PCR and ELISA Methods to Detect Different Stages of Plasmodium Vivax in Anopheles Arabiensis.

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