Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia

Abstract Background Plasmodium knowlesi has become a major public health concern in Sabah, Malaysian Borneo, where it is now the only cause of indigenous malaria. The importance of P. knowlesi has spurred on a series of studies on this parasite, as well as on the biology and ecology of its principal...

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Main Authors: Tock H. Chua, Benny Obrain Manin, Kimberly Fornace
Format: Article
Language:English
Published: BMC 2022-11-01
Series:Parasites & Vectors
Subjects:
Online Access:https://doi.org/10.1186/s13071-022-05552-9
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author Tock H. Chua
Benny Obrain Manin
Kimberly Fornace
author_facet Tock H. Chua
Benny Obrain Manin
Kimberly Fornace
author_sort Tock H. Chua
collection DOAJ
description Abstract Background Plasmodium knowlesi has become a major public health concern in Sabah, Malaysian Borneo, where it is now the only cause of indigenous malaria. The importance of P. knowlesi has spurred on a series of studies on this parasite, as well as on the biology and ecology of its principal vector, Anopheles balabacensis. However, there remain critical knowledge gaps on the biology of An. balabacensis, such as life history data and life table parameters. To fill these gaps, we conducted a life table study of An. balabacensis in the laboratory. Characterising vector life cycles and survival rates can inform more accurate estimations of the serial interval, the time between two linked cases, which is crucial to understanding and monitoring potentially changing transmission patterns. Methods Individuals of An. balabacensis were collected in the field in Ranau district, Sabah to establish a laboratory colony. Induced mating was used, and the life history parameters of the progeny were recorded. The age-stage, two-sex life table approach was used in the analysis. The culture conditions in the laboratory were 9 h light:15 h dark, mean temperature 25.7 °C ± 0.05 and relative humidity 75.8% ± 0.31. Results The eggs hatched within 2 days, and the larval stage lasted for 10.5 days in total, with duration of instar stages I, II, III and IV of 2.3, 3.7, 2.3, 2.2 days, respectively. The maximum total fecundity was 729 for one particular female, while the maximum female age-specific mean fecundity (m x ) was 142 at age 59 days. The gross reproductive rate or number of offspring per individual was about 102. On average, each female laid 1.81 ± 0.19 (range 1–7) batches of eggs, with 63% of the females producing only one batch; only one female laid six batches, while one other laid seven. Each batch comprised 159 ± 17.1 eggs (range 5–224) and the female ratio of offspring was 0.28 ± 0.06. The intrinsic rate of increase, finite rate of increase, net reproductive rate, mean generation time and doubling time were, respectively, 0.12 ± 0.01 day−1, 1.12 ± 0.01 day−1, 46.2 ± 14.97, 33.02 ± 1.85 and 5.97 days. Conclusions Both the net reproductive rate and intrinsic rate of increase of An. balabacensis are lower than those of other species in published studies. Our results can be used to improve models of P. knowlesi transmission and to set a baseline for assessing the impacts of environmental change on malaria dynamics. Furthermore, incorporating these population parameters of An. balabacensis into spatial and temporal models on the transmission of P. knowlesi would provide better insight and increase the accuracy of epidemiological forecasting. Graphical Abstract
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spelling doaj.art-374791e86a084c169bb4e3b6382ac9242022-12-22T04:36:43ZengBMCParasites & Vectors1756-33052022-11-011511910.1186/s13071-022-05552-9Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, MalaysiaTock H. Chua0Benny Obrain Manin1Kimberly Fornace2Department of Pathology and Microbiology, Faculty of Medicine and Health Sciences, Universiti Malaysia SabahDepartment of Pathology and Microbiology, Faculty of Medicine and Health Sciences, Universiti Malaysia SabahSchool of Biodiversity, One Health and Veterinary Medicine, University of GlasgowAbstract Background Plasmodium knowlesi has become a major public health concern in Sabah, Malaysian Borneo, where it is now the only cause of indigenous malaria. The importance of P. knowlesi has spurred on a series of studies on this parasite, as well as on the biology and ecology of its principal vector, Anopheles balabacensis. However, there remain critical knowledge gaps on the biology of An. balabacensis, such as life history data and life table parameters. To fill these gaps, we conducted a life table study of An. balabacensis in the laboratory. Characterising vector life cycles and survival rates can inform more accurate estimations of the serial interval, the time between two linked cases, which is crucial to understanding and monitoring potentially changing transmission patterns. Methods Individuals of An. balabacensis were collected in the field in Ranau district, Sabah to establish a laboratory colony. Induced mating was used, and the life history parameters of the progeny were recorded. The age-stage, two-sex life table approach was used in the analysis. The culture conditions in the laboratory were 9 h light:15 h dark, mean temperature 25.7 °C ± 0.05 and relative humidity 75.8% ± 0.31. Results The eggs hatched within 2 days, and the larval stage lasted for 10.5 days in total, with duration of instar stages I, II, III and IV of 2.3, 3.7, 2.3, 2.2 days, respectively. The maximum total fecundity was 729 for one particular female, while the maximum female age-specific mean fecundity (m x ) was 142 at age 59 days. The gross reproductive rate or number of offspring per individual was about 102. On average, each female laid 1.81 ± 0.19 (range 1–7) batches of eggs, with 63% of the females producing only one batch; only one female laid six batches, while one other laid seven. Each batch comprised 159 ± 17.1 eggs (range 5–224) and the female ratio of offspring was 0.28 ± 0.06. The intrinsic rate of increase, finite rate of increase, net reproductive rate, mean generation time and doubling time were, respectively, 0.12 ± 0.01 day−1, 1.12 ± 0.01 day−1, 46.2 ± 14.97, 33.02 ± 1.85 and 5.97 days. Conclusions Both the net reproductive rate and intrinsic rate of increase of An. balabacensis are lower than those of other species in published studies. Our results can be used to improve models of P. knowlesi transmission and to set a baseline for assessing the impacts of environmental change on malaria dynamics. Furthermore, incorporating these population parameters of An. balabacensis into spatial and temporal models on the transmission of P. knowlesi would provide better insight and increase the accuracy of epidemiological forecasting. Graphical Abstracthttps://doi.org/10.1186/s13071-022-05552-9Age-stage two-sex life tableAnopheles balabacensisPlasmodium knowlesi
spellingShingle Tock H. Chua
Benny Obrain Manin
Kimberly Fornace
Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia
Parasites & Vectors
Age-stage two-sex life table
Anopheles balabacensis
Plasmodium knowlesi
title Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia
title_full Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia
title_fullStr Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia
title_full_unstemmed Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia
title_short Life table analysis of Anopheles balabacensis, the primary vector of Plasmodium knowlesi in Sabah, Malaysia
title_sort life table analysis of anopheles balabacensis the primary vector of plasmodium knowlesi in sabah malaysia
topic Age-stage two-sex life table
Anopheles balabacensis
Plasmodium knowlesi
url https://doi.org/10.1186/s13071-022-05552-9
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AT kimberlyfornace lifetableanalysisofanophelesbalabacensistheprimaryvectorofplasmodiumknowlesiinsabahmalaysia