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Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field.

ABSTRACT: The populations of many pathogen species consist of a collection of common and rare strains but the factors underlying this strain-specific variation in frequency are often unknown. Understanding frequency variation among strains is particularly challenging for vector-borne pathogens where the strain-specific fitness depends on the performance in both the vertebrate host and the arthropod vector. Two sympatric multiple-strain tick-borne pathogens, Borrelia afzelii and B. garinii, that use the same tick vector, Ixodes ricinus, but different vertebrate hosts were studied. 454-sequencing of the polymorphic ospC gene was used to characterize the community of Borrelia strains in a local population of I. ricinus ticks over a period of 11 years. Estimates of the reproduction number (R0), a measure of fitness, were obtained for six strains of B. afzelii from a previous laboratory study. There was substantial variation in prevalence among strains and some strains were consistently common whereas other strains were consistently rare. In B. afzelii, the strain-specific estimates of R0 in laboratory mice explained over 70% of the variation in the prevalences of the strains in our local population of ticks. Our study shows that laboratory estimates of fitness can predict the community structure of multiple-strain pathogens in the field.

SUBMITTER: Durand J

PROVIDER: S-EPMC5431797 | biostudies-literature | 2017 May

REPOSITORIES: biostudies-literature

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Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field.

Durand Jonas J Jacquet Maxime M Rais Olivier O Gern Lise L Voordouw Maarten J MJ

Scientific reports 20170512 1

The populations of many pathogen species consist of a collection of common and rare strains but the factors underlying this strain-specific variation in frequency are often unknown. Understanding frequency variation among strains is particularly challenging for vector-borne pathogens where the strain-specific fitness depends on the performance in both the vertebrate host and the arthropod vector. Two sympatric multiple-strain tick-borne pathogens, Borrelia afzelii and B. garinii, that use the sa ...[more]

PMID: 28500292

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Project description:BACKGROUND:The required efforts, feasibility and predicted success of an intervention strategy against an infectious disease are partially determined by its basic reproduction number, R0. In its simplest form R0 can be understood as the product of the infectious period, the number of infectious contacts and the per-contact transmission probability, which in the case of vector-transmitted diseases necessarily extend to the vector stages. As vectors do not usually recover from infection, they remain infectious for life, which places high significance on the vector's life expectancy. Current methods for estimating the R0 for a vector-borne disease are mostly derived from compartmental modelling frameworks assuming constant vector mortality rates. We hypothesised that some of the assumptions underlying these models can lead to unrealistic high vector life expectancies with important repercussions for R0 estimates. METHODOLOGY AND PRINCIPAL FINDINGS:Here we used a stochastic, individual-based model which allowed us to directly measure the number of secondary infections arising from one index case under different assumptions about vector mortality. Our results confirm that formulas based on age-independent mortality rates can overestimate R0 by nearly 100% compared to our own estimate derived from first principles. We further provide a correction factor that can be used with a standard R0 formula and adjusts for the discrepancies due to erroneous vector age distributions. CONCLUSION:Vector mortality rates play a crucial role for the success and general epidemiology of vector-transmitted diseases. Many modelling efforts intrinsically assume these to be age-independent, which, as clearly demonstrated here, can lead to severe over-estimation of the disease's reproduction number. Our results thus re-emphasise the importance of obtaining field-relevant and species-dependent vector mortality rates, which in turn would facilitate more realistic intervention impact predictions.

Project description:After a request from the European Commission, EFSA's Panel on Animal Health and Welfare summarised the main characteristics of 36 vector-borne diseases (VBDs) in https://efsa.maps.arcgis.com/apps/PublicGallery/index.html?appid=dfbeac92aea944599ed1eb754aa5e6d1. The risk of introduction in the EU through movement of livestock or pets was assessed for each of the 36 VBDs individually, using a semiquantitative Method to INTegrate all relevant RISK aspects (MINTRISK model), which was further modified to a European scale into the http://www3.lei.wur.nl/mintrisk/ModelMgt.aspx. Only eight of the 36 VBD-agents had an overall rate of introduction in the EU (being the combination of the rate of entry, vector transmission and establishment) which was estimated to be above 0.001 introductions per year. These were Crimean-Congo haemorrhagic fever virus, bluetongue virus, West Nile virus, Schmallenberg virus, Hepatozoon canis, Leishmania infantum, Bunyamwera virus and Highlands J. virus. For these eight diseases, the annual extent of spread was assessed, assuming the implementation of available, authorised prevention and control measures in the EU. Further, the probability of overwintering was assessed, as well as the possible impact of the VBDs on public health, animal health and farm production. For the other 28 VBD-agents for which the rate of introduction was estimated to be very low, no further assessments were made. Due to the uncertainty related to some parameters used for the risk assessment or the instable or unpredictability disease situation in some of the source regions, it is recommended to update the assessment when new information becomes available. Since this risk assessment was carried out for large regions in the EU for many VBD-agents, it should be considered as a first screening. If a more detailed risk assessment for a specific VBD is wished for on a national or subnational level, the EFSA-VBD-RISK-model is freely available for this purpose.

Project description:Purpose: The aim was, in the frame of an anti-vector strategy, to use such genes to control Human and/or animal trypanosomiasis. The present objective was to verify whether field tsetse fly gene expression was modified in response to natural infection with trypanosomes as it was when insectary-raised flies were experimentally infected. Method: mRNA from 10 samples of Glossina palpalis (5 non-infected and 5 infected by Trypanosoma congolense s.l.) were sequenced on a high-output flow cell (400M clusters) using the NextSeq® 500/550 High Output v2 150 cycles kit (Illumina), in paired-end 75/75nt mode. The sequenced reads that passed quality filter were mapped onto the genome with the local alignment algorithm subread-align (Liao et al., 2013). Differential analysis was done with the SARTools R package (Varet et al., 2016), which runs separately DESeq2 (Love et al., 2014) and egdeR (Robinson et al., 2010). We identified orthologs between Glossina and Drosophila based on the identification of bidirectional best hits (BBH) using blastp (Altschul et al., 1997), and then made functional enrichment and pathway mapping of these DEGs. Results: Using the RNA-seq approach, differentially expressed genes (DEGs) have been identified in infected versus non-infected tsetse flies, including down-regulated genes and up-regulated genes. Some of the genes, whether down- or up-regulated, were very highly differentially expressed. Down-regulated genes were mainly involved in transcription/translation processes, while up-regulated encoded genes governing amino acid and nucleotide biosynthesis pathways. The data on the molecular cross-talk between the host and the parasite (and the fly microbiome that is always present) recorded when using an experimental biological model have its counterpart in field flies which in turn validates the use of experimental host/parasite couples. Conclusion: This study is the first evaluation of transcriptomic mechanisms related to infection in field tsetse flies. This opens up prospects for vector-based control strategies, and more precisely the blocking of transmission.

Dataset Information

Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field.

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Fitness estimates from experimental infections predict the long-term strain structure of a vector-borne pathogen in the field.

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