Evolutionary epidemiology of schistosomiasis: linking parasite genetics with disease phenotype in humans

Tine Huyse; Nele A.M. Boon; Frederik Van den Broeck; Moustapha Mbow; Anurag Chaturvedi; Lynn Meurs; Filip A.M. Volckaert; Katja Polman

doi:10.1016/j.ijpara.2017.07.010

Evolutionary epidemiology of schistosomiasis: linking parasite genetics with disease phenotype in humans

Tine Huyse^*, Nele A.M. Boon, Frederik Van den Broeck, Moustapha Mbow, Anurag Chaturvedi, Lynn Meurs, Filip A.M. Volckaert, Katja Polman

^*Corresponding author for this work

Research output: Contribution to Journal › Article › Academic › peer-review

Abstract

Here we assess the role of parasite genetic variation in host disease phenotype in human schistosomiasis by implementing concepts and techniques from environmental association analysis in evolutionary epidemiology. Schistosomiasis is a tropical disease that affects more than 200 million people worldwide and is caused by parasitic flatworms belonging to the genus Schistosoma. While the role of host genetics has been extensively studied and demonstrated, nothing is yet known on the contribution of parasite genetic variation to host disease phenotype in human schistosomiasis. In this study microsatellite genotypes of 1561 Schistosoma mansoni larvae collected from 44 human hosts in Senegal were linked to host characteristics such as age, gender, infection intensity, liver and bladder morbidity by means of multivariate regression methods (on each parasite locus separately). This revealed a highly significant association between allelic variation at the parasite locus L46951 and host infection intensity and bladder morbidity. Locus L46951 is located in the 3′ untranslated region of the cGMP-dependent protein kinase gene that is expressed in reproductive organs of adult schistosome worms and appears to be linked to egg production. This putative link between parasite genetic variation and schistosomiasis disease phenotype sets the stage for further functional research.

Original language	English
Pages (from-to)	107-115
Number of pages	9
Journal	International Journal for Parasitology
Volume	48
Issue number	2
DOIs	https://doi.org/10.1016/j.ijpara.2017.07.010
Publication status	Published - 1 Feb 2018
Externally published	Yes

Funding

We thank the field team of Richard Toll, A. Yague, M. Diop, M. Wade and N. Sy for assistance with sample collection and microscopic analysis. We also thank Hanne Dekort and Pascal Hablützel for useful comments on an earlier version of this manuscript and two anonymous referees for providing useful suggestions. Govert van Dam is acknowledged for the CAA measurements. Finally, special thanks to the people in Ndieumeul, Diokhor Tack and Pakh, Senegal, for their kind participation in the study. NB and FVdB benefited from a VLADOC PhD fellowship of the Flemish Interuniversity Council (VLIR-UOS), Belgium. Research was funded with a Research Grant of the Research Foundation—Flanders, Belgium (contract G.0552.10), a Krediet to navorsers (contract 1516913N) to TH and from travel grants awarded by VLIR-UOS to FVDB and NB. Appendix A

Funders	Funder number
Research Foundation—Flanders, Belgium	1516913N, G.0552.10
Vlaamse Interuniversitaire Raad
VLIRUOS

Keywords

cGMP-dependent protein kinase
Disease phenotype
Environmental association analysis
Follistatin
Molecular epidemiology
Parasite fecundity
Schistosoma mansoni

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title = "Evolutionary epidemiology of schistosomiasis: linking parasite genetics with disease phenotype in humans",

abstract = "Here we assess the role of parasite genetic variation in host disease phenotype in human schistosomiasis by implementing concepts and techniques from environmental association analysis in evolutionary epidemiology. Schistosomiasis is a tropical disease that affects more than 200 million people worldwide and is caused by parasitic flatworms belonging to the genus Schistosoma. While the role of host genetics has been extensively studied and demonstrated, nothing is yet known on the contribution of parasite genetic variation to host disease phenotype in human schistosomiasis. In this study microsatellite genotypes of 1561 Schistosoma mansoni larvae collected from 44 human hosts in Senegal were linked to host characteristics such as age, gender, infection intensity, liver and bladder morbidity by means of multivariate regression methods (on each parasite locus separately). This revealed a highly significant association between allelic variation at the parasite locus L46951 and host infection intensity and bladder morbidity. Locus L46951 is located in the 3′ untranslated region of the cGMP-dependent protein kinase gene that is expressed in reproductive organs of adult schistosome worms and appears to be linked to egg production. This putative link between parasite genetic variation and schistosomiasis disease phenotype sets the stage for further functional research.",

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author = "Tine Huyse and Boon, {Nele A.M.} and {Van den Broeck}, Frederik and Moustapha Mbow and Anurag Chaturvedi and Lynn Meurs and Volckaert, {Filip A.M.} and Katja Polman",

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AU - Boon, Nele A.M.

AU - Van den Broeck, Frederik

AU - Mbow, Moustapha

AU - Chaturvedi, Anurag

AU - Meurs, Lynn

AU - Volckaert, Filip A.M.

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AB - Here we assess the role of parasite genetic variation in host disease phenotype in human schistosomiasis by implementing concepts and techniques from environmental association analysis in evolutionary epidemiology. Schistosomiasis is a tropical disease that affects more than 200 million people worldwide and is caused by parasitic flatworms belonging to the genus Schistosoma. While the role of host genetics has been extensively studied and demonstrated, nothing is yet known on the contribution of parasite genetic variation to host disease phenotype in human schistosomiasis. In this study microsatellite genotypes of 1561 Schistosoma mansoni larvae collected from 44 human hosts in Senegal were linked to host characteristics such as age, gender, infection intensity, liver and bladder morbidity by means of multivariate regression methods (on each parasite locus separately). This revealed a highly significant association between allelic variation at the parasite locus L46951 and host infection intensity and bladder morbidity. Locus L46951 is located in the 3′ untranslated region of the cGMP-dependent protein kinase gene that is expressed in reproductive organs of adult schistosome worms and appears to be linked to egg production. This putative link between parasite genetic variation and schistosomiasis disease phenotype sets the stage for further functional research.

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Evolutionary epidemiology of schistosomiasis: linking parasite genetics with disease phenotype in humans

Abstract

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Keywords

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