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Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir, Myodes glareolus.

Salvador AR, Guivier E, Xuéreb A, Chaval Y, Cadet P, Poulle ML, Sironen T, Voutilainen L, Henttonen H, Cosson JF, Charbonnel N - BMC Microbiol. (2011)

Bottom Line: More specifically, PUUV infection was positively associated with the presence of Heligmosomum mixtum, and in a lesser extent, Aonchotheca muris-sylvatici.It was significantly lower in voles coinfected with A. muris-sylvatici, reflecting the influence of age on these latter infections.Further experimental analyses and long-term individual surveys are now required to confirm these correlative results, and to ascertain the causal links between helminth and PUUV infection risks.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitaries, Facultat de Farmacia, Universitat de Barcelona, Barcelona, Spain.

ABSTRACT

Background: Puumala virus, the agent of nephropathia epidemica (NE), is the most prevalent hantavirus in Europe. The risk for human infection seems to be strongly correlated with the prevalence of Puumala virus (PUUV) in populations of its reservoir host species, the bank vole Myodes glareolus. In humans, the infection risks of major viral diseases are affected by the presence of helminth infections. We therefore proposed to analyse the influence of both helminth community and landscape on the prevalence of PUUV among bank vole populations in the Ardennes, a PUUV endemic area in France.

Results: Among the 313 voles analysed, 37 had anti-PUUV antibodies. Twelve gastro-intestinal helminth species were recorded among all voles sampled. We showed that PUUV seroprevalence strongly increased with age or sexual maturity, especially in the northern forests (massif des Ardennes). The helminth community structure significantly differed between this part and the woods or hedgerows of the southern cretes pre-ardennaises. Using PUUV RNA quantification, we identified significant coinfections between PUUV and gastro-intestinal helminths in the northern forests only. More specifically, PUUV infection was positively associated with the presence of Heligmosomum mixtum, and in a lesser extent, Aonchotheca muris-sylvatici. The viral load of PUUV infected individuals tended to be higher in voles coinfected with H. mixtum. It was significantly lower in voles coinfected with A. muris-sylvatici, reflecting the influence of age on these latter infections.

Conclusions: This is the first study to emphasize hantavirus--helminth coinfections in natural populations. It also highlights the importance to consider landscape when searching for such associations. We have shown that landscape characteristics strongly influence helminth community structure as well as PUUV distribution. False associations might therefore be evidenced if geographic patterns of helminths or PUUV repartition are not previously identified. Moreover, our work revealed that interactions between helminths and landscape enhance/deplete the occurrence of coinfections between PUUV and H. mixtum or A. muris-sylvatici. Further experimental analyses and long-term individual surveys are now required to confirm these correlative results, and to ascertain the causal links between helminth and PUUV infection risks.

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Correspondence analysis of the helminth community structure. a) Factorial plan (F1 × F2) showing the relationships between the helminth species. b) Factorial plan of the landscape according to its effect on the helminth community. The grey circles represent the gravity centres of the three landscapes considered, forest (F), wood (W) and hedge network (H). The lines show the variation within each site. c) Schematic representation of the site map based on helminth community characteristics. Sites represented with circles have above average F1 factorial values, whereas sites represented with squares have below-average F1 factorial values. Hedge networks are indicated with black dashed lines. Circle or square sizes are proportional to the distance of the value above or below the average value.
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Figure 3: Correspondence analysis of the helminth community structure. a) Factorial plan (F1 × F2) showing the relationships between the helminth species. b) Factorial plan of the landscape according to its effect on the helminth community. The grey circles represent the gravity centres of the three landscapes considered, forest (F), wood (W) and hedge network (H). The lines show the variation within each site. c) Schematic representation of the site map based on helminth community characteristics. Sites represented with circles have above average F1 factorial values, whereas sites represented with squares have below-average F1 factorial values. Hedge networks are indicated with black dashed lines. Circle or square sizes are proportional to the distance of the value above or below the average value.

Mentions: Three helminth species, namely P. omphalodes, T. crassiceps and A. annulosa, were too rare to be included in the multivariate analysis of the community structure. The first two factors (named hereafter F1 and F2) of the CA performed on the nine other helminth species described 30.08% of the variability. T. arvicolae, M. muris and A. muris-sylvatici had the highest correlations with the negative part of F1 (respective absolute contributions in 1/10000: 768, 752 and 442). M. muris and A. muris-sylvatici were also strongly correlated with the negative part of F2 (respective absolute contributions in 1/10000: 3733 and 2535). T. taeniaeformis was correlated with the positive values of F1 (absolute contributions in 1/10000: 7651) and S. petrusewiczi with the positive values of F2 (absolute contributions in 1/10000: 1392) (Figure 3a).


Concomitant influence of helminth infection and landscape on the distribution of Puumala hantavirus in its reservoir, Myodes glareolus.

Salvador AR, Guivier E, Xuéreb A, Chaval Y, Cadet P, Poulle ML, Sironen T, Voutilainen L, Henttonen H, Cosson JF, Charbonnel N - BMC Microbiol. (2011)

Correspondence analysis of the helminth community structure. a) Factorial plan (F1 × F2) showing the relationships between the helminth species. b) Factorial plan of the landscape according to its effect on the helminth community. The grey circles represent the gravity centres of the three landscapes considered, forest (F), wood (W) and hedge network (H). The lines show the variation within each site. c) Schematic representation of the site map based on helminth community characteristics. Sites represented with circles have above average F1 factorial values, whereas sites represented with squares have below-average F1 factorial values. Hedge networks are indicated with black dashed lines. Circle or square sizes are proportional to the distance of the value above or below the average value.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3040693&req=5

Figure 3: Correspondence analysis of the helminth community structure. a) Factorial plan (F1 × F2) showing the relationships between the helminth species. b) Factorial plan of the landscape according to its effect on the helminth community. The grey circles represent the gravity centres of the three landscapes considered, forest (F), wood (W) and hedge network (H). The lines show the variation within each site. c) Schematic representation of the site map based on helminth community characteristics. Sites represented with circles have above average F1 factorial values, whereas sites represented with squares have below-average F1 factorial values. Hedge networks are indicated with black dashed lines. Circle or square sizes are proportional to the distance of the value above or below the average value.
Mentions: Three helminth species, namely P. omphalodes, T. crassiceps and A. annulosa, were too rare to be included in the multivariate analysis of the community structure. The first two factors (named hereafter F1 and F2) of the CA performed on the nine other helminth species described 30.08% of the variability. T. arvicolae, M. muris and A. muris-sylvatici had the highest correlations with the negative part of F1 (respective absolute contributions in 1/10000: 768, 752 and 442). M. muris and A. muris-sylvatici were also strongly correlated with the negative part of F2 (respective absolute contributions in 1/10000: 3733 and 2535). T. taeniaeformis was correlated with the positive values of F1 (absolute contributions in 1/10000: 7651) and S. petrusewiczi with the positive values of F2 (absolute contributions in 1/10000: 1392) (Figure 3a).

Bottom Line: More specifically, PUUV infection was positively associated with the presence of Heligmosomum mixtum, and in a lesser extent, Aonchotheca muris-sylvatici.It was significantly lower in voles coinfected with A. muris-sylvatici, reflecting the influence of age on these latter infections.Further experimental analyses and long-term individual surveys are now required to confirm these correlative results, and to ascertain the causal links between helminth and PUUV infection risks.

View Article: PubMed Central - HTML - PubMed

Affiliation: Laboratori de Parasitologia, Departament de Microbiologia i Parasitologia Sanitaries, Facultat de Farmacia, Universitat de Barcelona, Barcelona, Spain.

ABSTRACT

Background: Puumala virus, the agent of nephropathia epidemica (NE), is the most prevalent hantavirus in Europe. The risk for human infection seems to be strongly correlated with the prevalence of Puumala virus (PUUV) in populations of its reservoir host species, the bank vole Myodes glareolus. In humans, the infection risks of major viral diseases are affected by the presence of helminth infections. We therefore proposed to analyse the influence of both helminth community and landscape on the prevalence of PUUV among bank vole populations in the Ardennes, a PUUV endemic area in France.

Results: Among the 313 voles analysed, 37 had anti-PUUV antibodies. Twelve gastro-intestinal helminth species were recorded among all voles sampled. We showed that PUUV seroprevalence strongly increased with age or sexual maturity, especially in the northern forests (massif des Ardennes). The helminth community structure significantly differed between this part and the woods or hedgerows of the southern cretes pre-ardennaises. Using PUUV RNA quantification, we identified significant coinfections between PUUV and gastro-intestinal helminths in the northern forests only. More specifically, PUUV infection was positively associated with the presence of Heligmosomum mixtum, and in a lesser extent, Aonchotheca muris-sylvatici. The viral load of PUUV infected individuals tended to be higher in voles coinfected with H. mixtum. It was significantly lower in voles coinfected with A. muris-sylvatici, reflecting the influence of age on these latter infections.

Conclusions: This is the first study to emphasize hantavirus--helminth coinfections in natural populations. It also highlights the importance to consider landscape when searching for such associations. We have shown that landscape characteristics strongly influence helminth community structure as well as PUUV distribution. False associations might therefore be evidenced if geographic patterns of helminths or PUUV repartition are not previously identified. Moreover, our work revealed that interactions between helminths and landscape enhance/deplete the occurrence of coinfections between PUUV and H. mixtum or A. muris-sylvatici. Further experimental analyses and long-term individual surveys are now required to confirm these correlative results, and to ascertain the causal links between helminth and PUUV infection risks.

Show MeSH
Related in: MedlinePlus