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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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Results of the discriminant analysis performed on the helminth community of PUUV-seronegative and PUUV-seropositive bank voles sampled in the northern sites of the transect. a) Sample scores of the discriminant function for PUUV-seronegative and PUUV-seropositive bank voles. The symbols (-) and (+) represent the group averages of these two classes of individuals. b) Coefficient of the discriminant scores on this axis.
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Figure 4: Results of the discriminant analysis performed on the helminth community of PUUV-seronegative and PUUV-seropositive bank voles sampled in the northern sites of the transect. a) Sample scores of the discriminant function for PUUV-seronegative and PUUV-seropositive bank voles. The symbols (-) and (+) represent the group averages of these two classes of individuals. b) Coefficient of the discriminant scores on this axis.

Mentions: We therefore tested whether the helminth community varied between PUUV infected and non-infected bank voles. We analysed data independently for the Northern and the Southern parts of the transect. The discriminant analyses revealed significant differences when considering the northern area only (Massif des Ardennes, p = 0.005; Crêtes pré-ardennaises, p = 0.551, Figure 4a). The main discriminant species variable was the presence of H. mixtum, and in a lesser extent of A. muris-sylvatici (Figure 4b). Bank voles exhibiting anti-PUUV antibodies were more likely to be infected with these nematode species than bank voles with no anti-PUUV antibodies (H. mixtum: RR = 5.91, Fisher exact test: p = 0.002; A. muris-sylvatici: RR = 2.34, Fisher exact test, p = 0.125). We obtained similar results when comparing PUUV infected (with anti-PUUV antibodies and PUUV RNA) and non infected (without anti-PUUV antibodies or PUUV RNA) bank voles (H. mixtum: RR = 4.74, Fisher exact test: p = 0.007; A. muris-sylvatici: RR = 2.53, Fisher exact test, p = 0.102).


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)

Results of the discriminant analysis performed on the helminth community of PUUV-seronegative and PUUV-seropositive bank voles sampled in the northern sites of the transect. a) Sample scores of the discriminant function for PUUV-seronegative and PUUV-seropositive bank voles. The symbols (-) and (+) represent the group averages of these two classes of individuals. b) Coefficient of the discriminant scores on this axis.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 4: Results of the discriminant analysis performed on the helminth community of PUUV-seronegative and PUUV-seropositive bank voles sampled in the northern sites of the transect. a) Sample scores of the discriminant function for PUUV-seronegative and PUUV-seropositive bank voles. The symbols (-) and (+) represent the group averages of these two classes of individuals. b) Coefficient of the discriminant scores on this axis.
Mentions: We therefore tested whether the helminth community varied between PUUV infected and non-infected bank voles. We analysed data independently for the Northern and the Southern parts of the transect. The discriminant analyses revealed significant differences when considering the northern area only (Massif des Ardennes, p = 0.005; Crêtes pré-ardennaises, p = 0.551, Figure 4a). The main discriminant species variable was the presence of H. mixtum, and in a lesser extent of A. muris-sylvatici (Figure 4b). Bank voles exhibiting anti-PUUV antibodies were more likely to be infected with these nematode species than bank voles with no anti-PUUV antibodies (H. mixtum: RR = 5.91, Fisher exact test: p = 0.002; A. muris-sylvatici: RR = 2.34, Fisher exact test, p = 0.125). We obtained similar results when comparing PUUV infected (with anti-PUUV antibodies and PUUV RNA) and non infected (without anti-PUUV antibodies or PUUV RNA) bank voles (H. mixtum: RR = 4.74, Fisher exact test: p = 0.007; A. muris-sylvatici: RR = 2.53, Fisher exact test, p = 0.102).

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