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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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Comparison of PUUV viral load in bank voles infected with H. mixtum or A. muris-sylvatici and in those not infected by these helminth species. "0" indicates bank voles that are not infected with H. mixtum (resp. A. muris-sylvatici) and "1" indicates bank voles that are infected with at least 1 H. mixtum helminth (resp. A. muris-sylvatici). Only samples from the massif des Ardennes are considered. N indicates the sampling size for each category.
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Figure 5: Comparison of PUUV viral load in bank voles infected with H. mixtum or A. muris-sylvatici and in those not infected by these helminth species. "0" indicates bank voles that are not infected with H. mixtum (resp. A. muris-sylvatici) and "1" indicates bank voles that are infected with at least 1 H. mixtum helminth (resp. A. muris-sylvatici). Only samples from the massif des Ardennes are considered. N indicates the sampling size for each category.

Mentions: The viral load in infected individuals tended to be higher in voles coinfected with H. mixtum than in voles that did not carry any infection with this helminth species (F1,19 = 0.992, p = 0.331, Figure 5). Although the number of H. mixtum worms per vole had been counted, we could not analyse the relationship between PUUV viral load and H. mixtum burden. Indeed, among the eight voles that were coinfected by PUUV and H. mixtum, only one had more than one worm (this individual carried six H. mixtum worms), the seven other voles had only one H. mixtum worm. Surprisingly, voles coinfected with A. muris-sylvatici exhibited significantly lower viral load of PUUV than voles non-infected with this helminth species (F1,19 = 13.551, p = 0.001, Figure 5). As this negative relationship could be mediated by a delay between PUUV and A. muris-sylvatici infection, we analysed roughly the influence of vole age (reflected by vole mass) on these infections. We confirmed that voles coinfected with PUUV and A. muris-sylvatici were significantly heavier (thus probably older) than those infected with A. muris-sylvatici only, with PUUV only or non infected either with PUUV or A. muris-sylvatici (F3,96 = 7.279, p = 2 × 10-4).


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)

Comparison of PUUV viral load in bank voles infected with H. mixtum or A. muris-sylvatici and in those not infected by these helminth species. "0" indicates bank voles that are not infected with H. mixtum (resp. A. muris-sylvatici) and "1" indicates bank voles that are infected with at least 1 H. mixtum helminth (resp. A. muris-sylvatici). Only samples from the massif des Ardennes are considered. N indicates the sampling size for each category.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 5: Comparison of PUUV viral load in bank voles infected with H. mixtum or A. muris-sylvatici and in those not infected by these helminth species. "0" indicates bank voles that are not infected with H. mixtum (resp. A. muris-sylvatici) and "1" indicates bank voles that are infected with at least 1 H. mixtum helminth (resp. A. muris-sylvatici). Only samples from the massif des Ardennes are considered. N indicates the sampling size for each category.
Mentions: The viral load in infected individuals tended to be higher in voles coinfected with H. mixtum than in voles that did not carry any infection with this helminth species (F1,19 = 0.992, p = 0.331, Figure 5). Although the number of H. mixtum worms per vole had been counted, we could not analyse the relationship between PUUV viral load and H. mixtum burden. Indeed, among the eight voles that were coinfected by PUUV and H. mixtum, only one had more than one worm (this individual carried six H. mixtum worms), the seven other voles had only one H. mixtum worm. Surprisingly, voles coinfected with A. muris-sylvatici exhibited significantly lower viral load of PUUV than voles non-infected with this helminth species (F1,19 = 13.551, p = 0.001, Figure 5). As this negative relationship could be mediated by a delay between PUUV and A. muris-sylvatici infection, we analysed roughly the influence of vole age (reflected by vole mass) on these infections. We confirmed that voles coinfected with PUUV and A. muris-sylvatici were significantly heavier (thus probably older) than those infected with A. muris-sylvatici only, with PUUV only or non infected either with PUUV or A. muris-sylvatici (F3,96 = 7.279, p = 2 × 10-4).

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