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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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Sampling localities for M. glareolus in the French Ardennes. Forests and wooded areas are indicated in grey. White circles correspond to forested areas of the Northern massif des Ardennes. White and dashed circles respectively correspond to wooded areas and hedge networks of the Southern crêtes pré-ardennaises. The dashed line indicates the limit between the Northern massif des Ardennes and the Southern crêtes pré-ardennaises. Numbers refer to site codes indicated in Table 1.
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Figure 1: Sampling localities for M. glareolus in the French Ardennes. Forests and wooded areas are indicated in grey. White circles correspond to forested areas of the Northern massif des Ardennes. White and dashed circles respectively correspond to wooded areas and hedge networks of the Southern crêtes pré-ardennaises. The dashed line indicates the limit between the Northern massif des Ardennes and the Southern crêtes pré-ardennaises. Numbers refer to site codes indicated in Table 1.

Mentions: Bank voles were sampled from September to October 2008 as PUUV and helminth prevalence levels are usually higher in autumn, which corresponds to the end of the reproductive season [e.g. among many studies [29,30]]. We used French Agricultural Research Institute (INRA) live traps, fitted out with dormitory boxes and baited with potatoes and sunflower seeds. Nine sampling sites were surveyed along a North - South transect in the French Ardennes. They corresponded to three different landscape configurations: forests, which are found in the northern 'massif des Ardennes' and refer to large wooded areas of several thousand hectares, smaller forest fragments (wooded areas of about 50 km2) and hedge networks surrounding these fragments, which are found in the Southern 'crêtes pré-ardennaises' (Figure 1). Ten 200-m trap-lines composed of 20 traps placed at 10-m intervals were placed within each site. They were checked twice a day during three consecutive nights. The minimum distance between sites was 3.2 km, that is much larger than the dispersal distance of bank voles [estimated to be 500 m in patchy landscapes, [31]].


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)

Sampling localities for M. glareolus in the French Ardennes. Forests and wooded areas are indicated in grey. White circles correspond to forested areas of the Northern massif des Ardennes. White and dashed circles respectively correspond to wooded areas and hedge networks of the Southern crêtes pré-ardennaises. The dashed line indicates the limit between the Northern massif des Ardennes and the Southern crêtes pré-ardennaises. Numbers refer to site codes indicated in Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Sampling localities for M. glareolus in the French Ardennes. Forests and wooded areas are indicated in grey. White circles correspond to forested areas of the Northern massif des Ardennes. White and dashed circles respectively correspond to wooded areas and hedge networks of the Southern crêtes pré-ardennaises. The dashed line indicates the limit between the Northern massif des Ardennes and the Southern crêtes pré-ardennaises. Numbers refer to site codes indicated in Table 1.
Mentions: Bank voles were sampled from September to October 2008 as PUUV and helminth prevalence levels are usually higher in autumn, which corresponds to the end of the reproductive season [e.g. among many studies [29,30]]. We used French Agricultural Research Institute (INRA) live traps, fitted out with dormitory boxes and baited with potatoes and sunflower seeds. Nine sampling sites were surveyed along a North - South transect in the French Ardennes. They corresponded to three different landscape configurations: forests, which are found in the northern 'massif des Ardennes' and refer to large wooded areas of several thousand hectares, smaller forest fragments (wooded areas of about 50 km2) and hedge networks surrounding these fragments, which are found in the Southern 'crêtes pré-ardennaises' (Figure 1). Ten 200-m trap-lines composed of 20 traps placed at 10-m intervals were placed within each site. They were checked twice a day during three consecutive nights. The minimum distance between sites was 3.2 km, that is much larger than the dispersal distance of bank voles [estimated to be 500 m in patchy landscapes, [31]].

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