Abstract:ABSTRACT:Many zoonotic diseases are caused by rodent-borne viruses. Major fluctuations in the transmission of these viruses have been related to large changes in reservoir host population numbers due to external factors. However, the impact of the pathogen itself on the demography of its reservoir host is often overlooked. We investigated the impact of Puumala virus (PUUV) on survival and reproductive maturation probability of its reservoir host, the bank vole (Myodes glareolus). Three years (2004-06) of data … Show more
“…Such complex relationships between parasite infection and host fitness were indeed observed in other rodent-borne diseases. For example, infection of Puumala hantavirus in bank voles ( Myodes glareolus ) was initially assumed to be asymptomatic [51–53] but recent long-term field studies observed negative effects on the survival probability and an equivocal impact on the fecundity of females [36, 54, 55]. An important difference between Old World arenaviruses and hantaviruses, however, is that the latter causes persistent infections in their reservoir hosts [56], while the former infects their hosts mainly acutely [29, 43].…”
BackgroundIn order to optimize net transmission success, parasites are hypothesized to evolve towards causing minimal damage to their reservoir host while obtaining high shedding rates. For many parasite species however this paradigm has not been tested, and conflicting results have been found regarding the effect of arenaviruses on their rodent host species. The rodent Mastomys natalensis is the natural reservoir host of several arenaviruses, including Lassa virus that is known to cause Lassa haemorrhagic fever in humans. Here, we examined the effect of three arenaviruses (Gairo, Morogoro and Lassa virus) on four parameters of wild-caught Mastomys natalensis: body mass, head-body length, sexual maturity and fertility. After correcting for the effect of age, we compared these parameters between arenavirus-positive (arenavirus RNA or antibody) and negative animals using data from different field studies in Guinea (Lassa virus) and Tanzania (Morogoro and Gairo viruses).ResultsAlthough the sample sizes of our studies (1297, 749 and 259 animals respectively) were large enough to statistically detect small differences in body conditions, we did not observe any adverse effects of these viruses on Mastomys natalensis. We did find that sexual maturity was significantly positively related with Lassa virus antibody presence until a certain age, and with Gairo virus antibody presence in general. Gairo virus antibody-positive animals were also significantly heavier and larger than antibody-free animals.ConclusionTogether, these results suggest that the pathogenicity of arenaviruses is not severe in M. natalensis, which is likely to be an adaptation of these viruses to optimize transmission success. They also suggest that sexual behaviour might increase the probability of M. natalensis to become infected with arenaviruses.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2146-0) contains supplementary material, which is available to authorized users.
“…Such complex relationships between parasite infection and host fitness were indeed observed in other rodent-borne diseases. For example, infection of Puumala hantavirus in bank voles ( Myodes glareolus ) was initially assumed to be asymptomatic [51–53] but recent long-term field studies observed negative effects on the survival probability and an equivocal impact on the fecundity of females [36, 54, 55]. An important difference between Old World arenaviruses and hantaviruses, however, is that the latter causes persistent infections in their reservoir hosts [56], while the former infects their hosts mainly acutely [29, 43].…”
BackgroundIn order to optimize net transmission success, parasites are hypothesized to evolve towards causing minimal damage to their reservoir host while obtaining high shedding rates. For many parasite species however this paradigm has not been tested, and conflicting results have been found regarding the effect of arenaviruses on their rodent host species. The rodent Mastomys natalensis is the natural reservoir host of several arenaviruses, including Lassa virus that is known to cause Lassa haemorrhagic fever in humans. Here, we examined the effect of three arenaviruses (Gairo, Morogoro and Lassa virus) on four parameters of wild-caught Mastomys natalensis: body mass, head-body length, sexual maturity and fertility. After correcting for the effect of age, we compared these parameters between arenavirus-positive (arenavirus RNA or antibody) and negative animals using data from different field studies in Guinea (Lassa virus) and Tanzania (Morogoro and Gairo viruses).ResultsAlthough the sample sizes of our studies (1297, 749 and 259 animals respectively) were large enough to statistically detect small differences in body conditions, we did not observe any adverse effects of these viruses on Mastomys natalensis. We did find that sexual maturity was significantly positively related with Lassa virus antibody presence until a certain age, and with Gairo virus antibody presence in general. Gairo virus antibody-positive animals were also significantly heavier and larger than antibody-free animals.ConclusionTogether, these results suggest that the pathogenicity of arenaviruses is not severe in M. natalensis, which is likely to be an adaptation of these viruses to optimize transmission success. They also suggest that sexual behaviour might increase the probability of M. natalensis to become infected with arenaviruses.Electronic supplementary materialThe online version of this article (doi:10.1186/s13071-017-2146-0) contains supplementary material, which is available to authorized users.
“…Selection acting on Tnf promoter could therefore be linked to PUUV, either indirectly, or potentially directly. Indeed, several ongoing studies are providing evidence of negative effects of PUUV on different components of vole fitness, including survival [28,29,71] . …”
Section: Impact Of Immunity-related Genes On the Risk Of Hantavirumentioning
confidence: 99%
“…In rodents, which are the reservoirs of pathogenic hantaviruses, infection is persistent [26,27] and mainly asymptomatic but see [28,29,30]. Nevertheless rodents differ in their probability of being infected with their associated hantavirus e.g., [31].…”
We reviewed the associations of immunity-related genes with susceptibility of humans and rodents to hantaviruses, and with severity of hantaviral diseases in humans. Several class I and class II HLA haplotypes were linked with severe or benign hantavirus infections, and these haplotypes varied among localities and hantaviruses. The polymorphism of other immunity-related genes including the C4A gene and a high-producing genotype of TNF gene associated with severe PUUV infection. Additional genes that may contribute to disease or to PUUV infection severity include non-carriage of the interleukin-1 receptor antagonist (IL-1RA) allele 2 and IL-1β (-511) allele 2, polymorphisms of plasminogen activator inhibitor (PAI-1) and platelet GP1a. In addition, immunogenetic studies have been conducted to identify mechanisms that could be linked with the persistence/clearance of hantaviruses in reservoirs. Persistence was associated during experimental infections with an upregulation of anti-inflammatory responses. Using natural rodent population samples, polymorphisms and/or expression levels of several genes have been analyzed. These genes were selected based on the literature of rodent or human/hantavirus interactions (some Mhc class II genes, Tnf promoter, and genes encoding the proteins TLR4, TLR7, Mx2 and β3 integrin). The comparison of genetic differentiation estimated between bank vole populations sampled over Europe, at neutral and candidate genes, has allowed to evidence signatures of selection for Tnf, Mx2 and the Drb Mhc class II genes. Altogether, these results corroborated the hypothesis of an evolution of tolerance strategies in rodents. We finally discuss the importance of these results from the medical and epidemiological perspectives.
“…Inhalation of aerosolized rodent excreta is also considered the main route of infection to humans (Hjelle & Glass, 2000;Vapalahti et al, 2010). No apparent symptoms have been reported in rodent hosts due to hantavirus infection, but it may impair host survival in nature (Kallio et al, 2007;Luis et al, 2012;Tersago et al, 2012). The hantavirus infection induces a life-long antibody response where IgG appears in the bloodstream 2 to 3 weeks after infection, but viral RNA and/or infectious virus is found in various tissues, especially in the lungs of chronically infected animals (Botten et al, 2003;Hardestam et al, 2008;Meyer & Schmaljohn, 2000;Schountz et al, 2012).…”
The knowledge of viral shedding patterns and viraemia in the reservoir host species is a key factor in assessing the human risk of zoonotic viruses. The shedding of hantaviruses (family Bunyaviridae) by their host rodents has widely been studied experimentally, but rarely in natural settings. Here we present the dynamics of Puumala hantavirus (PUUV) shedding and viraemia in naturally infected wild bank voles (Myodes glareolus). In a monthly capture-mark-recapture study, we analysed 18 bank voles for the presence and relative quantity of PUUV RNA in the excreta and blood from 2 months before up to 8 months after seroconversion. The proportion of animals shedding PUUV RNA in saliva, urine and faeces peaked during the first month after seroconversion, but continued throughout the study period with only a slight decline. The quantity of shed PUUV in reverse transcription quantitative PCR (RT-qPCR) positive excreta was constant over time. In blood, PUUV RNA was present for up to 7 months but both the probability of viraemia and the virus load declined with time. Our findings contradict the current view of a decline in virus shedding after the acute phase and a short viraemic period in hantavirus infection -an assumption widely adopted in current epidemiological models. We suggest the life-long shedding as a means of hantaviruses to survive over host population bottlenecks, and to disperse in fragmented habitats where local host and/or virus populations face temporary extinctions. Our results indicate that the kinetics of pathogens in wild hosts may differ considerably from those observed in laboratory settings.
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