Drivers of Echinococcus multilocularis Transmission in China: Small Mammal Diversity,Landscape or Climate?

Background

Human alveolar echinococcocosis (AE) is a highly pathogenic zoonotic disease caused by the larval stage of the cestode E. multilocularis. Its life-cycle includes more than 40 species of small mammal intermediate hosts. Therefore, host biodiversity losses could be expected to alter transmission. Climate may also have possible impacts on E. multilocularis egg survival. We examined the distribution of human AE across two spatial scales, (i) for continental China and (ii) over the eastern edge of the Tibetan plateau. We tested the hypotheses that human disease distribution can be explained by either the biodiversity of small mammal intermediate host species, or by environmental factors such as climate or landscape characteristics.

Methodology/findings

The distributions of 274 small mammal species were mapped to 967 point locations on a grid covering continental China. Land cover, elevation, monthly rainfall and temperature were mapped using remotely sensed imagery and compared to the distribution of human AE disease at continental scale and over the eastern Tibetan plateau. Infection status of 17,589 people screened by abdominal ultrasound in 2002–2008 in 94 villages of Tibetan areas of western Sichuan and Qinghai provinces was analyzed using generalized additive mixed models and related to epidemiological and environmental covariates. We found that human AE was not directly correlated with small mammal reservoir host species richness, but rather was spatially correlated with landscape features and climate which could confirm and predict human disease hotspots over a 200,000 km² region.

Conclusions/Significance

E. multilocularis transmission and resultant human disease risk was better predicted from landscape features that could support increases of small mammal host species prone to population outbreaks, rather than host species richness. We anticipate that our study may be a starting point for further research wherein landscape management could be used to predict human disease risk and for controlling this zoonotic helminthic.     

Echinococcus multilocularis in red foxes (Vulpes vulpes) of the Italian Alpine region: is there a focus of autochthonous transmission?

Alveolar echinococcosis, caused by the metacestode of Echinococcus multilocularis, is a zoonosis with a wider distribution area than described in the past. Fox populations living in the Alpine regions of Italy had been considered free from this parasite until 2002, when two infected foxes (Vulpes vulpes) were detected in the Bolzano province (Trentino Alto Adige region) near the Austrian border. The aim of this work was to evaluate the prevalence of infection in red fox populations from five Italian regions. A modified nested PCR analysis was used to detect E. multilocularis DNA in faecal samples. Amplicons were confirmed by sequencing. Of 500 faecal samples from foxes shot in Valle d'Aosta (n=57), Liguria (n=44), Lombardy (n=102), Veneto (n=56), and Trentino Alto Adige (n=241) regions, 24 animals, all from the Trentino Alto Adige region, were found positive. Twenty-two positive animals originated from the Bolzano province and two positive animals from the Trento province. Several localities of the Bolzano province, in which positive foxes were detected, are the same as those where alveolar echinococcosis had been described in humans in the second half of the 19th century, suggesting an old endemicity for the investigated area, which is adjacent to endemic areas of Austria. Therefore, the question arises if we are observing an increase and expansion of foci, or if the new records are due to the more sensitive and specific methods used to detect the worm DNA.     

Host manipulation by Ligula intestinalis: a cause or consequence of parasite aggregation?

Previous investigations suggest that the infection of the cyprinid roach, Rutilus rutilus, with the larval plerocercoid forms of the cestode, Ligula intestinalis, creates behavioural and morphological changes in the fish host, potentially of adaptive significance to the parasite in promoting transmission to definitive avian hosts. Here we consider whether these behavioural changes are important in shaping the distribution of parasite individuals across the fish population. An examination of field data illustrates that fish infected with a single parasite were more scarce than expected under the negative binomial distribution, and in many months were more scarce than burdens of two, three or more, leading to a bimodal distribution of worm counts (peaks at 0 and >1). This scarcity of single-larval worm infections could be accounted for a priori by a predominance of multiple infection. However, experimental infections of roach gave no evidence for the establishment of multiple worms, even when the host was challenged with multiple intermediate crustacean hosts, each multiply infected. A second hypothesis assumes that host manipulation following an initial single infection leads to an increased probability of subsequent infection (thus creating a contagious distribution). If manipulated fish are more likely to encounter infected first-intermediate hosts (through microhabitat change, increased ingestion, or both), then host manipulation could act as a powerful cause of aggregation. A number of scenarios based on contagious distribution models of aggregation are explored, contrasted with alternative compound Poisson models, and compared with the empirical data on L. intestinalis aggregation in their roach intermediate hosts. Our results indicate that parasite-induced host manipulation in this system can function simultaneously as both a consequence and a cause of parasite aggregation. This mutual interaction between host manipulation and parasite aggregation points to a set of ecological interactions that are easily missed in most experimental studies of either phenomenon.     

Differential virulence in a multiple‐host parasite of bumble bees: resolving the paradox of parasite survival?

Parasite virulence determines both the impact that parasites have on their hosts and parasite fitness. While most studies of virulence have involved single-species host–parasite interactions, the majority of parasites are likely to use multiple concurrent host species. Our understanding of how this impacts on parasite epidemiology and virulence is limited. Using the bumble bee Bombus lucorum , which exists in sympatry with B. terrestris in multi-species assemblages, and their generalist micosporidian parasite Nosema bombi , we tested whether the apparent paradox of parasite maintenance due to parasite virulence in a single host, B. terrestris , could be resolved through understanding the parasite's virulence in this sympatric host species. Nosema bombi significantly impacted colony growth, individual longevity, and individual development in B. lucorum . However, these effects were different both qualitatively and quantitatively to the parasite's impact in B. terrestris . Infected colonies of B. lucorum successfully produced both male and female reproductives, and infected female reproductives were capable of successful mating. Variation in life-history across host species may explain differences in the virulence, or impact of the parasite in B. terrestris and B. lucorum , with species with shorter life-cycles being more likely to transfer the parasite from one annual generation to the next. These results suggest that to understand the virulence and epidemiology of multi-host parasites we need to examine their ecological interactions across their various host species.     

Reappraising the theme of breeding systems in Echinococcus: is outcrossing a rare phenomenon?

Selfing has been considered the most common mode of reproduction in Echinococcus flatworms. However, population genetic studies on the asexual larval stage involving nuclear co-dominant markers have not always revealed significant heterozygote deficiencies--the expected outcome of a regularly and highly inbred population. In this study, we analysed the genetic structure of Echinococcus granulosus sensu lato populations from Southern Brazil during their adult (sexual) stage using 1 mitochondrial and 1 nuclear marker (cox 1 and mdh, respectively). We show that parasite genetic differentiation is largest among definitive hosts (domestic dogs) from different farms, suggesting that transmission is mostly maintained within a farm. Moreover, we show that heterozygote deficiencies are not significant, and we suggest that outbreeding is the most common mode of reproduction of the parasite in that region.     

Costly parasite resistance: a genotype-dependent handicap in sand lizards?

Male sand lizards (Lacerta agilis) with a specific restriction fragment length polymorphism fragment in their major histocompatibility complex (MHC) genotype ('O-males') are more resistant to ectoparasites (a tick, Ixodes ricinus) than are males that lack this fragment ('NO-males'). However, emerging evidence suggests that such adaptive immune responses are costly, here manifested by reduced body condition and a compromised defence against secondary infections by haemoprotid parasites that use the ticks as vectors. Subsequent to tick encounter, O-males suffer from a higher leucocyte-erythrocyte ratio, and higher haemoprotid parasitaemia, in particular in relation to vector encounter rate. Furthermore, O-males (i.e. successful tick defenders) with more haemoprotid parasites remaining in their blood stream were in better body condition, whereas this did not apply in NO-males, demonstrating that the adaptive immunoreaction can--in the short term--be energetically even more costly than being moderately parasitized. In agreement with Zahavian handicap theory, O-males had a (marginally) higher reproductive success than males that lacked this fragment.     

Dissemination of spores in a glasshouse: Pattern or chaos?

The dissemination of particles in a glasshouse with three united compartments was observed from experiments withLycopodium sp. The experiments were performed in a glasshouse with open and closed ventilation openings, spore sources on two heights above soil surface, and in two consecutive time intervals. The spores were caught with self constructed spore traps placed at regular distances from each other. Air circulation was observed using smoke-puffs. High ventilation caused a rapid cleaning of the air while in a closed glasshouse spores remained suspended for quite a long time. Though the three compartments of the glasshouse were not separated by walls, a so-called cell structure of the individual compartments could be indicated.     

Inflammation in atherosclerosis: a cause or a result of vascular disorders?

Sound data support the concept that in atherosclerosis, inflammation and dyslipidemia intersect each other and that irrespective of the initiator, both participate from the early stages to the ultimate fate of the atheromatous plaque. The two partakers manoeuvre a vicious circle in atheroma formation: dyslipidaemia triggers an inflammatory process and inflammation elicits dyslipidaemia. Independent of the initial cause, the atherosclerotic lesions occur focally, in particular arterial-susceptible sites, by a process that, although continuous, can be arbitrarily divided into a sequence of consecutive stages that lead from fatty streak to the fibro-lipid plaque and ultimately to plaque rupture and thrombosis. In the process, the initial event is a change in endothelial cells (EC) constitutive properties. Then, the molecular alarm signals send by dysfunctional EC are decoded by specific blood immune cells (monocytes, T lymphocytes, neutrophils, mast cells) and by the resident vascular cells, that respond by initiating a robust inflammatory process, in which the cells and the factors they secrete hasten the atheroma development. Direct and indirect crosstalk between the cells housed within the nascent plaque, complemented by the increase in risk factors of atherosclerosis lead to atheroma development and outcome. The initial inflammatory response can be regarded as a defense/protective reaction mechanism, but its further amplification, speeds up atherosclerosis. In this review, we provide an overview on the role of inflammation and dyslipidaemia and their intersection in atherogenesis. The data may add to the foundation of a novel attitude in the diagnosis and treatment of atherosclerosis.     

River blindness: a role for parasite retinoid-binding proteins in the generation of pathology?

A new family of fatty acid- and retinoid-binding proteins has recently been identified in nematodes. These are apparently nematode specific and have very different structures and binding characteristics to their mammalian counterparts. Retinoids have important roles in vision, tissue differentiation and repair, and can profoundly affect collagen synthesis. Binding proteins released by a parasite might therefore play a part in the generation of the skin and eye pathology seen in river blindness. They might also be involved in the formation of the subcutaneous nodules induced by this parasite.     

Is parasite pressure a driver of chemical cue diversity in ants?

Parasites and pathogens are possibly key evolutionary forces driving recognition systems. However, empirical evidence remains sparse. The ubiquitous pioneering ant Formica fusca is exploited by numerous socially parasitic ant species. We compared the chemical cue diversity, egg and nest mate recognition abilities in two Finnish and two UK populations where parasite pressure is high or absent, respectively. Finnish populations had excellent egg and nest mate discrimination abilities, which were lost in the UK populations. The loss of discrimination behaviour correlates with a loss in key recognition compounds (C₂₅-dimethylalkanes). This was not owing to genetic drift or different ecotypes since neutral gene diversity was the same in both countries. Furthermore, it is known that the cuticular hydrocarbon profiles of non-host ant species remain stable between Finland and the UK. The most parsimonious explanation for the striking difference in the cue diversity (number of C₂₅-dimethylalkanes isomers) between the UK and Finland populations is the large differences in parasite pressure experienced by F. fusca in the two countries. These results have strong parallels with bird (cuckoo) studies and support the hypothesis that parasites are driving recognition cue diversity.     

Cost of resistance: relationship between reduced fertility and increased resistance in a snail—schistosome host—parasite system

Natural host populations often exhibit genetic variability in resistance to parasitism. One possible mechanism for maintaining such diversity is a trade-off between fitness costs associated with resistance and fitness costs associated with parasitism. However, little is known about the nature or magnitude of these costs in animal populations. Using artificial selection experiments in a Biomphalaria glabrata–Schistosoma mansoni host–parasite system, we demonstrated that resistance and susceptibility to infection are heritable. We then investigated whether resistance had any associated costs in terms of snail reproductive success. Susceptible-selected snail lines showed significantly higher fertility (number of offspring produced) than resistant-selected or unselected control snail lines, irrespective of current infection status. There were no consistent differences between snail lines in fecundity, proportion of abnormal egg masses produced, or mean number of eggs per egg mass. Mortality rate was higher among infected than uninfected snails. These results are consistent with snails incurring costs of resistance to schistosome infection in the absence of the parasite.