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1.  Mortality associated with avian reovirus infection in a free-living magpie (Pica pica) in Great Britain 
Background
Avian reoviruses (ARVs) cause a range of disease presentations in domestic, captive and free-living bird species. ARVs have been reported as a cause of significant disease and mortality in free-living corvid species in North America and continental Europe. Until this report, there have been no confirmed cases of ARV-associated disease in British wild birds.
Case presentation
Sporadic individual magpie (Pica pica) mortality was detected at a single site in Buckinghamshire, England, April-September 2013. An adult female magpie was found moribund and subsequently died. Post-mortem examination identified hepatomegaly and splenomegaly as the most severe macroscopic abnormalities. Histopathological examination revealed extensive hepatic and splenic necrosis. Transmission electron microscopy (TEM) identified virions of a size (circa 78 nm diameter) and morphology consistent with ARV in both the liver and the small intestinal (SI) contents. Nucleic acid extracted from pooled liver and spleen was positive on both a pan-reovirus nested PCR targeting the RNA-dependent RNA polymerase gene and a PCR using primers specific to the ARV sigma C protein gene. Virus isolated from the liver and the SI contents was characterised by a syncytial-type cytopathic effect, a reovirus-like appearance on TEM and sequence identical to that from PCR of tissues. In situ hybridisation confirmed co-localisation of ARV with lesions in the liver and spleen, implicating ARV as the causative agent. Splenic lymphoid atrophy and necrotic stomatitis associated with Aspergillus fumigatus infection were consistent with generalised immunosuppression and resultant opportunistic infection.
Conclusions
The pathology and comprehensive virus investigations in this case indicate ARV as the primary pathogen in this magpie, with concurrent secondary infection subsequent to immunosuppression, as has been observed with reoviral infections in other bird species. ARV should be considered as a differential diagnosis for magpie, and potentially other corvid, disease and mortality incidents. This is the first demonstration of ARV-associated mortality in a wild bird in Britain. The prevalence and significance of ARV infection in British wild birds, and its implications for poultry and captive bird health, are currently unknown.
doi:10.1186/s12917-015-0329-5
PMCID: PMC4336486
Avian reovirus; Magpie; Pica pica; Hepatic necrosis; Splenic necrosis
2.  Using Modelling to Disentangle the Relative Contributions of Zoonotic and Anthroponotic Transmission: The Case of Lassa Fever 
Background
Zoonotic infections, which transmit from animals to humans, form the majority of new human pathogens. Following zoonotic transmission, the pathogen may already have, or may acquire, the ability to transmit from human to human. With infections such as Lassa fever (LF), an often fatal, rodent-borne, hemorrhagic fever common in areas of West Africa, rodent-to-rodent, rodent-to-human, human-to-human and even human-to-rodent transmission patterns are possible. Indeed, large hospital-related outbreaks have been reported. Estimating the proportion of transmission due to human-to-human routes and related patterns (e.g. existence of super-spreaders), in these scenarios is challenging, but essential for planned interventions.
Methodology/Principal Findings
Here, we make use of an innovative modeling approach to analyze data from published outbreaks and the number of LF hospitalized patients to Kenema Government Hospital in Sierra Leone to estimate the likely contribution of human-to-human transmission. The analyses show that almost of the cases at KGH are secondary cases arising from human-to-human transmission. However, we found much of this transmission is associated with a disproportionally large impact of a few individuals (‘super-spreaders’), as we found only of human cases result in an effective reproduction number (i.e. the average number of secondary cases per infectious case) , with a maximum value up to .
Conclusions/Significance
This work explains the discrepancy between the sizes of reported LF outbreaks and a clinical perception that human-to-human transmission is low. Future assessment of risks of LF and infection control guidelines should take into account the potentially large impact of super-spreaders in human-to-human transmission. Our work highlights several neglected topics in LF research, the occurrence and nature of super-spreading events and aspects of social behavior in transmission and detection.
Author Summary
Many pathogens have the ability to infect different species. Lassa fever virus is an important example; this virus infects a species of rodent in West Africa, and can cause a severe disease in people. Lassa fever virus is transmitted from rodent-to-rodent, rodent-to-human, human-to-human and perhaps human-to-rodent. So far, the relative importance of these routes has not been assessed. Here we focus on the risk for humans; undoubtedly, most human infections are acquired by contact with rodents or their urine, but the relative risk of rodent-to-human and human-to-human transmission is unknown. We use mathematical modeling to address this. First, we identified Lassa fever outbreaks known to be due to human-to-human chains of transmission. Then, we looked at people hospitalized with the disease in Kenema Government Hospital, Sierra Leone (KGH), who could have been infected either by rodents or humans. We asked, what should the proportion of patients be who get infected by humans, assuming the statistical patterns observed in the human-to-human chains are the same in both instances? We found that around of patients with Lassa fever in KGH probably acquired the disease from another person. In addition, the patterns of disease in people suggest that these of cases are probably initiated by only a small number of infected people (who could be thought of as super-spreaders).
doi:10.1371/journal.pntd.0003398
PMCID: PMC4288732  PMID: 25569707
3.  Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis 
BMC Genomics  2014;15(1):1066.
Background
Bacteria in the genus Ruminococcus are ubiquitous members of the mammalian gastrointestinal tract. In particular, they are important in ruminants where they digest a wide range of plant cell wall polysaccharides. For example, Ruminococcus albus 7 is a primary cellulose degrader that produces acetate usable by its bovine host. Moreover, it is one of the few organisms that ferments cellulose to form ethanol at mesophilic temperatures in vitro. The mechanism of cellulose degradation by R. albus 7 is not well-defined and is thought to involve pilin-like proteins, unique carbohydrate-binding domains, a glycocalyx, and cellulosomes. Here, we used a combination of comparative genomics, fermentation analyses, and transcriptomics to further clarify the cellulolytic and fermentative potential of R. albus 7.
Results
A comparison of the R. albus 7 genome sequence against the genome sequences of related bacteria that either encode or do not encode cellulosomes revealed that R. albus 7 does not encode for most canonical cellulosomal components. Fermentation analysis of R. albus 7 revealed the ability to produce ethanol and acetate on a wide range of fibrous substrates in vitro. Global transcriptomic analysis of R. albus 7 grown at identical dilution rates on cellulose and cellobiose in a chemostat showed that this bacterium, when growing on cellulose, utilizes a carbohydrate-degrading strategy that involves increased transcription of the rare carbohydrate-binding module (CBM) family 37 domain and the tryptophan biosynthetic operon.
Conclusions
Our data suggest that R. albus 7 does not use canonical cellulosomal components to degrade cellulose, but rather up-regulates the expression of CBM37-containing enzymes and tryptophan biosynthesis. This study contributes to a revised model of carbohydrate degradation by this key member of the rumen ecosystem.
Electronic supplementary material
The online version of this article (doi:10.1186/1471-2164-15-1066) contains supplementary material, which is available to authorized users.
doi:10.1186/1471-2164-15-1066
PMCID: PMC4300822  PMID: 25477200
Ruminococcus albus; Cellulose utilization; Ethanol production
4.  Proximity to Coast Is Linked to Climate Change Belief 
PLoS ONE  2014;9(7):e103180.
Psychologists have examined the many psychological barriers to both climate change belief and concern. One barrier is the belief that climate change is too uncertain, and likely to happen in distant places and times, to people unlike oneself. Related to this perceived psychological distance of climate change, studies have shown that direct experience of the effects of climate change increases climate change concern. The present study examined the relationship between physical proximity to the coastline and climate change belief, as proximity may be related to experiencing or anticipating the effects of climate change such as sea-level rise. We show, in a national probability sample of 5,815 New Zealanders, that people living in closer proximity to the shoreline expressed greater belief that climate change is real and greater support for government regulation of carbon emissions. This proximity effect held when adjusting for height above sea level and regional poverty. The model also included individual differences in respondents' sex, age, education, political orientation, and wealth. The results indicate that physical place plays a role in the psychological acceptance of climate change, perhaps because the effects of climate change become more concrete and local.
doi:10.1371/journal.pone.0103180
PMCID: PMC4105574  PMID: 25047568
5.  Continent-wide panmixia of an African fruit bat facilitates transmission of potentially zoonotic viruses 
Nature communications  2013;4:10.1038/ncomms3770.
The straw-coloured fruit bat, Eidolon helvum, is Africa’s most widely distributed and commonly hunted fruit bat, often living in close proximity to human populations. This species has been identified as a reservoir of potentially zoonotic viruses, but uncertainties remain regarding viral transmission dynamics and mechanisms of persistence. Here we combine genetic and serological analyses of populations across Africa, to determine the extent of epidemiological connectivity among E. helvum populations. Multiple markers reveal panmixia across the continental range, at a greater geographical scale than previously recorded for any other mammal, whereas populations on remote islands were genetically distinct. Multiple serological assays reveal antibodies to henipaviruses and Lagos bat virus in all locations, including small isolated island populations, indicating that factors other than population size and connectivity may be responsible for viral persistence. Our findings have potentially important public health implications, and highlight a need to avoid disturbances which may precipitate viral spillover.
doi:10.1038/ncomms3770
PMCID: PMC3836177  PMID: 24253424
6.  Bat Flight and Zoonotic Viruses 
Emerging Infectious Diseases  2014;20(5):741-745.
High metabolism and body temperatures of flying bats might enable them to host many viruses.
Bats are sources of high viral diversity and high-profile zoonotic viruses worldwide. Although apparently not pathogenic in their reservoir hosts, some viruses from bats severely affect other mammals, including humans. Examples include severe acute respiratory syndrome coronaviruses, Ebola and Marburg viruses, and Nipah and Hendra viruses. Factors underlying high viral diversity in bats are the subject of speculation. We hypothesize that flight, a factor common to all bats but to no other mammals, provides an intensive selective force for coexistence with viral parasites through a daily cycle that elevates metabolism and body temperature analogous to the febrile response in other mammals. On an evolutionary scale, this host–virus interaction might have resulted in the large diversity of zoonotic viruses in bats, possibly through bat viruses adapting to be more tolerant of the fever response and less virulent to their natural hosts.
doi:10.3201/eid2005.130539
PMCID: PMC4012789  PMID: 24750692
bats; body temperature; Chiroptera; emerging zoonotic viruses; fever; flight; metabolic rate; mammals
7.  A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? 
Bats are the natural reservoirs of a number of high-impact viral zoonoses. We present a quantitative analysis to address the hypothesis that bats are unique in their propensity to host zoonotic viruses based on a comparison with rodents, another important host order. We found that bats indeed host more zoonotic viruses per species than rodents, and we identified life-history and ecological factors that promote zoonotic viral richness. More zoonotic viruses are hosted by species whose distributions overlap with a greater number of other species in the same taxonomic order (sympatry). Specifically in bats, there was evidence for increased zoonotic viral richness in species with smaller litters (one young), greater longevity and more litters per year. Furthermore, our results point to a new hypothesis to explain in part why bats host more zoonotic viruses per species: the stronger effect of sympatry in bats and more viruses shared between bat species suggests that interspecific transmission is more prevalent among bats than among rodents. Although bats host more zoonotic viruses per species, the total number of zoonotic viruses identified in bats (61) was lower than in rodents (68), a result of there being approximately twice the number of rodent species as bat species. Therefore, rodents should still be a serious concern as reservoirs of emerging viruses. These findings shed light on disease emergence and perpetuation mechanisms and may help lead to a predictive framework for identifying future emerging infectious virus reservoirs.
doi:10.1098/rspb.2012.2753
PMCID: PMC3574368  PMID: 23378666
trait-based approaches; zoonoses; viral richness; reservoir host; spillover; Chiroptera
8.  Using network theory to identify the causes of disease outbreaks of unknown origin 
The identification of undiagnosed disease outbreaks is critical for mobilizing efforts to prevent widespread transmission of novel virulent pathogens. Recent developments in online surveillance systems allow for the rapid communication of the earliest reports of emerging infectious diseases and tracking of their spread. The efficacy of these programs, however, is inhibited by the anecdotal nature of informal reporting and uncertainty of pathogen identity in the early stages of emergence. We developed theory to connect disease outbreaks of known aetiology in a network using an array of properties including symptoms, seasonality and case-fatality ratio. We tested the method with 125 reports of outbreaks of 10 known infectious diseases causing encephalitis in South Asia, and showed that different diseases frequently form distinct clusters within the networks. The approach correctly identified unknown disease outbreaks with an average sensitivity of 76 per cent and specificity of 88 per cent. Outbreaks of some diseases, such as Nipah virus encephalitis, were well identified (sensitivity = 100%, positive predictive values = 80%), whereas others (e.g. Chandipura encephalitis) were more difficult to distinguish. These results suggest that unknown outbreaks in resource-poor settings could be evaluated in real time, potentially leading to more rapid responses and reducing the risk of an outbreak becoming a pandemic.
doi:10.1098/rsif.2012.0904
PMCID: PMC3627096  PMID: 23389893
emerging infectious disease; encephalitis; complex networks; South Asia; cluster analysis; early warning systems
9.  Epidemiological Evidence That Garden Birds Are a Source of Human Salmonellosis in England and Wales 
PLoS ONE  2014;9(2):e88968.
The importance of wild bird populations as a reservoir of zoonotic pathogens is well established. Salmonellosis is a frequently diagnosed infectious cause of mortality of garden birds in England and Wales, predominantly caused by Salmonella enterica subspecies enterica serovar Typhimurium definitive phage types 40, 56(v) and 160. In Britain, these phage types are considered highly host-adapted with a high degree of genetic similarity amongst isolates, and in some instances are clonal. Pulsed field gel electrophoresis, however, demonstrated minimal variation amongst matched DT40 and DT56(v) isolates derived from passerine and human incidents of salmonellosis across England in 2000–2007. Also, during the period 1993–2012, similar temporal and spatial trends of infection with these S. Typhimurium phage types occurred in both the British garden bird and human populations; 1.6% of all S. Typhimurium (0.2% of all Salmonella) isolates from humans in England and Wales over the period 2000–2010. These findings support the hypothesis that garden birds act as the primary reservoir of infection for these zoonotic bacteria. Most passerine salmonellosis outbreaks identified occurred at and around feeding stations, which are likely sites of public exposure to sick or dead garden birds and their faeces. We, therefore, advise the public to practise routine personal hygiene measures when feeding wild birds and especially when handling sick wild birds.
doi:10.1371/journal.pone.0088968
PMCID: PMC3935841  PMID: 24586464
10.  Is Chytridiomycosis Driving Darwin’s Frogs to Extinction? 
PLoS ONE  2013;8(11):e79862.
Darwin’s frogs (Rhinoderma darwinii and R. rufum) are two species of mouth brooding frogs from Chile and Argentina that have experienced marked population declines. Rhinoderma rufum has not been found in the wild since 1980. We investigated historical and current evidence of Batrachochytrium dendrobatidis (Bd) infection in Rhinoderma spp. to determine whether chytridiomycosis is implicated in the population declines of these species. Archived and live specimens of Rhinoderma spp., sympatric amphibians and amphibians at sites where Rhinoderma sp. had recently gone extinct were examined for Bd infection using quantitative real-time PCR. Six (0.9%) of 662 archived anurans tested positive for Bd (4/289 R. darwinii; 1/266 R. rufum and 1/107 other anurans), all of which had been collected between 1970 and 1978. An overall Bd-infection prevalence of 12.5% was obtained from 797 swabs taken from 369 extant individuals of R. darwinii and 428 individuals representing 18 other species of anurans found at sites with current and recent presence of the two Rhinoderma species. In extant R. darwinii, Bd-infection prevalence (1.9%) was significantly lower than that found in other anurans (7.3%). The prevalence of infection (30%) in other amphibian species was significantly higher in sites where either Rhinoderma spp. had become extinct or was experiencing severe population declines than in sites where there had been no apparent decline (3.0%; x2 = 106.407, P<0.001). This is the first report of widespread Bd presence in Chile and our results are consistent with Rhinoderma spp. declines being due to Bd infection, although additional field and laboratory investigations are required to investigate this further.
doi:10.1371/journal.pone.0079862
PMCID: PMC3835940  PMID: 24278196
11.  The emergence and spread of finch trichomonosis in the British Isles 
Finch trichomonosis, caused by the protozoal parasite Trichomonas gallinae, was first recognized as an emerging infectious disease of British passerines in 2005. The first year of seasonal epidemic mortality occurred in 2006 with significant declines of greenfinch Carduelis chloris and chaffinch Fringilla coelebs populations. Here, we demonstrate that large-scale mortality, principally of greenfinch, continued in subsequent years, 2007–2009, with a shifting geographical distribution across the British Isles over time. Consequent to the emergence of finch trichomonosis, the breeding greenfinch population in Great Britain has declined from ca 4.3 million to ca 2.8 million birds and the maximum mean number of greenfinches (a proxy for flock size) visiting gardens has declined by 50 per cent. The annual rate of decline of the breeding greenfinch population within England has exceeded 7 per cent since the initial epidemic. Although initially chaffinch populations were regionally diminished by the disease, this has not continued. Retrospective analyses of disease surveillance data showed a rapid, widespread emergence of finch trichomonosis across Great Britain in 2005 and we hypothesize that the disease emerged by T. gallinae jumping from columbiforms to passeriforms. Further investigation is required to determine the continuing impact of finch trichomonosis and to develop our understanding of how protozoal diseases jump host species.
doi:10.1098/rstb.2012.0130
PMCID: PMC3427565  PMID: 22966140
Trichomonas gallinae; trichomonosis; greenfinch; Carduelis chloris; emerging infectious disease; population decline
12.  PAI-1 promotes the accumulation of exudate macrophages and worsens pulmonary fibrosis following type II alveolar epithelial cell injury 
The Journal of pathology  2012;228(2):170-180.
Fibrotic disorders of the lung are associated with perturbations in the plasminogen activation system. Specifically, plasminogen activator inhibitor-1 (PAI-1) expression is increased relative to the plasminogen activators. A direct role for this imbalance in modulating the severity of lung scarring following injury has been substantiated in the bleomycin model of pulmonary fibrosis. However, it remains unclear whether derangements in the plasminogen activation system contribute more generally to the pathogenesis of lung fibrosis beyond bleomycin injury. To answer this question, we employed an alternative model of lung scarring, in which type II alveolar epithelial cells (AECs) are specifically injured by administering diphtheria toxin (DT) to mice genetically engineered to express the human DT receptor (DTR) off the surfactant protein C promoter. This targeted AEC injury results in the diffuse accumulation of interstitial collagen. In the present study, we found that this targeted type II cell insult also increases PAI-1 expression in the alveolar compartment. We identified AECs and lung macrophages to be sources of PAI-1 production. To determine whether this elevated PAI-1 concentration was directly related to the severity of fibrosis, DTR+ mice were crossed into a PAI-1-deficient background (DTR+: PAI-1−/−). DT administration to DTR+: PAI-1−/− animals caused significantly less fibrosis than was measured in DTR+ mice with intact PAI-1 production. PAI-1 deficiency also abrogated the accumulation of CD11b+ exudate macrophages that were found to express PAI-1 and type-1 collagen. These observations substantiate the critical function of PAI-1 in pulmonary fibrosis pathogenesis and provide new insight into a potential mechanism by which this pro-fibrotic molecule influences collagen accumulation.
doi:10.1002/path.3992
PMCID: PMC3529409  PMID: 22262246
PAI-1; lung; fibrosis; macrophage
13.  Peroxisome proliferator-activated receptor γ agonist effect on rheumatoid arthritis: a randomized controlled trial 
Arthritis Research & Therapy  2013;15(5):R110.
Introduction
Rheumatoid arthritis (RA), a chronic inflammatory disease, is associated with insulin resistance. Experimental evidence indicates that the relationship between insulin resistance and inflammation is bidirectional: Inflammation promotes insulin resistance, and insulin resistance promotes inflammation. Therefore, we examined the hypothesis that pioglitazone, a thiazolidinedione peroxisome proliferator-activated receptor γ agonist, would decrease inflammation and disease activity and improve insulin resistance in patients with RA.
Methods
In a single-center, randomized, double-blind, placebo-controlled crossover study patients with RA (N = 34) receiving stable therapy were randomized to also receive either pioglitazone 45 mg daily (n = 17) or matching placebo (n = 17) for eight weeks. This was followed by a four-week washout period and alternative treatment for eight weeks. Outcomes included change in Disease Activity Score in 28 joints (DAS28) score, individual components of the DAS28 score and homeostatic model assessment for insulin resistance (HOMA). Intention-to-treat analysis and linear mixed-effects models were used.
Results
Patients had a mean (±SD) age of 51 (±14.2) years, 82.4% were female and baseline DAS28 high-sensitivity C-reactive protein (DAS28-CRP) was 4.58 (±1.1) units. Addition of pioglitazone was associated with a 9.3% reduction (95% confidence interval (CI) = 0.17% to 17.6%) in DAS28-CRP (P = 0.046), but no significant change in DAS28 erythrocyte sedimentation rate (DAS28-ESR) (P = 0.92). There was a 10.7mm (95% CI = 0.4 to 20.9 mm) improvement in patient-reported global health (P = 0.042), a 48.6% decrease (95% CI = 27.6% to 63.5%) in CRP (P < 0.001) and a 26.4% decrease (95% CI = 3.7% to 43.8%) in insulin resistance as measured by HOMA (P = 0.025), but no significant reduction in swollen or tender joint count or in ESR (all P > 0.05). Lower-extremity edema was more common during pioglitazone treatment (16%) than placebo (0%).
Conclusion
Addition of pioglitazone to RA therapy improves insulin resistance and modestly reduces RA disease activity measured by DAS28-CRP and two of its components, including patient-reported global health and CRP, but not DAS28-ESR or ESR.
Trial registration
NCT00763139
doi:10.1186/ar4290
PMCID: PMC3978636  PMID: 24020899
14.  Primate communication in the pure ultrasound 
Biology Letters  2012;8(4):508-511.
Few mammals—cetaceans, domestic cats and select bats and rodents—can send and receive vocal signals contained within the ultrasonic domain, or pure ultrasound (greater than 20 kHz). Here, we use the auditory brainstem response (ABR) method to demonstrate that a species of nocturnal primate, the Philippine tarsier (Tarsius syrichta), has a high-frequency limit of auditory sensitivity of ca 91 kHz. We also recorded a vocalization with a dominant frequency of 70 kHz. Such values are among the highest recorded for any terrestrial mammal, and a relatively extreme example of ultrasonic communication. For Philippine tarsiers, ultrasonic vocalizations might represent a private channel of communication that subverts detection by predators, prey and competitors, enhances energetic efficiency, or improves detection against low-frequency background noise.
doi:10.1098/rsbl.2011.1149
PMCID: PMC3391437  PMID: 22319094
ultrasound; sensory ecology; bioacoustics; auditory brainstem response; evoked potential audiogram
15.  Social drive and the evolution of primate hearing 
The structure and function of primate communication have attracted much attention, and vocal signals, in particular, have been studied in detail. As a general rule, larger social groups emit more types of vocal signals, including those conveying the presence of specific types of predators. The adaptive advantages of receiving and responding to alarm calls are expected to exert a selective pressure on the auditory system. Yet, the comparative biology of primate hearing is limited to select species, and little attention has been paid to the effects of social and vocal complexity on hearing. Here, we use the auditory brainstem response method to generate the largest number of standardized audiograms available for any primate radiation. We compared the auditory sensitivities of 11 strepsirrhine species with and without independent contrasts and show that social complexity explains a significant amount of variation in two audiometric parameters—overall sensitivity and high-frequency limit. We verified the generality of this latter result by augmenting our analysis with published data from nine species spanning the primate order. To account for these findings, we develop and test a model of social drive. We hypothesize that social complexity has favoured enhanced hearing sensitivities, especially at higher frequencies.
doi:10.1098/rstb.2011.0219
PMCID: PMC3367701  PMID: 22641824
Strepsirrhini; hearing; auditory brainstem response; evoked potential audiogram; sensory ecology; acoustic communication
16.  Metagenomic study of the viruses of African straw-coloured fruit bats: Detection of a chiropteran poxvirus and isolation of a novel adenovirus 
Virology  2013;441(2):95-106.
Viral emergence as a result of zoonotic transmission constitutes a continuous public health threat. Emerging viruses such as SARS coronavirus, hantaviruses and henipaviruses have wildlife reservoirs. Characterising the viruses of candidate reservoir species in geographical hot spots for viral emergence is a sensible approach to develop tools to predict, prevent, or contain emergence events. Here, we explore the viruses of Eidolon helvum, an Old World fruit bat species widely distributed in Africa that lives in close proximity to humans. We identified a great abundance and diversity of novel herpes and papillomaviruses, described the isolation of a novel adenovirus, and detected, for the first time, sequences of a chiropteran poxvirus closely related with Molluscum contagiosum. In sum, E. helvum display a wide variety of mammalian viruses, some of them genetically similar to known human pathogens, highlighting the possibility of zoonotic transmission.
Highlights
•The first metagenomic study of a chiropteran (bat) suborder.•Demonstrates a novel and thorough bioinformatics pipeline for metagenomic studies.•Multiple novel, diverse viruses present in an urban African bat bushmeat species.•The study is supported with further molecular evidence and virus isolation.•The study contains the first evidence of chiropteran poxviruses and a novel bat adenovirus isolate.
doi:10.1016/j.virol.2013.03.014
PMCID: PMC3667569  PMID: 23562481
Virome; Bat; Megabat; Poxvirus; Viral emergence; Metagenomics; Adenovirus
17.  The Population Decline and Extinction of Darwin’s Frogs 
PLoS ONE  2013;8(6):e66957.
Darwin’s frogs (Rhinoderma darwinii and R. rufum) are two species of mouth-brooding frogs from Chile and Argentina. Here, we present evidence on the extent of declines, current distribution and conservation status of Rhinoderma spp.; including information on abundance, habitat and threats to extant Darwin’s frog populations. All known archived Rhinoderma specimens were examined in museums in North America, Europe and South America. Extensive surveys were carried out throughout the historical ranges of R. rufum and R. darwinii from 2008 to 2012. Literature review and location data of 2,244 archived specimens were used to develop historical distribution maps for Rhinoderma spp. Based on records of sightings, optimal linear estimation was used to estimate whether R. rufum can be considered extinct. No extant R. rufum was found and our modelling inferred that this species became extinct in 1982 (95% CI, 1980–2000). Rhinoderma darwinii was found in 36 sites. All populations were within native forest and abundance was highest in Chiloé Island, when compared with Coast, Andes and South populations. Estimated population size and density (five populations) averaged 33.2 frogs/population (range, 10.2–56.3) and 14.9 frogs/100 m2 (range, 5.3–74.1), respectively. Our results provide further evidence that R. rufum is extinct and indicate that R. darwinii has declined to a much greater degree than previously recognised. Although this species can still be found across a large part of its historical range, remaining populations are small and severely fragmented. Conservation efforts for R. darwinii should be stepped up and the species re-classified as Endangered.
doi:10.1371/journal.pone.0066957
PMCID: PMC3680453  PMID: 23776705
18.  Aedes Taeniorhynchus Vectorial Capacity Informs A Pre-Emptive Assessment Of West Nile Virus Establishment In Galápagos 
Scientific Reports  2013;3:1519.
Increased connectivity with the mainland has led to the arrival of many invasive species to the Galápagos Islands, including novel pathogens, threatening the archipelago's unique fauna. Here we consider the potential role of the mosquito Aedes taeniorhynchus in maintaining the flavivirus West Nile virus [WNV] should it reach the islands. We report on three components of vectorial capacity - vector competency, distributional abundance and host-feeding. In contrast to USA strains, Galápagos A. taeniorhynchus is a competent and efficient WNV vector, capable of transmission at 5 days post-exposure. Based on 25 blood-meals, mammalian feeding suggests a potential bridge vector role should contact with key amplification taxa occur. Vector population abundance is driven primarily by climatic factors, peaking between January and March. As a ubiquitous competent vector, A. taeniorhynchus may facilitate future WNV establishment, therefore it is vital to ensure the biosecurity of Galápagos to prevent introductions of pathogens such as WNV.
doi:10.1038/srep01519
PMCID: PMC3605609  PMID: 23519190
19.  Demography of straw-colored fruit bats in Ghana 
Journal of mammalogy  2012;93(5):1393-1404.
Eidolon helvum is widely distributed across sub-Saharan Africa where it forms large, dense colonies. The species is migratory and satellite telemetry studies have demonstrated that individuals can migrate over 2,500 km. It is a common source of bush meat in West Africa and evidence of infection with potentially zoonotic viruses has been found in West African colonies. The species, therefore, is of interest to both ecologists and those interested in public health. Despite this, demographic parameters of the species are unknown. We focused our study primarily on a colony of up to 1,000,000 bats that roost in trees in Accra, Ghana to obtain estimates of birth rate and survival probability. Aging of bats by examination of tooth cementum annuli allowed use of life tables to indicate an annual survival probability for juveniles of 0.43 (95% confidence interval [CI] 0.16–0.77) and for adults of 0.83 (95% CI 0.73–0.93). Additionally, an annual adult survival probability of 0.63 (95% CI 0.27–0.88) was estimated by following 98 radiocollared bats over a year; capture–recapture data were analyzed using multistate models to address the confounding factor of emigration. True survival probabilities may be in between the 2 estimates, because permanent emigration may lead to underestimation in the capture–recapture study, and population decline may lead to overestimation in the life table analysis. Birth rates (0.96 young per female per year, 95% CI 0.92–0.98) and colony size changes were also estimated. Estimation of these key parameters will allow future analyses of both infection dynamics within, and harvest sustainability of, E. helvum populations.
doi:10.1644/11-MAMM-A-270.1
PMCID: PMC3605799  PMID: 23525358
capture–recapture; Eidolon helvum; multistate model; population dynamics; survival; tooth cementum
20.  West Africa - A Safe Haven for Frogs? A Sub-Continental Assessment of the Chytrid Fungus (Batrachochytrium dendrobatidis) 
PLoS ONE  2013;8(2):e56236.
A putative driver of global amphibian decline is the panzootic chytrid fungus Batrachochytrium dendrobatidis (Bd). While Bd has been documented across continental Africa, its distribution in West Africa remains ambiguous. We tested 793 West African amphibians (one caecilian and 61 anuran species) for the presence of Bd. The samples originated from seven West African countries - Bénin, Burkina Faso, Côte d'Ivoire, Ghana, Guinea, Liberia, Sierra Leone - and were collected from a variety of habitats, ranging from lowland rainforests to montane forests, montane grasslands to humid and dry lowland savannahs. The species investigated comprised various life-history strategies, but we focused particularly on aquatic and riparian species. We used diagnostic PCR to screen 656 specimen swabs and histology to analyse 137 specimen toe tips. All samples tested negative for Bd, including a widespread habitat generalist Hoplobatrachus occipitalis which is intensively traded on the West African food market and thus could be a potential dispersal agent for Bd. Continental fine-grained (30 arc seconds) environmental niche models suggest that Bd should have a broad distribution across West Africa that includes most of the regions and habitats that we surveyed. The surprising apparent absence of Bd in West Africa indicates that the Dahomey Gap may have acted as a natural barrier. Herein we highlight the importance of this Bd-free region of the African continent - especially for the long-term conservation of several threatened species depending on fast flowing forest streams (Conraua alleni (“Vulnerable”) and Petropedetes natator (“Near Threatened”)) as well as the “Critically Endangered” viviparous toad endemic to the montane grasslands of Mount Nimba (Nimbaphrynoides occidentalis).
doi:10.1371/journal.pone.0056236
PMCID: PMC3572032  PMID: 23426141
21.  Novel, Potentially Zoonotic Paramyxoviruses from the African Straw-Colored Fruit Bat Eidolon helvum 
Journal of Virology  2013;87(3):1348-1358.
Bats carry a variety of paramyxoviruses that impact human and domestic animal health when spillover occurs. Recent studies have shown a great diversity of paramyxoviruses in an urban-roosting population of straw-colored fruit bats in Ghana. Here, we investigate this further through virus isolation and describe two novel rubulaviruses: Achimota virus 1 (AchPV1) and Achimota virus 2 (AchPV2). The viruses form a phylogenetic cluster with each other and other bat-derived rubulaviruses, such as Tuhoko viruses, Menangle virus, and Tioman virus. We developed AchPV1- and AchPV2-specific serological assays and found evidence of infection with both viruses in Eidolon helvum across sub-Saharan Africa and on islands in the Gulf of Guinea. Longitudinal sampling of E. helvum indicates virus persistence within fruit bat populations and suggests spread of AchPVs via horizontal transmission. We also detected possible serological evidence of human infection with AchPV2 in Ghana and Tanzania. It is likely that clinically significant zoonotic spillover of chiropteran paramyxoviruses could be missed throughout much of Africa where health surveillance and diagnostics are poor and comorbidities, such as infection with HIV or Plasmodium sp., are common.
doi:10.1128/JVI.01202-12
PMCID: PMC3554137  PMID: 23152534
22.  Emergence of a Novel Avian Pox Disease in British Tit Species 
PLoS ONE  2012;7(11):e40176.
Avian pox is a viral disease with a wide host range. In Great Britain, avian pox in birds of the Paridae family was first diagnosed in a great tit (Parus major) from south-east England in 2006. An increasing number of avian pox incidents in Paridae have been reported each year since, indicative of an emergent infection. Here, we utilise a database of opportunistic reports of garden bird mortality and morbidity to analyse spatial and temporal patterns of suspected avian pox throughout Great Britain, 2006–2010. Reports of affected Paridae (211 incidents) outnumbered reports in non-Paridae (91 incidents). The majority (90%) of Paridae incidents involved great tits. Paridae pox incidents were more likely to involve multiple individuals (77.3%) than were incidents in non-Paridae hosts (31.9%). Unlike the small wart-like lesions usually seen in non-Paridae with avian pox in Great Britain, lesions in Paridae were frequently large, often with an ulcerated surface and caseous core. Spatial analyses revealed strong clustering of suspected avian pox incidents involving Paridae hosts, but only weak, inconsistent clustering of incidents involving non-Paridae hosts. There was no spatial association between Paridae and non-Paridae incidents. We documented significant spatial spread of Paridae pox from an origin in south-east England; no spatial spread was evident for non-Paridae pox. For both host clades, there was an annual peak of reports in August/September. Sequencing of the avian poxvirus 4b core protein produced an identical viral sequence from each of 20 great tits tested from Great Britain. This sequence was identical to that from great tits from central Europe and Scandinavia. In contrast, sequence variation was evident amongst virus tested from 17 non-Paridae hosts of 5 species. Our findings show Paridae pox to be an emerging infectious disease in wild birds in Great Britain, apparently originating from viral incursion from central Europe or Scandinavia.
doi:10.1371/journal.pone.0040176
PMCID: PMC3504035  PMID: 23185231
23.  Individual and Population-Level Impacts of an Emerging Poxvirus Disease in a Wild Population of Great Tits 
PLoS ONE  2012;7(11):e48545.
Emerging infectious diseases of wildlife can have severe effects on host populations and constitute a pressing problem for biodiversity conservation. Paridae pox is an unusually severe form of avipoxvirus infection that has recently been identified as an emerging infectious disease particularly affecting an abundant songbird, the great tit (Parus major), in Great Britain. In this study, we study the invasion and establishment of Paridae pox in a long-term monitored population of wild great tits to (i) quantify the impact of this novel pathogen on host fitness and (ii) determine the potential threat it poses to population persistence. We show that Paridae pox significantly reduces the reproductive output of great tits by reducing the ability of parents to fledge young successfully and rear those young to independence. Our results also suggested that pathogen transmission from diseased parents to their offspring was possible, and that disease entails severe mortality costs for affected chicks. Application of multistate mark-recapture modelling showed that Paridae pox causes significant reductions to host survival, with particularly large effects observed for juvenile survival. Using an age-structured population model, we demonstrate that Paridae pox has the potential to reduce population growth rate, primarily through negative impacts on host survival rates. However, at currently observed prevalence, significant disease-induced population decline seems unlikely, although pox prevalence may be underestimated if capture probability of diseased individuals is low. Despite this, because pox-affected model populations exhibited lower average growth rates, this emerging infectious disease has the potential to reduce the resilience of populations to other environmental factors that reduce population size.
doi:10.1371/journal.pone.0048545
PMCID: PMC3504048  PMID: 23185263
24.  Epidemiology of the Emergent Disease Paridae pox in an Intensively Studied Wild Bird Population 
PLoS ONE  2012;7(11):e38316.
Paridae pox, a novel avipoxvirus infection, has recently been identified as an emerging infectious disease affecting wild tit species in Great Britain. The incursion of Paridae pox to a long-term study site where populations of wild tits have been monitored in detail for several decades provided a unique opportunity to obtain information on the local-scale epidemiological characteristics of this novel infection during a disease outbreak. Using captures of >8000 individual birds, we show that, within two years of initial emergence, Paridae pox had become established within the population of great tits (Parus major) reaching relatively high peak prevalence (10%), but was far less prevalent (<1%) in sympatric populations of several other closely related, abundant Paridae species. Nonlinear smoothing models revealed that the temporal pattern of prevalence among great tits was characterised by within-year fluctuations indicative of seasonal forcing of infection rates, which was likely driven by multiple environmental and demographic factors. There was individual heterogeneity in the course of infection and, although recovery was possible, diseased individuals were far less likely to be recaptured than healthy individuals, suggesting a survival cost of infection. This study demonstrates the value of long-term monitoring for obtaining key epidemiological data necessary to understand disease dynamics, spread and persistence in natural populations.
doi:10.1371/journal.pone.0038316
PMCID: PMC3504069  PMID: 23185230
25.  A framework for the study of zoonotic disease emergence and its drivers: spillover of bat pathogens as a case study 
Many serious emerging zoonotic infections have recently arisen from bats, including Ebola, Marburg, SARS-coronavirus, Hendra, Nipah, and a number of rabies and rabies-related viruses, consistent with the overall observation that wildlife are an important source of emerging zoonoses for the human population. Mechanisms underlying the recognized association between ecosystem health and human health remain poorly understood and responding appropriately to the ecological, social and economic conditions that facilitate disease emergence and transmission represents a substantial societal challenge. In the context of disease emergence from wildlife, wildlife and habitat should be conserved, which in turn will preserve vital ecosystem structure and function, which has broader implications for human wellbeing and environmental sustainability, while simultaneously minimizing the spillover of pathogens from wild animals into human beings. In this review, we propose a novel framework for the holistic and interdisciplinary investigation of zoonotic disease emergence and its drivers, using the spillover of bat pathogens as a case study. This study has been developed to gain a detailed interdisciplinary understanding, and it combines cutting-edge perspectives from both natural and social sciences, linked to policy impacts on public health, land use and conservation.
doi:10.1098/rstb.2012.0228
PMCID: PMC3427567  PMID: 22966143
bat; zoonosis; emergence; collaborative framework

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