Mortality trajectory analysis reveals the drivers of sex-specific epidemiology in natural wildlife-disease interactions (original) (raw)

Multi-state modelling reveals sex-dependent transmission, progression and severity of tuberculosis in wild badgers

Epidemiology and Infection, 2013

SUMMARYStatistical models of epidemiology in wildlife populations usually consider diseased individuals as a single class, despite knowledge that infections progress through states of severity. Bovine tuberculosis (bTB) is a serious zoonotic disease threatening the UK livestock industry, but we have limited understanding of key epidemiological processes in its wildlife reservoirs. We estimated differential survival, force of infection and progression in disease states in a population of Eurasian badgers (Meles meles), naturally infected with bTB. Our state-dependent models overturn prevailing categorizations of badger disease states, and find novel evidence for early onset of disease-induced mortality in male but not female badgers. Males also have higher risk of infection and more rapid disease progression which, coupled with state-dependent increases in mortality, could promote sex biases in the risk of transmission to cattle. Our results reveal hidden complexities in wildlife dis...

The effects of bovine tuberculosis (Mycobacterium bovis) on mortality in a badger (Meles meles) population in England

Journal of Zoology, 2000

The mortality rates of badgers Meles meles were estimated, using data from a long-term capture±mark± recapture study of an undisturbed badger population in south-west England. Two life table methods were used: fusion and discounting. Badgers were allocated to a particular TB status for all or part of their lives according to their degree of infection with bovine tuberculosis Mycobacterium bovis. Separate life tables were created for animals with each TB status, and for males and females, and the estimated mortality rates were compared statistically. The progression of M. bovis infection, and the positions of M. bovis lesions were also analysed. The main ®ndings are: (a) uninfected male badgers have a signi®cantly higher mortality rate than uninfected females, (b) infected badgers which are not excreting M. bovis do not have a signi®cantly higher mortality rate than uninfected badgers, (c) badgers which are excreting M. bovis have a much higher mortality rate than uninfected badgers, (d) male badgers appear to cope with M. bovis infection less well than females, and (e) there may be sex differences in the mode of spread of M. bovis in badgers.

Modelling bovine tuberculosis in badgers in England: preliminary results

Mammalia, 1995

Bovine tuberculosis (TB) appears to be endemic within the badger population of southwest England. The total number of cattle herds with confirmed tuberculosis has increased from 197 in 1992 to 320 in 1993, and the badger is believed to be responsible for many of these breakdowns. Data on a high density badger population naturally infected with tuberculosis have been collected since the late 1970s. This paper presents some of the results of this epidemiological study and shows how localised the disease has been over a number of years. We also describe a number of models that have been used to help understand the progression of the disease within the population. These are simple, within-group infection models used primarily to help to understand the disease dynamics. The option to add vaccination, or restructure the model for other species, such as possums is always available. The results suggest that TB would only be sustained for long periods in social groups with about eight or more members, and that disease spread does not correspond to classical epidemiological models. Resume.-La tuberculose bovine (TB) apparait etre endemique chez les blaireaux du sudouest de l'Angleterre. Le nombre total de troupeaux de betail avec une tuberculose confirmee s'est accru de 197 en 1992 ä 320 en 1993, et le blaireau est considere comme responsable de beaucoup de ces cas. Des donnees concernant une population ä haute densite de blaireaux naturellement infectes par la tuberculose ont etc collectees depuis les annees 1970. Cette note presente certains des resultats de cette etude epidemiologique et montre combien la maladie a etc localisee pendant un certain nombre d'annees. Nous decrivons aussi un certain nombre de modeles qui ont etc utilises pour aider a la comprehension de la progression de la maladie dans la population. Ceux-ci sont des modeles simples d'infection intra-groupe, utilises pour aider ä la comprehension de la dynamique de la maladie. L'option d'ajouter la vaccination, ou de restructurer le modele pour d'autres especes, comme les opossums, est possible. Les resultats suggerent que la tuberculose se maintiendrait longtemps dans des groupes sociaux d'environ huit membres, et que la dispersion de la maladie ne correspond pas a des modeles epidemiologiques classiques.

Novel coupling of individual-based epidemiological and demographic models predicts realistic dynamics of tuberculosis in alien buffalo

1. Increasing sophistication of population viability analysis has broadened our capacity to model population change while accounting for system complexity and uncertainty. However, many emergent properties of population dynamics, such as the coupling of demographic processes with transmission and spread of disease, are still poorly understood. 2. We combined an individual-based demographic (Vortex) and epidemiological (Outbreak) model using a novel command-centre module (MetaModel Manager) to predict the progression of bovine tuberculosis in introduced swamp buffalo Bubalus bubalis in northern Australia and validated the model with data from a large-scale disease-monitoring and culling programme. We also assessed the capacity to detect disease based on incrementing sentinel (randomly sampled individuals) culling rates. 3. We showed that even high monitoring effort (1000 culled sentinels) has a low (<10%) probability of detecting the disease, and current sampling is inadequate. 4. Testing proportional and stepped culling rates revealed that up to 50% of animals must be killed each year to reduce disease prevalence to near-eradication levels. 5. Sensitivity analysis indicated that prevalence depended mainly on population demography (e.g. female age at primiparity) and the additional mortality induced by disease, with only minor contributions from epidemiological characteristics such as probability of transmission and encounter rate. This is a useful finding because the disease parameters are the least well known. 6. Synthesis and applications. Our models suggest that details of population demography should be incorporated into epidemiological models to avoid extensive bias in predictions of disease spread and effectiveness of control. Importantly, we demonstrate that low detection probabilities challenge the effectiveness of existing disease-monitoring protocols in northern Australia. The command-centre module we describe linking demographic and epidemiological models provides managers with the tools necessary to make informed decisions regarding disease management.

Demographic buffering and compensatory recruitment promotes the persistence of disease in a wildlife population

Ecology letters, 2016

Demographic buffering allows populations to persist by compensating for fluctuations in vital rates, including disease-induced mortality. Using long-term data on a badger (Meles meles Linnaeus, 1758) population naturally infected with Mycobacterium bovis, we built an integrated population model to quantify impacts of disease, density and environmental drivers on survival and recruitment. Badgers exhibit a slow life-history strategy, having high rates of adult survival with low variance, and low but variable rates of recruitment. Recruitment exhibited strong negative density-dependence, but was not influenced by disease, while adult survival was density independent but declined with increasing prevalence of diseased individuals. Given that reproductive success is not depressed by disease prevalence, density-dependent recruitment of cubs is likely to compensate for disease-induced mortality. This combination of slow life history and compensatory recruitment promotes the persistence of...

A Bayesian analysis of a Test and Vaccinate or Remove study to control bovine tuberculosis in badgers (Meles meles)

PLOS ONE, 2021

A novel five year Test and Vaccinate or Remove (TVR) wildlife research intervention project in badgers (Meles meles)commenced in 2014 in a 100km2area of Northern Ireland. It aimed to increase the evidence base around badgers and bovine TB and help create well-informed and evidence-based strategies to address the issue of cattle-to-cattle spread and spread between cattle and badgers. It involved real-time trap-side testing of captured badgers and vaccinating those that tested negative for bTB (BadgerBCG–BCG Danish 1331) and removal of those that tested bTB positive using the Dual-Path Platform VetTB test (DPP) for cervids (Chembio Diagnostic Systems, Medford, NY USA). Four diagnostic tests were utilised within the study interferon gamma release assay (IGRA), culture (clinical samples and post mortem), DPP using both whole blood and DPP using serum. BCG Sofia (SL222) was used in the final two years because of supply issues with BadgerBCG. Objectives for this study were to evaluate the...

Estimating the risk of cattle exposure to tuberculosis posed by wild deer relative to badgers in England and Wales

2009

Wild deer populations in Great Britain are expanding in range and probably in numbers, and relatively high prevalence of bovine tuberculosis (bTB, caused by infection with Mycobacterium bovis) in deer occurs locally in parts of southwest England. To evaluate the M. bovis exposure risk posed to cattle by wild deer relative to badgers in England and Wales, we constructed and parameterized a quantitative risk model with the use of information from the literature (on deer densities, activity patterns, bTB epidemiology, and pathology) and contemporary data on deer, cattle, and badger (Meles meles) distribution and abundance. The median relative risk score for each of the four deer species studied-red (Cervus elaphus), fallow (Dama dama), and roe (Capreolus capreolus) deer, and muntjac (Muntiacus reevesi)-was lower than unity (the relative risk set for badgers, the putative main wildlife reservoir of M. bovis in England and Wales). However, the 95th percentiles associated with risk estimates were large, and the upper limits for all four deer species exceeded unity. Although M. bovis exposure risks to cattle from deer at pasture are likely to be lower than those from badgers across most areas of England and Wales where cattle are affected by bTB because these areas coincide with high-density badger populations but not high-density deer populations, we predict the presence of localized areas where relative risks posed by deer may be considerable. Moreover, wherever deer are infected, risks to cattle may be additive to those posed by badgers. There are considerable knowledge gaps associated with bTB in deer, badgers, and cattle, and data available for model parameterization were generally of low quality and high variability, and consequently model output were subject to some uncertainty. Improved estimates of the proportion of time that deer of each species spend at pasture, the likelihood and magnitude of M. bovis excretion, and local badger and deer densities appear most important for improving estimates of relative risk in this system.

Herd-level bovine tuberculosis risk factors: assessing the role of low-level badger population disturbance

Scientific Reports, 2015

Bovine TB (bTB) is endemic in Irish cattle and has eluded eradication despite considerable expenditure, amid debate over the relative roles of badgers and cattle in disease transmission. Using a comprehensive dataset from Northern Ireland (>10,000 km 2 ; 29,513 cattle herds), we investigated interactions between host populations in one of the first large-scale risk factor analyses for new herd breakdowns to combine data on both species. Cattle risk factors (movements, international imports, bTB history, neighbours with bTB) were more strongly associated with herd risk than arealevel measures of badger social group density, habitat suitability or persecution (sett disturbance). Highest risks were in areas of high badger social group density and high rates of persecution, potentially representing both responsive persecution of badgers in high cattle risk areas and effects of persecution on cattle bTB risk through badger social group disruption. Average badger persecution was associated with reduced cattle bTB risk (compared with high persecution areas), so persecution may contribute towards sustaining bTB hotspots; findings with important implications for existing and planned disease control programmes.

Investigating the spatial dynamics of bovine tuberculosis in badger populations: evaluating an individual-based simulation model

Ecological Modelling, 2003

We describe an individual-based spatially-explicit model designed to investigate the dynamics of badger populations and TB epidemiology in a real landscape. We develop a methodology for evaluating the sensitivity of the model to its input parameters through the use of power analysis, partial correlation coefficients and binary logistic regression. This novel approach to sensitivity analysis provides a formal statement of confidence in our findings based on statistical power, and a solution for analysing sparse data sets of disease prevalence. The sensitivity analysis revealed that the simulated badger population size after 20 years was most dependent on five parameters affecting female recruitment (probability of breeding, mortality of adult females in the first half of the year, mortality of juvenile females in the second half of the year and mortality of female cubs in the both halves of the year). The simulated prevalence of TB was most affected by the population size, the rate at which infectious badgers transmit the disease to other members of their social group, and the rate at which the disease is spread outside of the social group.

The spatio-temporal distribution of Mycobacterium bovis (bovine tuberculosis) infection in a high-density badger population

Journal of Animal Ecology, 2000

1. The European badger (Meles meles) is implicated as a reservoir of Mycobacterium bovis (bovine TB) infection for cattle in Britain and Ireland. In the present study the spatio-temporal distribution of M. bovis infection was investigated. Analyses were carried out on data from a long-term epidemiological and ecological study of the dynamics of bovine TB in a wild population of badgers at Woodchester Park in south-west England. 2. During the 15 years of the capture±mark±recapture study (1982±96), 3316 trapping and post-mortem records were obtained from 1270 individual badgers. Annual prevalence of infection based on positive serological and bacterial tests varies between 10Á3% and 17Á7% of the population. 3. Infection was aggregated in social groups in the west of the study area, con®rming the ®ndings of previous studies. However, temporal trends in disease were not synchronized amongst neighbouring groups, suggesting low rates of disease transfer between them. 4. There was signi®cant serial correlation in the disease status within groups over time, suggesting that infection persists for many years in some social groups. The presence of infectious adult female badgers in groups was associated with new infections, and provides further evidence for their importance in the maintenance of infection within groups. However, no statistically signi®cant correlations were detected between the demographic characteristics of social groups and group infection status. 5. The distribution of disease re¯ects stable persistent foci of infection in the badger population, with limited evidence of transfer between social groups. The accurate identi®cation of stable foci of infection would allow a range of management strategies for the control of bovine TB to be eciently targeted in such populations. However, the extent to which this pattern of infection is representative of low-density and disturbed badger populations is unknown.