Experimental assessment of cross-species transmission in a natural multihost-multivector-multipathogen community.

Vector-borne pathogens, many of which cause major suffering worldwide, often circulate in diverse wildlife communities comprising multiple reservoir host and/or vector species. However, the complexities of these systems make it challenging to determine the contributions these different species make to transmission. We experimentally manipulated transmission within a natural multihost-multipathogen-multivector system, by blocking flea-borne pathogen transmission from either of two co-occurring host species (bank voles and wood mice). Through genetic analysis of the resulting infections in the hosts and vectors, we show that both host species likely act together to maintain the overall flea community, but cross-species pathogen transmission is relatively rare-most pathogens were predominantly found in only one host species, and there were few cases where targeted treatment affected pathogens in the other host species. However, we do provide experimental evidence of some reservoir-spillover dynamics whereby reductions of some infections in one host species are achieved by blocking transmission from the other host species. Overall, despite the apparent complexity of such systems, we show there can be 'covert simplicity', whereby pathogen transmission is primarily dominated by single host species, potentially facilitating the targeting of key hosts for control, even in diverse ecological communities.

A systematized review and qualitative synthesis of potential risk factors associated with the occurrence of non-O157 Shiga toxin-producing Escherichia coli (STEC) in the primary production of cattle.

Human infection with Shiga toxin-producing Escherichia coli (STEC) causes an estimated 2.8 million cases of acute illness worldwide each year. Serogroup O157 is the most commonly diagnosed STEC in humans, but cases linked to non-O157 STEC serogroups have increased recently due to increased surveillance and improvements to detection methods. Cattle are an important reservoir for STEC O157 and the same may be true for non-O157 STEC; therefore, reducing the occurrence of these pathogens in cattle could mitigate human infection risk. A systematized literature review of articles published within the Scopus database since 2010 (employing a partially systematic approach) was therefore conducted followed by qualitative synthesis of evidence to provide a structured overview of potential risk factors for non-O157 STEC in primary cattle production. Overall, few relevant studies were identified (n = 22), highlighting that more studies are needed. Consistently significant associations were only identified with respect to cattle age (broadly higher rate of isolation from young animals compared to adults) and season of sampling (generally increased isolation of non-O157 STEC in summer). However, wide variation in study designs, including notable differences in laboratory detection methods, means drawing more general conclusions is currently not possible based on the results of this review. However, it is likely that the development of more sensitive methods for non-O157 STEC detection in potential livestock reservoirs and increased standardization across statistically sound epidemiological investigations are required to identify pertinent risk factors.

Multihost Bartonella parasites display covert host specificity even when transmitted by generalist vectors.

Many parasites infect multiple sympatric host species, and there is a general assumption that parasite transmission between co-occurring host species is commonplace. Such between-species transmission could be key to parasite persistence within a disease reservoir and is consequently an emerging focus for disease control. However, while a growing body of theory indicates the potential importance of between-species transmission for parasite persistence, conclusive empirical evidence from natural communities is lacking, and the assumption that between-species transmission is inevitable may therefore be wrong. We investigated the occurrence of between-species transmission in a well-studied multihost parasite system. We identified the flea-borne Bartonella parasites infecting sympatric populations of Apodemus sylvaticus (wood mice) and Myodes glareolus (bank voles) in the UK and confirmed that several Bartonella species infect both rodent species. However, counter to previous knowledge, genetic characterization of these parasites revealed covert host specificity, where each host species is associated with a distinct assemblage of genetic variants, indicating that between-species transmission is rare. Limited between-species transmission could result from rare encounters between one host species and the parasites infecting another and/or host-parasite incompatibility. We investigated the occurrence of such encounter and compatibility barriers by identifying the flea species associated with each rodent host, and the Bartonella variants carried by individual fleas. We found that the majority of fleas were host-generalists but the assemblage of Bartonella variants in fleas tended to reflect the assemblage of Bartonella variants in the host species they were collected from, thus providing evidence of encounter barriers mediated by limited between-species flea transfer. However, we also found several fleas that were carrying variants never found in the host species from which they were collected, indicating some degree of host-pathogen incompatibility when barriers to encounter are overcome. Overall, these findings challenge our default perceptions of multihost parasite persistence, as they show that despite considerable overlaps in host species ecology, separate populations of the same parasite species may circulate and persist independently in different sympatric host species. This questions our fundamental understanding of endemic transmission dynamics and the control of infection within natural reservoir communities.

Difference in differences analysis evaluates the effects of the badger control policy on bovine tuberculosis in England.

Persistent tuberculosis (TB) in cattle populations in England has been associated with an exchange of infection with badgers (Meles meles). A badger control policy (BCP) commenced in 2013. Its aim was to decrease TB incidence in cattle by reducing the badger population available to provide a wildlife reservoir for bovine TB. Monitoring data from 52 BCP intervention areas 200-1600 km2 in size, starting over several years, were used to estimate the change in TB incidence rate in cattle herds, which was associated with time since the start of the BCP in each area. A difference in differences analysis addressed the non-random selection and starting sequence of the areas. The herd incidence rate of TB reduced by 56% (95% Confidence Interval 41-69%) up to the fourth year of BCP interventions, with the largest drops in the second and third years. There was insufficient evidence to judge whether the incidence rate reduced further beyond 4 years. These estimates are the most precise for the timing of declines in cattle TB associated with interventions primarily targeting badgers. They are within the range of previous estimates from England and Ireland. This analysis indicates the importance of reducing transmission from badgers to reduce the incidence of TB in cattle, noting that vaccination of badgers, fertility control and on farm biosecurity may also achieve this effect.

Study of Animal Mixing and the Dynamics of Hepatitis E Virus Infection on a Farrow-to-Finish Pig Farm.

In Europe, swine are a livestock reservoir for Hepatitis E virus genotype 3 (HEV-3). Consumption of food containing HEV-3 can cause zoonotic human infection, though risk is reduced by heat treatment. Implementing controls that limit infection in slaughter pigs may further reduce foodborne transmission risk but knowledge of infection dynamics on commercial farms is limited. This study addressed this knowledge gap and in particular investigated the influence of group mixing. Faeces were collected from grower (n = 212) and fattener (n = 262) pigs on a farrow-to-finish farm on four occasions. HEV RNA was detected on all occasions, and prevalence was higher in growers (85.8%) than fatteners (26.0%; p < 0.001). HEV-positive samples were also collected from the wider farm environment (n = 67; 64.7% prevalence), indicating potential sources for HEV re-circulation within the herd. Timing of infection in a cohort was also investigated. HEV was absent from all piglet faeces (n = 98) and first detected at weaner stage (25.7% prevalence), but only in groups weaned earlier or comprising pigs from many different litters. Farrowing sow faeces (n = 75) were HEV-negative but antibodies were detected in blood from two sows. Results suggest that multiple factors influence HEV infection dynamics on pig farms, and potential foci for further study into practical control solutions are highlighted.

In-depth farm investigations and an exploratory risk factor analysis for the presence of Salmonella on broiler farms in Great Britain.

Salmonella is a major cause of foodborne illness across Europe but there has been little recent research on its control in broiler production in Great Britain. Investigations of Salmonella presence on 20 broiler farms and a separate exploratory risk factor analysis involving 36 Salmonella-positive farms and 22 Salmonella-negative farms were carried out to investigate Salmonella contamination and control on broiler farms in Great Britain. Sources of Salmonella persistence on farm and potential risk factors for on-farm contamination were identified, enabling provision of up-to-date advice on Salmonella control to farmers. Twenty broiler farms across England and Wales were intensively sampled over time. Most farms were included in the study after routine testing as part of the Salmonella National Control Programmes (NCPs) identified regulated Salmonella serovars or potential associations with outbreak cases of significance for human health. Across all farms and visits, the highest proportion of Salmonella-positive samples were from areas exterior to broiler houses compared to anterooms or house interiors. Exterior Salmonella-positive samples were primarily collected from the immediate areas around the houses, with the highest proportions being from drainage, farm tracks/driveways, and pooled water. Elimination of Salmonella was variable but was most successful inside affected houses (compared to exterior areas) and for regulated Salmonella serovars under the Salmonella NCPs and high priority Salmonella strains with multi-drug resistances. It is likely that the financial and reputational concerns associated with regulated Salmonella serovars and those of greater public health significance underlie the reason that these serovars were more effectively controlled at farm level, as effective elimination of Salmonella can involve a considerable investment in infrastructure, time and resources. Without perceived direct benefits in eliminating non-regulated Salmonella serovars at farm level it can be challenging to maintain the required motivation and investment. A separate farm-level risk factor analysis was carried out using data collected from 58 broiler farms representing six GB broiler companies. Risk of testing positive for Salmonella via NCP sampling in the previous year was greater in the absence of house-specific anterooms and if at least some poultry houses were surrounded by soil/grass compared to if all were surrounded by concrete or a mixture of concrete and stones/gravel. Odds of testing positive for Salmonella in the previous year was also greater for farms whose maximum holding capacity was >100,000 birds, and farms where the usual number of visitors per day was 0-1 compared to 2-3. The analysis was exploratory and caution is required with interpretation, but results provide preliminary insight into aspects of farm management that may be important, practicable targets for Salmonella control on broiler farms in GB.

Risk factor analysis for Salmonella contamination of broiler chicken (Gallus gallus) hatcheries in Great Britain.

Salmonellosis is the second most commonly reported zoonosis in the European Union and contaminated meat from broiler chickens (Gallus gallus) is an important source of human infection. In Great Britain (GB), prevalence of Salmonella enterica in broiler flocks is low, having declined considerably since the introduction of the Salmonella National Control Programme in 2010. However, this decreasing trend has stabilised in recent years and serovars with known ability to persistently colonise hatcheries have been isolated from broiler flocks with increasing frequency, indicating that further controls on hatchery contamination are required. The broiler industry in GB has changed dramatically over the last 15 years, with greater intensification and dominance by a small number of very large companies which rely on relatively few hatcheries. An investigation of risk factors for Salmonella contamination in GB broiler hatcheries was therefore carried out so that relevant up-to-date advice on Salmonella control can be provided. Twenty-two hatcheries, representing most commercial scale GB broiler hatcheries, were visited between 2015 and 2018. Salmonella contamination was comprehensively investigated at each hatchery by collecting between 108 and 421 environmental swab samples per hatchery (6990 samples in total from all hatcheries). An in-depth questionnaire on hatchery operations was completed for each hatchery, and results were incorporated into a risk factor analysis (univariable followed by multivariable mixed effects logistic regression) to identify factors associated with Salmonella occurrence. Overall, 6.0 % (416/6990) of environmental samples were Salmonella-positive and Salmonella was isolated from 17/22 hatcheries. Ten different serovars were isolated, the most common being S. Senftenberg and S. Mbandaka which are known hatchery colonisers. Sixty-four risk factor variables were investigated. Twenty-two of these were initially retained based on univariable analyses (p ≤ 0.25) and six were ultimately left in the final multivariable model (p ≤ 0.05). Salmonella detection was positively associated with having ≥30 hatchers in regular use compared to fewer (Odds ratio [OR] 23.7, 95 % confidence interval [CI] 6.7-84.2), storing trays in process rooms (OR 28.8, CI 7.8-106.3), drying set-up trolleys in corridors (OR 15.6, CI 5.9-41.4) and having skips located in enclosed areas (OR 8.99, CI 5.89-41.35). Using a closed waste disposal system was negatively associated with Salmonella detection (OR 0.08, CI 0.04-0.18) and the odds of detecting Salmonella in hatcheries with 31-60 total workers was lower compared to hatcheries with ≤30 staff (OR 0.16, CI 0.06-0.40). Despite the complexities of hatchery enterprises, changes to a relatively small number of features may significantly reduce the occurrence of hatchery contamination.