Laura A. Hughes

Emerging Infectious Disease Leads to Rapid Population Declines of Common British Birds

Emerging infectious diseases are increasingly cited as threats to wildlife, livestock and humans alike. They can threaten geographically isolated or critically endangered wildlife populations; however, relatively few studies have clearly demonstrated the extent to which emerging diseases can impact populations of common wildlife species. Here, we report the impact of an emerging protozoal disease on British populations of greenfinch Carduelis chloris and chaffinch Fringilla coelebs, two of the most common birds in Britain. Morphological and molecular analyses showed this to be due to Trichomonas gallinae. Trichomonosis emerged as a novel fatal disease of finches in Britain in 2005 and rapidly became epidemic within greenfinch, and to a lesser extent chaffinch, populations in 2006. By 2007, breeding populations of greenfinches and chaffinches in the geographic region of highest disease incidence had decreased by 35% and 21% respectively, representing mortality in excess of half a million birds. In contrast, declines were less pronounced or absent in these species in regions where the disease was found in intermediate or low incidence. Also, populations of dunnock Prunella modularis, which similarly feeds in gardens, but in which T. gallinae was rarely recorded, did not decline. This is the first trichomonosis epidemic reported in the scientific literature to negatively impact populations of free-ranging non-columbiform species, and such levels of mortality and decline due to an emerging infectious disease are unprecedented in British wild bird populations. This disease emergence event demonstrates the potential for a protozoan parasite to jump avian host taxonomic groups with dramatic effect over a short time period.

Characterisation of Salmonella enterica serotype Typhimurium isolates from wild birds in northern England from 2005 – 2006

BackgroundSeveral studies have shown that a number of serovars of Salmonella enterica may be isolated from wild birds, and it has been suggested that wild birds may play a role in the epidemiology of human and livestock salmonellosis. However, little is known about the relationship between wild bird S. enterica strains and human- and livestock- associated strains in the United Kingdom. Given the zoonotic potential of salmonellosis, the main aim of this study was to investigate the molecular epidemiology of S. enterica infections in wild birds in the north of England and, in particular, to determine if wild bird isolates were similar to those associated with disease in livestock or humans.ResultsThirty two Salmonella enterica isolates were collected from wild birds in northern England between February 2005 and October 2006, of which 29 were S. enterica serovar Typhimurium (S. Typhimurium); one S. Newport, one S. Senftenberg, and one isolate could not be classified by serotyping. Further analysis through phage typing and macro-restriction pulsed-field gel electrophoresis indicated that wild passerine deaths associated with salmonellosis were caused by closely-related S. Typhimurium isolates, some of which were clonal. These isolates were susceptible to all antimicrobials tested, capable of invading and persisting within avian macrophage-like HD11 cells in vitro, and contained a range of virulence factors associated with both systemic and enteric infections of birds and mammals. However, all the isolates lacked the sopE gene associated with some human and livestock disease outbreaks caused by S. Typhimurium.ConclusionThe wild bird isolates of S. enterica characterised in this investigation may not represent a large zoonotic risk. Molecular characterisation of isolates suggested that S. Typhimurium infection in wild passerines is maintained within wild bird populations and the causative strains may be host-adapted.

Molecular Epidemiology and Characterization of Campylobacter spp. Isolated from Wild Bird Populations in Northern England

ABSTRACT Campylobacter infections have been reported at prevalences ranging from 2 to 50% in a range of wild bird species, although there have been few studies that have investigated the molecular epidemiology of Campylobacter spp. Consequently, whether wild birds are a source of infection in humans or domestic livestock or are mainly recipients of domestic animal strains and whether separate cycles of infection occur remain unknown. To address these questions, serial cross-sectional surveys of wild bird populations in northern England were carried out over a 2-year period. Fecal samples were collected from 2,084 wild bird individuals and screened for the presence of Campylobacter spp. A total of 56 isolates were recovered from 29 birds sampled at 15 of 167 diverse locales. Campylobacter jejuni, Campylobacter lari, and Campylobacter coli were detected by PCR, and the prevalences of different Campylobacter spp. in different avian families ranged from 0% to 33%. Characterization of 36 C. jejuni isolates by multilocus sequence typing revealed that wild birds carry both livestock-associated and unique strains of C. jejuni. However, the apparent absence of unique wild bird strains of C. jejuni in livestock suggests that the direction of infection is predominantly from livestock to wild birds. C. lari was detected mainly in wild birds sampled in an estuarine or coastal habitat. Fifteen C. lari isolates were analyzed by macrorestriction pulsed-field gel electrophoresis, which revealed genetically diverse populations of C. lari in Eurasian oystercatchers (Haematopus ostralegus) and clonal populations in magpies (Pica pica).

Genetically diverse coronaviruses in wild bird populations of northern England.

Infectious bronchitis virus (IBV) causes a costly respiratory viral disease of chickens. The role of wild birds in the epidemiology of IBV is poorly understood. We detected diverse coronaviruses by PCR in wildfowl and wading birds in England. Sequence analysis showed some viruses to be related to IBV.

A clonal strain of Trichomonas gallinae is the aetiologic agent of an emerging avian epidemic disease

Trichomonas gallinae is a protozoan parasite that is well characterised as a cause of trichomonosis in columbid and raptor species world-wide. The parasite emerged as a novel infection of British passerines in 2005, leading to epidemic mortality associated with significant declines of breeding populations of greenfinches (Carduelis chloris) and chaffinches (Fringilla coelebs). We characterised the extent of T. gallinae genotypic heterogeneity within the affected wild British avifauna by analysing individual isolates from 17 of the species affected. To do so, we employed improved platform-based multilocus typing tools as well as the hydrogenosomal Fe-hydrogenase gene as a single marker locus for fine-typing. We found no evidence of heterogeneity amongst the parasites infecting British passerines, indicating that a clonal strain of T. gallinae is the causative agent of this emerging infectious disease.

Antimicrobial prescribing practice in UK equine veterinary practice

REASONS FOR PERFORMING STUDY Antimicrobial use is known to select for the emergence of resistant strains of bacteria; therefore prudent use in both human and veterinary medicine is essential to preserve their efficacy. OBJECTIVES To characterise antimicrobial prescribing patterns in UK equine practice and evaluate factors associated with prescribing. METHODS A postal questionnaire including 4 clinical scenarios was sent to 740 veterinary surgeons that treat horses. Data were collected on the clinician, their practice and sources of information regarding antimicrobials and their use. Multivariable logistic regression analysis was used to ascertain factors associated with 5 outcomes; prescribing off-licence drugs; prescribing at incorrect doses; prescribing 3rd or 4th generation cephalosporins; prescribing fluoroquinolones and prescribing potentiated sulphonamides. RESULTS Questionnaires were completed by 38% of veterinary surgeons who were sent questionnaires. Less than 1% of practices had antimicrobial use guidelines. Trimethoprim-sulphonamides were most commonly prescribed in each clinical scenario. Eleven percent of prescriptions were for antimicrobial drugs not licensed for use in horses in the UK. Five percent of prescriptions for licensed antimicrobials were under the recommended dose rate and 56% over the recommended dose rate. Fluoroquinolones and 3rd and 4th generation cephalosporins accounted for 1 and 3% of prescriptions, respectively. Veterinary surgeons working at referral practices were more likely to prescribe 3rd and 4th generation cephalosporins and fluoroquinolones and off-licence antimicrobials whereas those working in first-opinion practices were more likely to prescribe potentiated sulphonamides. Sources of information regarding antimicrobials also had an effect on prescribing. CONCLUSIONS AND POTENTIAL RELEVANCE Prescription of antimicrobials at inappropriate doses was common even when provided with the weight of the animal. It is uncommon for UK equine veterinary practices to have guidelines for antimicrobial use. The introduction of such guidelines could lead to more prudent use of antimicrobials.

Pulsed-Field Gel Electrophoresis Supports the Presence of Host-Adapted Salmonella enterica subsp. enterica Serovar Typhimurium Strains in the British Garden Bird Population

ABSTRACT Salmonellosis is a frequently diagnosed infectious disease of passerine birds in garden habitats within Great Britain with potential implications for human and domestic animal health. Postmortem examinations were performed on 1,477 garden bird carcasses of circa 50 species from England and Wales, 1999 to 2007 inclusive. Salmonellosis was confirmed in 263 adult birds of 10 passerine species in this 11-year longitudinal study. A subset of 124 fully biotyped Salmonella enterica subsp. enterica serovar Typhimurium isolates was examined using pulsed-field gel electrophoresis to investigate the hypothesis that these strains are host adapted and to determine whether this molecular technique offers greater resolution in understanding the epidemiology of Salmonella Typhimurium infection than phage typing alone. For the two most common phage types, definitive type (DT) 40 and DT56v, which together accounted for 97% (120/124) of isolates, pulsed-field gel electrophoresis groupings closely correlated with phage type with remarkably few exceptions. A high degree of genetic similarity (>90%) was observed within and between the two most common pulsed-field gel electrophoresis groups. No clustering or variation was found in the pulsed-field gel electrophoresis groupings by bird species, year, or geographical region beyond that revealed by phage typing. These findings support the hypothesis that there are currently two host-adapted Salmonella phage types, S. Typhimurium DT40 and DT56v, circulating widely in British garden birds and that the reservoir of infection is maintained within wild bird populations. Large-scale multilocus sequence typing studies are required to further investigate the epidemiology of this infection.

Evidence of Spread of the Emerging Infectious Disease, Finch Trichomonosis, by Migrating birds

Finch trichomonosis emerged in Great Britain in 2005 and led to epidemic mortality and a significant population decline of greenfinches, Carduelis chloris and chaffinches, Fringilla coelebs, in the central and western counties of England and Wales in the autumn of 2006. In this article, we show continued epidemic spread of the disease with a pronounced shift in geographical distribution towards eastern England in 2007. This was followed by international spread to southern Fennoscandia where cases were confirmed at multiple sites in the summer of 2008. Sequence data of the ITS1/5.8S/ITS2 ribosomal region and part of the small subunit (SSU) rRNA gene showed no variation between the British and Fennoscandian parasite strains of Trichomonas gallinae. Epidemiological and historical ring return data support bird migration as a plausible mechanism for the observed pattern of disease spread, and suggest the chaffinch as the most likely primary vector. This finding is novel since, although intuitive, confirmed disease spread by migratory birds is very rare and, when it has been recognised, this has generally been for diseases caused by viral pathogens. We believe this to be the first documented case of the spread of a protozoal emerging infectious disease by migrating birds.

Cross-sectional survey of antimicrobial prescribing patterns in UK small animal veterinary practice

The increase in the prevalence of antimicrobial resistance has resulted in both human and veterinary antimicrobial use coming under increased scrutiny. The aim of this study was to characterise antimicrobial prescribing patterns in small-animal veterinary practices in the UK. A cross-sectional survey of UK small animal veterinarians was undertaken. A postal questionnaire to evaluate antimicrobial prescribing habits was sent to 900 clinicians. Data were collected on the clinicians, their practices and their sources of information regarding antimicrobials and their use. Respondents were asked if they would prescribe antimicrobials to animals described in four clinical scenarios, and, if so, to provide details of the prescription(s). Questionnaires were completed by 51% of the veterinarians. Only 3.5% of clinicians reported that their practice had an antimicrobial use policy. Penicillins were most commonly prescribed in three clinical scenarios, and 1st generation cephalosporins were most commonly prescribed in a scenario about canine pyoderma. In one scenario, fluoroquinolones and 3rd generation cephalosporins accounted for 10% and 13% of prescriptions respectively. Five percent of all prescriptions were under the recommended dose and 20% were over the recommended dose. Overall, 2.3% of prescriptions were not licensed for use in dogs or cats in the UK. Associations between the use of various antimicrobial drugs and independent variables were analysed using multivariable logistic regression models. Off-license prescriptions and inaccurate dosing of antimicrobials by small-animal clinicians in the UK appears to occur. Antimicrobial use guidelines are rare in small animal practice. The introduction of such guidelines has been shown to lead to more appropriate use of antimicrobials and is therefore recommended.

Risk factors for the use of prescription antibiotics on UK broiler farms

OBJECTIVES Despite growing concerns about the emergence of antibiotic-resistant strains of bacteria, little work has been carried out to investigate reasons for prescription antibiotic use in UK farming systems. We carried out a nationwide survey of broiler farms to determine risk factors for the use of prescription antibiotics. METHODS A cross-sectional questionnaire-based survey of UK broiler farms was undertaken covering flock placement dates from July 2002 until July 2003 and was based on information concerning 54% of the national broiler population reared on 497 farms. Data were collected on all aspects of broiler production and multivariable logistic regression analyses were performed to determine risk factors for two dependent variables; therapeutic and preventive use of antibiotics. RESULTS The major indications for the use of antibiotics for therapeutic purposes were enteric and respiratory disease, the strongest association being with the occurrence of necrotic enteritis. No direct association was found between the use of antibiotics for preventive purposes and disease. Multivariable logistic regression analysis indicated that the main drivers for the use of antibiotics for disease prevention may be poultry company disease prevention policies and farm management practices. CONCLUSIONS With increasing restrictions on the use of antibiotics in food-producing animals, research efforts need to be focused on the epidemiology of enteric and respiratory disease in poultry. The cost of disease to the broiler industry is great, resulting in the use of antibiotics for preventive purposes to safeguard against large financial losses. More research into alternative disease control measures is required.