Barend M. deC. Bronsvoort

Animal movements and the spread of infectious diseases

Domestic and wild animal population movements are important in the spread of disease. There are many recent examples of disease spread that have occurred as a result of intentional movements of livestock or wildlife. Understanding the volume of these movements and the risks associated with them is fundamental in elucidating the epidemiology of these diseases, some of which might entail zoonotic risks. The importance of the worldwide animal trade is reviewed and the role of the unregulated trade in animals is highlighted. A range of key examples are discussed in which animal movements have resulted in the introduction of pathogens to previously disease-free areas. Measures based on heightened surveillance are proposed that mitigate the risks of new pathogen introductions.

A framework for evaluating animals as sentinels for infectious disease surveillance

The dynamics of infectious diseases are highly variable. Host ranges, host responses to pathogens and the relationships between hosts are heterogeneous. Here, we argue that the use of animal sentinels has the potential to use this variation and enable the exploitation of a wide range of pathogen hosts for surveillance purposes. Animal sentinels may be used to address many surveillance questions, but they may currently be underused as a surveillance tool and there is a need for improved interdisciplinary collaboration and communication in order to fully explore the potential of animal sentinels. In different contexts, different animal hosts will themselves vary in their capacity to provide useful information. We describe a conceptual framework within which the characteristics of different host populations and their potential value as sentinels can be evaluated in a broad range of settings.

Serological Patterns of Brucellosis, Leptospirosis and Q Fever in Bos indicus Cattle in Cameroon

Brucellosis, leptospirosis and Q fever are important infections of livestock causing a range of clinical conditions including abortions and reduced fertility. In addition, they are all important zoonotic infections infecting those who work with livestock and those who consume livestock related products such as milk, producing non-specific symptoms including fever, that are often misdiagnosed and that can lead to severe chronic disease. This study used banked sera from the Adamawa Region of Cameroon to investigate the seroprevalences and distributions of seropositive animals and herds. A classical statistical and a multi-level prevalence modelling approach were compared. The unbiased estimates were 20% of herds were seropositive for Brucella spp. compared to 95% for Leptospira spp. and 68% for Q fever. The within-herd seroprevalences were 16%, 35% and 39% respectively. There was statistical evidence of clustering of seropositive brucellosis and Q fever herds. The modelling approach has the major advantage that estimates of seroprevalence can be adjusted for the sensitivity and specificity of the diagnostic test used and the multi-level structure of the sampling. The study found a low seroprevalence of brucellosis in the Adamawa Region compared to a high proportion of leptospirosis and Q fever seropositive herds. This represents a high risk to the human population as well as potentially having a major impact on animal health and productivity in the region.

Echinococcus granulosus infection in domestic dogs in urban and rural areas of the Coquimbo region, north-central Chile

Hydatidosis is a zoonotic disease caused by the cystic stage of the cestode parasite Echinoccocus granulosus, in which the definitive hosts are mainly domestic dogs. This parasite is regarded mainly as a rural disease, where man is exposed through contact with eggs excreted by definitive hosts; however, some studies have shown that domestic dogs can get infected within urban areas. This study was conducted to assess differences in prevalence of E. granulosus in urban and rural sites in Coquimbo region of Chile. From 2005 to 2006 a cross-sectional household questionnaire survey was conducted in Coquimbo and Ovalle cities, in three towns and in rural sites along two transects from these cities to the Fray Jorge NP in the Coquimbo region. Faecal samples were collected from dogs during the questionnaire survey and tested for Echinococcus coproantigens. Positive dogs were found in urban areas. Analysis of risk factors indicated that dogs inhabiting the borders of urban areas were at greater risk of being coproantigen positive than those in the centre of these areas. These results are likely to be related to the custom of slaughtering livestock at home in urban areas during local celebrations, which could favour the importation of E. granulosus to urban areas by acquiring livestock contaminated with cysts from rural sites. This study shows that surveillance and control measures in livestock and domestic dogs need to be introduced in urban areas as well as rural areas of the Coquimbo region to reduce the public health risk of hydatid disease.

Echinococcus granulosus infection in humans and livestock in the Coquimbo region, north-central Chile.

Cyst echinococcosis (CE) is one of the most important zoonosis in Chile, where studies have focussed mainly in moist southern regions. The present study was conducted to determine the prevalence of cystic echinococcosis (CE) in livestock and humans in the semiarid Coquimbo region in north-central Chile. A review of all surgical cases of CE in humans reported in the Elqui, Limarí and Choapa provinces in Coquimbo region for the period comprising 1995-2006 was obtained. In addition, a retrospective study of CE covering condemnation records from slaughterhouses of these provinces from the same period was carried out. The surgical incidence of CE in humans ranged between 2.3 and 8.5 cases per 10(5) people, with more cases reported in provinces with a higher percentage of rural inhabitants (Limarí and Choapa). A total of 174,034 cattle, 22,208 goats, 35,404 sheep, 25,355 swine and 9391 equines were examined during the period. Higher prevalence of CE was detected in cattle (24%), followed by swine (14%), sheep (11%), goats (6%), and equines (9%). More cases of CE in livestock were also found in provinces with higher rural population. The overall trend of the prevalence of CE for each livestock species across years was a significant downward one, except for swine in Elqui and sheep and swine in Choapa. Cattle showed higher prevalence of CE in liver in Elqui, in kidney in Limarí and in lungs in Choapa. Swine showed similar prevalence by organs in all provinces. Sheep showed higher prevalence of CE in liver in Elqui and Limarí and lower prevalence in Choapa. Goats presented higher prevalence of CE in kidney in all provinces, and equines had higher prevalence of CE in liver in the provinces where animals were slaughtered. Further studied are needed to assess whether these differences are due to different strains affecting these species or due to ecological factors. When analyzing the CE prevalence of each species within each province, a negative correlation between prevalence of CE in goats and rainfall in the Limarí province was found. This could be attributed to changes in management practices and/or ecological factors. This study shows that surveillance of CE at slaughterhouses combined with the analyses of incidence in humans can be used to detect areas with a higher risk of infection. Improvements in record-keeping of infected animals at slaughterhouses are proposed in order to trace back farms where infection was most likely acquired.

Implications of the cattle trade network in Cameroon for regional disease prevention and control

Movement of live animals is a major risk factor for the spread of livestock diseases and zoonotic infections. Understanding contact patterns is key to informing cost-effective surveillance and control strategies. In West and Central Africa some of the most rapid urbanization globally is expected to increase the demand for animal-source foods and the need for safer and more efficient animal production. Livestock trading points represent a strategic contact node in the dissemination of multiple pathogens. From October 2014 to May 2015 official transaction records were collected and a questionnaire-based survey was carried out in cattle markets throughout Western and Central-Northern Cameroon. The data were used to analyse the cattle trade network including a total of 127 livestock markets within Cameroon and five neighboring countries. This study explores for the first time the influence of animal trade on infectious disease spread in the region. The investigations showed that national borders do not present a barrier against pathogen dissemination and that non-neighbouring countries are epidemiologically connected, highlighting the importance of a regional approach to disease surveillance, prevention and control. Furthermore, these findings provide evidence for the benefit of strategic risk-based approaches for disease monitoring, surveillance and control, as well as for communication and training purposes through targeting key regions, highly connected livestock markets and central trading links.

Factors Associated with Acquisition of Human Infective and Animal Infective Trypanosome Infections in Domestic Livestock in Western Kenya

Background Trypanosomiasis is regarded as a constraint on livestock production in Western Kenya where the responsibility for tsetse and trypanosomiasis control has increasingly shifted from the state to the individual livestock owner. To assess the sustainability of these localised control efforts, this study investigates biological and management risk factors associated with trypanosome infections detected by polymerase chain reaction (PCR), in a range of domestic livestock at the local scale in Busia, Kenya. Busia District also remains endemic for human sleeping sickness with sporadic cases of sleeping sickness reported. Results In total, trypanosome infections were detected in 11.9% (329) out of the 2773 livestock sampled in Busia District. Multivariable logistic regression revealed that host species and cattle age affected overall trypanosome infection, with significantly increased odds of infection for cattle older than 18 months, and significantly lower odds of infection in pigs and small ruminants. Different grazing and watering management practices did not affect the odds of trypanosome infection, adjusted by host species. Neither anaemia nor condition score significantly affected the odds of trypanosome infection in cattle. Human infective Trypanosoma brucei rhodesiense were detected in 21.5% of animals infected with T. brucei s.l. (29/135) amounting to 1% (29/2773) of all sampled livestock, with significantly higher odds of T. brucei rhodesiense infections in T. brucei s.l. infected pigs (OR = 4.3, 95%CI 1.5-12.0) than in T. brucei s.l. infected cattle or small ruminants. Conclusions Although cattle are the dominant reservoir of trypanosome infection it is unlikely that targeted treatment of only visibly diseased cattle will achieve sustainable interruption of transmission for either animal infective or zoonotic human infective trypanosomiasis, since most infections were detected in cattle that did not exhibit classical clinical signs of trypanosomiasis. Pigs were also found to be reservoirs of infection for T. b. rhodesiense and present a risk to local communities.

Repeated high doses of avermectins cause prolonged sterilisation, but do not kill, Onchocerca ochengi adult worms in African cattle

Background Ivermectin (Mectizan™, Merck and CO. Inc.) is being widely used in the control of human onchocerciasis (Onchoverca volvulus) because of its potent effect on microfilariae. Human studies have suggested that, at the standard dose of 150 μg/kg an annual treatment schedule of ivermectin reversibly interferes with female worm fertility but is not macrofilaricidal. Because of the importance of determining whether ivermectin could be macrofilaricidal, the efficacy of high and prolonged doses of ivermectin and a related avermectin, doramectin, were investigated in cattle infected with O. ochengi. Methods Drugs with potential macrofilaricidal activity, were screened for the treatment of human onchocerciasis, using natural infections of O. ochengi in African cattle. Three groups of 3 cows were either treated at monthly intervals (7 treatments) with ivermectin (Ivomec®, Merck and Co. Inc.) at 500 μg/kg or doramectin (Dectamax®, Pfizer) at 500 μg/kg or not treated as controls. Intradermal nodules were removed at 6 monthly intervals and adult worms were examined for signs of drug activity. Results There was no significant decline in nodule diameter, the motility of male and female worms, nor in male and female viability as determined by the ability to reduce tetrazolium, compared with controls, at any time up to 24 months from the start of treatments (mpt). Embryogenesis, however, was abrogated by treatment, which was seen as an accumulation of dead and dying intra-uterine microfilariae (mf) persisting for up to 18 mpt. Skin mf densities in treated animals had fallen to zero by <3 mpt, but by 18 mpt small numbers of mf were found in the skin of some treated animals and a few female worms were starting to produce multi-cellular embryonic stages. Follow-up of the doramectin treated group at 36 mpt showed that mf densities had still only regained a small proportion of their pre-treatment levels. Conclusion These results have important implications for onchocerciasis control in the field. They suggest that ivermectin given at repeated high does may sterilise O. volvulus female worms for prolonged periods but is unlikely to kill them. This supports the view that control programmes may need to continue treatments with ivermectin for a period of decades and highlights the need to urgently identify new marcofiliaricidal compounds.

The vaccination of 35,000 dogs in 20 working days using combined static point and door-to-door methods in Blantyre, Malawi

An estimated 60,000 people die of rabies annually. The vast majority of cases of human rabies develop following a bite from an infected dog. Rabies can be controlled in both human and canine populations through widespread vaccination of dogs. Rabies is particularly problematic in Malawi, costing the country an estimated 13 million USD and 484 human deaths annually, with an increasing paediatric incidence in Blantyre City. Consequently, the aim of this study was to vaccinate a minimum of 75% of all the dogs within Blantyre city during a one month period. Blantyre’s 25 administrative wards were divided into 204 working zones. For initial planning, a mean human:dog ratio from the literature enabled estimation of dog population size and dog surveys were then performed in 29 working zones in order to assess dog distribution by land type. Vaccination was conducted at static point stations at weekends, at a total of 44 sites, with each operating for an average of 1.3 days. On Monday to Wednesday, door-to-door vaccination sessions were undertaken in the areas surrounding the preceding static point stations. 23,442 dogs were vaccinated at static point stations and 11,774 dogs were vaccinated during door-to-door vaccinations. At the end of the 20 day vaccination programme, an assessment of vaccination coverage through door-to-door surveys found that of 10,919 dogs observed, 8,661 were vaccinated resulting in a vaccination coverage of 79.3% (95%CI 78.6–80.1%). The estimated human:dog ratio for Blantyre city was 18.1:1. Mobile technology facilitated the collection of data as well as efficient direction and coordination of vaccination teams in near real time. This study demonstrates the feasibility of vaccinating large numbers of dogs at a high vaccination coverage, over a short time period in a large African city.

Seroepidemiology of bovine viral diarrhoea virus (BVDV) in the Adamawa Region of Cameroon and use of the SPOT test to identify herds with PI calves.

Bovine viral diarrhoea, caused by the bovine viral diarrhoea virus (BVDV) in the Pestivirus genus of the Flaviviridae, is one of the most important diseases of cattle world wide causing poor reproductive performance in adult cattle and mucosal disease in calves. In addition it causes immunosuppression and increased susceptibility to other infections, the impact of which is uncertain, particularly in sub-Saharan Africa where animals are exposed to a much wider range and higher intensity of infections compared to Europe. There are no previous estimates of the seroprevalence of BVDV in cattle in Cameroon. This paper describes the serological screening for antibodies to BVDV and antigen of BVDV in a cattle population in the Adamawa Region of Cameroon in 2000. The estimates of herd-level and within herd seroprevalences adjusted for test imperfections were 92% and 30% respectively and 16.5% of herds were classed as having a persistently infected calf (PI) in the herd within the last year based on the “spot” test approach. There was evidence of clustering of herds with PI calves across the north and west of the Region which corresponds with the higher cattle density areas and of self-clearance of infection from herds. A multivariable model was developed for the risk of having a PI calf in the herd; proximity to antelope, owning a goat, mixing with 10 other herds at grazing and the catchment area of the veterinary centre the herd was registered at were all significant risk factors. Very little is known about BVDV in sub-Saharan Africa and these high seroprevalences suggest that there is a large problem which may be having both direct impacts on fertility and neonate mortality and morbidity and also indirect effects through immunosuppression and susceptibility to other infections. Understanding and accounting for BVDV should be an important component of epidemiological studies of other diseases in sub-Saharan Africa.