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Zoonotic Challenges Print E-mail

Greater efforts are required to understand and control potential human pathogens in wildlife, and to use "animal sentinels" to signal communicable disease threats


Bernard Dixon

Cases of campylobacteriosis rose steadily and alarmingly in New Zealand between 1980 and 2006. The problem was, in fact, more serious there than in many other parts of the world. But Campylobacter is now well under control. Over the past year or so, case numbers have halved.

The achievement is attributable to the introduction of a variety of conventional but hitherto-neglected hygiene measures to reduce the proliferation and spread of the organism in New Zealand's poultry industry. But the crucial factor seems to have been some sophisticated computer modelling studies upon which the new controls were based. Nigel French and colleagues at Massey University in Palmerston North used epidemiological data from human cases, combined with genotyping and microbial exposure data, to estimate and monitor the proportion of cases of the disease stemming from food and environmental exposure.

Rather than adopting a single technique, French and his coworkers combined findings from four different types of modelling, including those designed to reflect movement of the pathogen within hosts, between hosts, and between different farms. One model, of proportional similarity, estimated the area of overlap between the frequency distributions of, for example, bacterial subtypes from different sources.

Speaking at a Society for Applied Microbiology (SfAM) meeting in Manchester, United Kingdom, French said that the modelling approach had also been crucial in ensuring that the poultry industry complied with the new control methods. "Although we still have limited understanding of individual transmission pathways, this work has enabled us to identify the contribution from the key amplifying hosts, including poultry from individual suppliers," he said. "We have also used detailed street-level spatial models to characterize the nature of the exposure to genotypes associated with poultry and ruminant sources, and this work has highlighted differences in the nature of rural and urban exposures in different age groups."

The study, conducted in the Manawatu region of New Zealand, seems too good to be true. Not so. This is a real and remarkable success story-in which, crucially, French's modelling methodology provided the clinching evidence to influence an industry initially highly resistant to any suggestion that chickens were the major source of campylobacteriosis in the country. Even conventional case-control studies had failed to do the job because they gave ambiguous and anomalous results (in one instance suggesting that eating chicken at home was more risky than eating it at a friend's house).

French's case history was an exceptional success story told during the SfAM conference. The tenor of much of the rest of the meeting reflected a blend of frustration and optimism towards what the organisers called "zoonotic challenges of the 21st century." Frustration stemmed from a growing recognition of the fragmentary nature of our knowledge of the behavior within wildlife of microorganisms transmissible to humans. Optimism came from a parallel realization that we could, without great difficulty, repair those deficits and apply the results to enhance the control of human diseases.

Sally Cutler, from the University of East London, gave one example of surprisingly incomplete knowledge-that of the extent of leptospirosis among rodents in the U.K., despite their existence as reservoirs for Leptospira species known to be pathogenic in humans. Using PCR methods on kidney samples from voles and 394 Y Microbe / Volume 4, Number 9, 2009 other wildlife, she and colleagues at the University of Edinburgh demonstrated that 8% of 200 rodent samples showed evidence of infection. The predominant species, identified in 3.5% of samples, was L. borgpetersenii. Others included L. interrogans, L. weilii, and L. noguchii. These are disquieting findings. They reflect a real risk to human health posed by a disease whose danger is underestimated because livestock are vaccinated against it while human cases are reported only infrequently.

One of Cutler's colleagues in Edinburgh, Anna Meredith, reinforced the argument that more use could be made of wild animals as "sentinels" to indicate the presence of organisms that can threaten human populations. With odd exceptions, such as the dying crows that signalled the arrival of West Nile Virus in New York City in 1999, wildlife is under-exploited for this purpose.

"We should in particular be investigating opportunities for monitoring carnivores-including true predators such as wild and domestic cats, which hunt and consume live vertebrate prey, and scavengers (for example crows, magpies, jackdaws, and rooks) that opportunistically consume dead prey and predator species," Meredith said. "Around 43% of zoonotic pathogens infect carnivores, and thus represent a suitable taxonomic group for detecting many of the pathogens of concern for human health." Other papers delivered in Edinburgh highlighted zoonoses controllable through wellestablished knowledge and techniques, rather than new strategies, but which are nevertheless neglected or overlooked in some parts of the world. "There is little doubt that canine rabies control is epidemiologically and practically feasible through vaccination," said Tiziana Lembo of Glasgow University. "Yet this form of the disease remains a substantial public health burden, with human fatalities, in much of Africa and Asia. It has even been increasing across sub-Saharan Africa."

One basis for optimism regarding vaccination is that divergences among typical canid viruses in these areas are surprisingly low, with no evidence of species-specific virus-host associations. Mass dog immunization campaigns have, indeed, had dramatic impacts on dog cases and human deaths in both the developed and developing world. And as Lembo reported, data from Africa have shown that the vast majority of dog populations are accessible for parenteral vaccination. The requisite 70% coverage is attainable in both rural and urban settings. The real challenge is that of securing the cooperation of local communities in establishing and operating vaccination centers. Scepticism or apathy can mean that these opportunities are not fulfilled.

Glyn Hewinson from the U.K. Veterinary Laboratories Agency reported both failure and success in efforts to deal with the threat to humans of bovine tuberculosis. In Britain, where badgers are a reservoir for the mycobacterium, culling the animals has been bedeviled by the problem of surviving badgers moving beyond their own territory and spreading infection further afield. A new strategy, based on the injection of an oral vaccine into the mouths of animals trapped and then released, may get under way in 2010, subject to approval of the vaccine by the Veterinary Medicines Directorate.

In New Zealand, oral vaccination had already succeeded in lowering the incidence of TB among brushtail possums (introduced originally from Australia). Immunisation of possums in a TBendemic area was 95% efficacious in females and 92% efficacious in males.

An unexpected report in Manchester came from Pierre Wattiau of the Veterinary and Agrochemical Research Centre in Brussels, Belgium. In a paper entitled "Wool-sorters' Disease in Belgium," he discussed risks of Bacillus anthracis infection arising during the industrial processing of wool and goat hair, which has almost disappeared from Western industrialized societies. Investigating a Belgian scouring factory active since 1880, he found B. anthracis in goat hair from the Middle East, and 4-7 out of 69 workers serologically positive for the organism. Appropriate protective measures have been recommended.

Unsurprisingly, the SfAM meeting heard a number of examples of microbiologists working on zoonoses who had themselves succumbed to infection. None was more horrendous than that of Philip Elzer of Louisiana State University. Warning his audience of the severe, debilitating nature of brucellosis, he was able to add personal experience of 18 months of illness to his more objective scientific data. In his case, however, treatment was less straightforward than it would be for most other patients. The strain he was studying had been genetically modified, and carried an antibiotic resistance gene.
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