The changing Brucella ecology: novel reservoirs, new threats

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Abstract

Brucellosis is a zoonosis that preceded humans but continues to cause significant medical, veterinary and socioeconomic problems, mainly because its overall burden remains underestimated and neglected. Its ecology, or what we know of it, has evolved rapidly in recent years. Two novel species, Brucella ceti and B. pinnipedialis, with the potential for causing human disease have been isolated from marine mammals. Another novel species, B. microti, has been isolated from wildlife animals, whilst B. inopinata has been isolated from a human case. An active spillover of Brucella between domestic animals and wildlife is also being recognised, with elk transmitting B. abortus to cattle, and freshwater fish becoming infected with B. melitensis from waste meat. In recent years the global epidemiology of the disease has not altered drastically, apart from increased awareness of brucellosis in sub-Saharan Africa and a rapid expansion of disease endemicity in the Balkan Peninsula. Isolated stories and events underline that Brucella knows no borders. The modern world has offered the pathogen the ability to travel and manifest itself anywhere and has also offered scientists the ability to track these manifestations better than ever before. This may allow the disease to be neglected no longer, or at least to be recognised as neglected.

Introduction

Brucellosis is a re-emerging zoonosis that has resurfaced at the epicentre of scientific interest and will continue to do so because of (1) its evolving epidemiology, which has seen new foci of both human and animal disease related to particular major sociopolitical events [1], (2) Brucella's inclusion on all lists of potential biological weapons, although this inclusion might predominantly be of historical importance [2], (3) Brucella's changing ecology, which is resulting in the recognition of new human populations at high risk of exposure, (4) the evolving scientific debate on the taxonomy of Brucella species and the genus as a whole [3], and (5) the recognition that human disease may mimic tuberculosis in its tendency to produce chronic, latent infection [4], [5].

Yet this re-emergence is predominantly one of scientific interest and not one of the pathogen and the disease per se. After all, Brucella may actually be the oldest recognised bacterium, one that may have caused disease, recognisable even today, in hominins hundreds of thousands of years ago [6]. The disease has been perpetually present but ignored because it is a human and animal disease of the poor. Yet even for a country with moderate endemicity, such as Greece, the annual economic burden of human disease has been estimated as higher than that of influenza and other ‘fashionable’ diseases, and is only lower than the economic burden of tuberculosis, meningitis and hepatitis B (the latter because of costly therapies) [7]. If there is a neglected disease, brucellosis is its definition.

Section snippets

Trends in global epidemiology

Modern international travel practices have resulted in increased exposure to a series of pathogens, including brucellosis, that are not encountered in everyday clinical practice of the developed world [8]. The global epidemiology of the disease, as outlined in a 2006 review [1], has seen the emergence of Central Asia, along with the Middle East, as the primary worldwide foci. This has been the result of political changes and the evolution of free trade in countries previously under a communist

Brucella taxonomy: more and more new entries

For many decades the Brucella genus included six species, four of which were pathogenic for humans (Table 1). Biovars were recognised for certain of these species and the classification has remained relatively unchanged since the recognition of B. neotomae in the late 1960s. However, in the 1990s, pathogens categorised as Brucella spp. were recognised in marine mammals [18], [19]. These novel species were eventually categorised as B. ceti (affecting predominantly porpoises and dolphins) and B.

Old species, new threats?

The role of B. canis in human disease is considered limited. Yet there are increasing reports of small outbreaks related to this species [27], which is not diagnosed with classical serology as readily as the other species pathogenic for humans.

The role of B. suis biovars in inducing infection has also been considered limited. However, there are increasing reports of brucellosis observed in hunters in contact with or consuming meat from wild boar [28], [29], [30]. B. suis was definitely

Wildlife as a constant reservoir

The role of wildlife animals as a reservoir for human disease has already been outlined in the case of the risk to hunters. Wildlife species naturally infected with Brucella can also serve as a reservoir for animal disease. This is the case with disease transmission between wild boar and domestic pigs and, more interestingly, between elk and cattle. The latter possibility has resulted in major political debate in the USA in recent years, with elk trapping, testing and, if positive, killing in

A new world likely to expand

Recognition of the ubiquitous presence of Brucella in the environment will most likely continue. The magnitude of marine mammal brucellosis and its clinical importance for human disease is only starting to become evident. The recognition of at least four new species in recent years will soon be followed by at least two more, doubling the number of confirmed species in less than a decade. Furthermore, the recognition that classical species persist, re-emerge in new foci, penetrate the borders of

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