Open access peer-reviewed chapter

Risk Factors for Brucella spp. in Domestic and Wild Animals

Written By

Ana Cláudia Coelho, Juan García Díez and Adosinda Maria Coelho

Submitted: 15 December 2014 Reviewed: 24 August 2015 Published: 19 November 2015

DOI: 10.5772/61325

From the Edited Volume

Updates on Brucellosis

Edited by Manal Mohammad Baddour

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Abstract

Brucella spp. is the aetiological agent of brucellosis, a serious contagious disease that results in reproductive failure and that has profound public health significance because of its zoonotic characteristics. This disease also is responsible for a high economic impact associated with the application of prevention, surveillance and test-and-slaughter programmes in animals by national authorities. Brucella spp. infects a large variety of animals and their prevalence is variable worldwide, mainly associated with the presence or absence of control programmes and also with the vaccination of animals against brucellosis. To achieve the control and eradication of brucellosis, the identification of the risk factors of brucellosis that maintain the infection in animals and/or the environment is fundamental. Although several risks have been identified, the most important have been associated with the biology of the bacteria, animal management (age, sex, species or breed), herd management (herd/flock size, number of species, contact with wild animals or type of animal production), farm management (facilities, cleaning and disinfection or veterinary support) and farmers’ knowledge about the disease. Thus, to benefit from proper risk identification of brucellosis, it is essential to put a cost-effective and efficient brucellosis control programme into place.

Keywords

  • Brucellosis
  • risk factors
  • animals
  • prevalence

1. Introduction

Brucellosis is a serious contagious disease that results in reproductive failure and has profound public health significance because of its zoonotic characteristics [1]. In animals, brucellosis can be considered as one of the most economically important zoonosis worldwide, resulting in clinical disease, abortion, neonatal losses, increased calving intervals, reduced fertility, decreased milk production, increased culling rates because of metritis and the emergency slaughtering of infected animals and also an impediment to free animal movement and trade [2-4]. However, a high economic impact is associated with the human disease and also by the application of prevention, surveillance and test-and-slaughter programmes in animals by national authorities [4,5].

Brucella spp. infects a large variety of animals as described in Table 1. Classically, the genus Brucella includes six recognized species based on antigenic/biochemical characteristics and primary host species [6]. Brucella abortus (cattle), Brucella melitensis (sheep and goats), Brucella suis (swine, cattle, rodents, wild ungulates), Brucella ovis (sheep), Brucella canis (dogs) and Brucella neotomae (rodents). More recently, other species have been recognized such as B. ceti (cetaceans), Brucella pinnipedialis (seals), Brucella microti (voles) and Brucella inopinata. The last was isolated from a breast implant in a human with clinical signs of brucellosis [7].

Animals Brucella spp. Hosts Reference
Domestic/Farm animals Alpacas, Cattle, Dogs, Goats, Horses, Llamas, Pigs, Sheep [8,9,10-14]
Wild animals Bears, Bison, Buffalo, Camelids, Caribou, Deer, Elk, Ferrets, Foxes, Rabbits, Rodents, Wolves [15,16,17-22]
Birds Partridges, Quails [23,24]
Marine mammals Dolphins, Dugongs, Manatees, Otters, Sea porpoise [15,23-29]

Table 1.

Hosts of Brucella spp. among the literature

The epidemiology of brucellosis is variable worldwide. In developed countries, brucellosis has been eradicated or presents low individual prevalence due to control programmes and vaccination of animals [30,31]. Currently, the brucellosis status of a country is based on the epidemiology in domestic animals. However, to consider a country free of brucellosis, it may also include epidemiological data regarding brucellosis in both wild animals and in marine animals [15,25].

According to the data available at the World Organisation for Animal Health (OIE) (2009), brucellosis (including B. abortus and B. melitensis) was not reported in several countries such as the USA, Australia and several European countries. Among the latter, Mediterranean countries such as Spain, Portugal, Italy and Greece are not brucellosis free today [32-35]. On the other hand, the picture of the prevalence of brucellosis has changed in South America, Africa, Middle East and Asia, where brucellosis is endemic because control programmes are insufficient or they basically do not have a great impact in animal and human health [5,26]. Since official data about prevalence of brucellosis in these countries is scarce, reports carried out in these areas show a large variability in the prevalence (Table 2).

The aim of brucellosis control is both to decrease the impact on human health and avoid economic consequences through reducing exposure to Brucella spp. and increase resistance to the infection among animal populations. To achieve this objective, several measures such as test-and-slaughter programmes and/or biosecurity measures (hygiene, control of animal movements, vaccination or reproductive management, etc.) should be performed [30]. However, to achieve success against brucellosis, the elaboration of control and eradication programmes must first identify all the potential risks that maintain the infection in animals and/or the environment.

Species Country Individual prevalence Lab method Reference
Cattle Brazil
Libya
Bangladesh
Nigeria
India
Uganda
Uganda
2.9%
42%
2.66%
24.0%
5,00%
14%
5%
RBT+2ME
RBT
RBT + I-ELISA
RBT+ELISA
RBT + ELISA
RBT
ELISA
[43]
[44]
[45]
[46]
[47]
[48]
[49]
Sheep Libya
Bangladesh
Nigeria
Kyrgyzstan
24%
2.31%
14.5%
8.9%
RBT
RBT + I-ELISA
RBT + SAT
RBT
[44]
[45]
[49]
[50]
Goat Libya
Bangladesh
Uganda
Nigeria
Kyrgyzstan
31%
3.15%
17%
16.1%
2.5%
RBT
RBT + I-ELISA
RBT
RBT+SAT
RBT
[44]
[45]
[48]
[49]
[50]
Horses Iran
Nigeria
Pakistan
2.5%
14.7%
20.7%
RBT
RBT
RBT
[51]
[52]
[53]
Dog Iran
Argentina
Nigeria
Nigeria
Iran
4.90%
14.7%
5.46%
28.6%
10.62%
IA
RBT
RBT
RBT
IA
[54]
[55]
[56]
[57]
[58]
Swine Croatia 1% RBT [11]
Coyote USA 18% Card test [59]
Camels Egypt 5.7% RBT [18]
Wild boars Switzerland
USA
1.5%
23.4%
RBT
CT+STT+RT+CFT
[60]
[61]
Marine mammals USA
USA
0.03%
38%
C-ELISA
RBT+CFT+ELISA
[62]
[63]

Table 2.

Seroprevalence of brucellosis among the different species

IA: Immunochromatography assay; RT: rivanol test; C-ELISA: competitive ELISA; CT: card test; STT: standard tube test; LAB method: laboratory method for brucellosis diagnostic; ELISA: Enzyme-Linked Immunosorbent Assay; RBT: Rose Bengal Test; 2ME: 2-mercaptoetanol test; CFT: Complement Fixation Test; I-ELISA: indirect ELISA; SAT: serum agglutination test


Identification of risk factors of brucellosis has been reported in epidemiological studies [36-41]. Although several risks have been identified, the most important are related to farm management, animal management and knowledge about the disease [42]. Thus, to benefit from proper risk identification of brucellosis, it is essential to put a cost-effective and efficient brucellosis control programme into place.

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2. Risk factors of brucellosis in animals

The risk factors can be categorized into those associated with characteristics of animal populations, management and the parasite biology.

2.1. Risk factors associated with the biology of Brucella spp.

Brucella abortus is the aetiological agent of bovine brucellosis and responsible for an economically important cause of abortions in cattle [31]. B. abortus also affects other species such as bison, buffalo or elks representing an important risk for the maintenance of the agent in the animal population with special importance in areas where wildlife and cattle rearing occur together [15]. Moreover, infections in wildlife can hinder eradication efforts in cattle. B. abortus is still a human pathogen and outbreaks associated from infected cattle and also from ingesting contaminated dairy products represent an important risk of infection [4].

Brucella melitensis can affect most domestic animals, but dairy sheep and goats are especially susceptible. Sheep have different receptivity according to breed, while in goats this association has not been reported [64]. B. melitensis is the main etiological agent of brucellosis in small ruminants, although sheep can be also infected by B. ovis. Sporadic cases of brucellosis have been described in sheep and goats as B. abortus and B. suis [65,66]. The dogs that guard the herds and flocks can also be infected [67].

Dogs, cats and other wild carnivores such as foxes or wolves present an important role in the epidemiology of brucellosis, because they act as mechanical disseminators due to the transportation of infected foetuses or placentas from abortions in infected herds and flocks. Since pigs are susceptible to infection by B. melitensis, pig farms present some epidemiological importance where both species are reared [68]. In addition, wild ruminants with potential contact with infected sheep and/or goats could be infected with B. melitensis, maintaining the infection in natural environment [15].

Porcine brucellosis is caused by Brucella suis biovars 1, 2 or 3. The disease caused by biovars 1 and 3 is similar, while that caused by biovar 2 differs from 1 and 3 in its host range, its limited geographical distribution and its pathology [66]. In domestic pigs, risk factors associated with infection are ingestion of aborted foetuses, foetal membranes, abortion products and uterine discharges, or contaminated foodstuffs. Transmission during copulation is very common [66,69,70]. Artificial insemination with contaminated semen or conjunctival mucosal should also be considered a risk [66,71].

The infection of a pig herd by brucellosis could be associated with the purchase/entrance of infected animals, contact with wildlife reservoirs, use of contaminated semen or feed [72] or the use of a lend boar. Other risk factors could be attributed to transmission of the disease by mechanical vectors due to contamination of vehicles, holding equipment or utensils and also to the introduction of infected offal (e.g. placenta and afterbirths) [70]. Serological screening and purchase from brucellosis-free herds should reduce this risk [70].

The likelihood of the introduction of the infection from potentially infected wild boar, free-range pigs or hares and its establishment in outdoor and backyard pig populations depends on housing management such as the type of housing (outdoor vs indoor), low levels of biosecurity, direct or indirect contact with infected wild boar, free-ranging pigs or hares, feeding practices (i.e. home prepared food vs commercial food), purchasing animals or semen without testing, no testing of live pigs, husbandry systems, lack of detection of unapparent infections, contamination of semen collection centres and equipment, contamination of transport vehicles, transport of pigs from different holdings or mixing of pigs [70].

2.2. Risk factors associated with the host

2.2.1. Age

Age has been referred to as one of the intrinsic factors associated with brucellosis. Higher seroprevalence of brucellosis has been observed in older animals, both in cattle and small ruminants with a prevalence odds ratio (POR) of about 2.0 in cattle over 5 years old and a POR of about 1.7 in small ruminants over 2 years old [43,73-77]. Similar results have been observed in wild boars and camels [78,79]. Brucellosis has traditionally been considered a disease of adult animals since susceptibility increases after sexual maturity and pregnancy [80]. However, variations in the age of sexual maturity among breeds could present differences between age and brucellosis positivity [81]. Brucella spp. presented a tropism to the reproductive tract due to the production of erythritol, a 4-carbon sugar produced in the foetal tissues of ruminants that stimulates the growth of Brucella [82]. Thus, it may also explain the higher prevalence in adult animals than in young [83]. On the other hand, a higher prevalence of brucellosis in adults has also been associated with longer contact with infected animals or with the environment. This potential risk may be significant in those herds without culling of positive animals [84]. It must be kept in mind though that this low prevalence might be faulty because young animals can be infected without clinical symptoms presenting serologic response for only one week [83,84].

2.2.2. Sex

The influence of sex in the prevalence of brucellosis has been studied in cattle, small ruminants and wild animals [74,77,79,80,84]. Female ruminants presented a higher odds of brucellosis infection, the same has been observed in female dogs compared to male dogs [85]. Although this is difficult to explain, it could be associated with the intrinsic biology of the microorganisms and its tropism to the foetal tissues as previously described. Since brucellosis infection in males presented clinical signs such as epididymitis and orchitis, the prevalence in males could be lower than females because they may be culled faster [86]. On the other hand, the absence of clinical signs such as abortion or metritis in non-pregnant infected females or the absence of farmers’ observation/identification of abortions in extensive herds may also explain the higher prevalence in females. In addition, in non-pregnant females, brucellosis becomes chronic. This fact has important epidemiological implications since, after an initial immune response, animals may be asymptomatic carriers, the antibodies disappear from circulation and are difficult to detect with traditional serological techniques [87]. Since brucellosis in pigs may affect both males and females equally, sex susceptibility has not been fully demonstrated [72]. Regarding wild boars, the behavior of females living in matriarchal groups could explain the higher prevalence [79].

2.2.3. Species and breed

The prevalence of brucellosis is variable among species and region as described in Table 2. However, prevalence in farm animals seems to be lower in small ruminants than large ruminants [44,84] and lower in sheep than in goats [45,88,89]. Transmission of brucellosis occurs in ruminants through the excretion of contaminated materials from the female genital tract, which constitutes the main form of transmission to other animals and humans. In most of the circumstances, the main route of spread is the placenta, foetal fluids and vaginal discharges expelled after delivery or abortion. At that time, large numbers of Brucella are released [90]. The vaginal excretion of Brucella spp. in goats is greater and more prolonged than sheep, lasting for 2-3 months. In sheep, it is generally lower and normally ceases within 3 weeks after birth or abortion. It is also common that excretion occurs through milk or semen [91]. The excretion of Brucella in milk is generally intermittent and usually only appears 6 to 12 days after the abortion. In goats, the excretion is more abundant and more prolonged, so there is an increased risk of infection via the consumption of milk from this species [92,93].

The phenomenon of latent brucellosis in sheep was observed in lambs born from infected mothers that breast-feed with milk contaminated with Brucella. These lambs are seronegative to adulthood, while in females, the latency of brucellosis is maintained until the first pregnancy, a period in which the disease process develops [94].

Infected females thus present a high number of abortions with special importance in primiparous females [87].

In game animals, seroprevalence in wild boars seems to be higher than wild ruminants [8,95-98]. To the best of our knowledge, there is no evidence of higher susceptibility to brucellosis within specific species. In the case of horses, they have usually been considered more resistant to brucellosis than ruminants [51], but the variation of prevalence reported in endemic areas of brucellosis [99,100] seems to be discussible. The information available about differences of brucellosis infection by species is scarce. In sheep, pregnant dams do not present Brucella spp. in vaginal discharges, contrary to that observed in goats [101], where excretion may extend over two or three months [102]. Thus, the higher prevalence in specific species could be achievable through the intrinsic characteristics of the etiological agent [103].

Regarding the breed, a higher prevalence of brucellosis has been reported [104] in cross-breed cattle than local breeds, although other reports indicated no statistical differences among cattle breeds [46,105]. In small ruminants, Maltese and South American sheep breeds seem to present a greater resistance to brucellosis compared to the sheep breeds of Southwest Asia and the Mediterranean, such as the Awassi breed [13,106,107]. Although Husky and Chihuahua dog breeds appeared to be more prone to Brucella infection than other breeds, their infection seems most likely influenced by other factors such as the local dog population or owners than by dog breed [107]. In swine, some breeds such as Duroc and Jersey Red crosses may be less susceptible to experimental challenge with B. suis, suggesting some genetic resistance [108]. Previous studies showed that stray dogs demonstrated a greater than three-fold rate of infection versus non-stray dogs [109].

Keypoint: Risk factors associated with Brucella spp. and the host

Brucella abortus is the aetiological agent of bovine brucellosis in cattle although also infects other species such as bison, buffalo or elks. It represents an important risk to the maintenance of the agent in the animal population with special importance in areas where wildlife and cattle commingled. B. melitensis is the main etiological agent of brucellosis in small ruminants, although sheep can be also infected by B. ovis. Sporadic cases of brucellosis have been described in sheep and goats as B. abortus and B. suis. Porcine brucellosis is caused by Brucella suis biovars 1, 2 or 3. The disease caused by biovars 1 and 3 is similar, while that caused by biovar 2 differs from 1 and 3 in its host range, its limited geographical distribution and its pathology.

Several risk factors of brucellosis have been associated with the host such as age, sex, species or breed. Regarding age, higher seroprevalence of brucellosis is observed in older animals since susceptibility increases after sexual maturity and pregnancy. It could be associated with the tropism of Brucella spp. to erythritol, a 4-carbon sugar produced in the foetal tissues of ruminants that stimulates the growth of Brucella. This fact may explain the higher prevalence in adult animals than in young ones. With regard to sex, the odds of infection by brucellosis in ruminants are higher in female than male probably associated with the tropism to the foetal tissues as previously described. Species and breed have also been described as risk factors. In farm animals, the prevalence seems to be lower in small ruminants than large ruminants and lower in sheep than in goats. In this last case, the vaginal excretion of Brucella spp. in goats is greater and more prolonged than sheep, lasting for 2-3 months whereas excretion in sheep is generally lower and normally ceases within 3 weeks after birth or abortion. Regarding the breed, there is not consensus among the studies. Thus, some of them reported higher prevalence of brucellosis in cross-breed cattle than local breeds. In small ruminant, Maltese and South American sheep breeds seem to present a greater resistance to brucellosis compared to the sheep breeds of Southwest Asia and the Mediterranean, such as the Awassi breed.

2.3. Risk factors associated with herds

2.3.1. Herd/flock size

An important risk factor for brucellosis seropositivity is herd size, being higher in large herds and/or flocks. An increased odds ratio for seropositivity has been largely reported in cattle [82,84,104,110] as well as in small ruminants [77,86,111]. In contrast, no statistical differences among goat flocks were observed in the literature [112,113].

The higher prevalence of brucellosis in large herds and/or flocks has been associated with several factors, such as a higher number of animals tested in larger herds means the probability of detecting at least one seropositive animal is greater [77] or the higher number of animals increases the likelihood of transmission of the disease by contact among them [114]. The low prevalence of brucellosis in small-sized herds could also be associated with the herd and/or farm management [86]. Thus, small-sized flocks usually graze at pastures near or contiguous to the farm, avoiding contact with other flocks or utilization of common paths and/or roads. Because premises for small herds or flocks are smaller, cleaning, disinfection and manure removal procedures are easier and less time consuming to the farmer. Disinfection is also facilitated by the low resistance of Brucella spp. to most disinfectant agents [115] and by the low cost of this operation. Farmers of small-sized herds may easily control the partum period and usually keep dams away from the flock during parturition. This measure is very important in case of abortions, to avoid pasture contamination. In these small sized herds, replacement is usually made by reposition and economic trade is not frequent. Thus, the absence of an elevated rate of animal movement decreases the likelihood of infection.

The health status of a flock may influence the predisposition to brucellosis infection. Thus, in small-sized herds, farmers can easily identify sick animals and veterinary and preventive treatments are usually carried out at low financial cost. Regarding the official control of brucellosis by the official veterinary authority, small-sized flocks are easily controlled and in the case of a positive finding, most farmers agree to cull the whole flock to maintain the brucellosis-free status and also to avoid a zoonotic infection [116,117]. In addition, the vaccination coverage of young animals with RB-51 or Rev-1 is more easily achievable in these herds.

On the other hand, the higher prevalence of brucellosis observed in large flocks may be also associated with the utilization of communal pasture areas, utilization of common paths and/or roads and due to contact with others flocks [114]. Cleaning and disinfection procedures of premises and manure removal in large-sized flocks is more difficult than in medium or small flocks because it requires the availability of mechanical equipment and consequently a higher financial cost. An increased prevalence of brucellosis associated with decreased of proper manure removal, cleaning and disinfection procedures has been described [118]. The control of reproductive management is difficult in large flocks, where parturitions on grazing areas are frequent and abortions are a source of pasture contamination. In addition, animal movement in large herds is frequent, both for replacement and/or trade, thereby increasing the risk of infection by brucellosis. Due to the higher cost of veterinary treatments and/or application of preventive programmes, animals in large flocks may be more susceptible to brucellosis infection. Moreover, associated with high numbers of animals unvaccinated and/or non-blood sampled animals may occur and remained unprotected and susceptible in case of infection. In addition, these animals act as a source of brucellosis contamination to the rest of the herds [74,118] and in the case of positive animals, farmers hesitate to slaughter the entire flock.

In dogs, the risk of transmission increases in kennel environments due to the high interaction among the animals and reduced space, which infected dogs share with other healthy ones to play, defecate or urinate [119]. Kennels with a history of abortion are 13 times more likely to be seropositive than kennels without this record [120].

Transmission studies have demonstrated that the exposure of healthy dogs to abortion products is an easy way for B. canis transmission [119]. The aborting bitch presents a high risk for the spread of infection to healthy dogs. B. canis is also found in the milk of infected lactating bitches, which might lead to the potential infection of nursing pups [121]. The high POR of seropositivity in kennels with a history of abortions could be associated with the presence of Brucella over long periods of time, caused by the absence of good reproductive practices and exposure to body fluids in the environment [120].

2.3.2. Number of species

Farming several species in the same herd has been described as a risk factor [78,80,84], although there is no evidence of higher susceptibility of brucellosis in specific species. Thus, an increase in prevalence where several species intermingle is difficult to explain but could be associated with higher chances of being Brucella seropositive because of multiple sources of infection.

It has been suggested that brucellosis is transmitted only rarely from sheep and goats to cattle, or among cattle [88]. However, the higher risk for cattle on farms which also had sheep or goats suggests that some of the cattle infections may have originated from small ruminants since B. melitensis biovar 3 was isolated from cow’s milk.

Because B. melitensis is considered the most virulent of Brucella, it may explain the increased POR in cattle rearing with small ruminants [103]. In addition, the susceptibility of all ruminants to infection by B. abortus may explain the higher prevalence of brucellosis in cattle herds in contact with buffaloes or wild ruminants [37,122]. Horses seem to be resistant to brucellosis, although the risk of infection increases when they intermingle with cattle [46].

In regions where B. melitensis has been confirmed in sheep and goats, cattle can become infected with this bacterium [74]. It has not yet been determined whether B. melitensis can be kept alone in a population of cattle in the absence of small ruminants. B. melitensis causes abortion in cattle similarly to B. abortus.

As previously described, horses present a certain resistance against brucellosis, however, seropositivity has been associated with horses in areas without brucellosis control programmes for large and small ruminants. In addition, B. suis infection in horses has been reported in those commingling with swine [123].

The presence of swine could be a risk for brucellosis transmission to cattle [123] and is a public health concern. However, recent studies showed that cattle intermingling with pigs in the same area do not seem to be infected by Brucella spp. and do not contribute to its maintenance [125]. In contrast, the risk of cattle infection by B. suis from wild boar has been recently described [126].

The practice of mixing cattle, either through grazing or sharing watering points, is a significant risk factor for brucellosis [104,127,128]. Community pastures should be treated as livestock unit and control measures must be applied to all animals [129].

Other researchers [84] found that the disease is easily transmitted in areas where extensive production systems predominate, based on grazing and the high mobility of herds, the mixture of species in the same herd and where sharing pastures, roads and water sources occurs. Mobility increases the likelihood of contact with other potentially infected herds or wild animals that are reservoirs of disease.

The presence of dogs has been described as a risk for brucellosis infection in farm animals [125] and represents a potential epidemiological threat in endemic and/or brucellosis areas without brucellosis control programmes. However, dogs are a potential risk in the diffusion of brucellosis, acting as mechanical disseminators by feeding on aborted foetuses, dragging them along and spreading the bacteria [107].

Canine brucellosis is usually caused by B. canis, although infection by B. abortus, B. suis and B. melitensis have been reported [129]. Previous studies showed that dogs have been identified as a link in the brucellosis transmission chain. B. abortus and B. melitensis can be transmitted from cattle to farm dogs playing the role as vector. Brucella can produce disease in dogs via ingestion of infected reproductive tissues [9]. Infected dogs with B. abortus can spread organisms into the environment through urine, vaginal secretions, aborted foetuses or faeces. If a pregnant dog is infected with B. abortus, it may abort, and the tissues and vaginal discharges have a great potential for transmitting Brucella to susceptible cattle [9,129]. Dogs can also be infected with B. suis via ingesting aborted swine foetuses [71]. Thus, the elimination of infected cattle may not necessarily eradicate the disease [9].

2.4. Risk factors associated with farm management and environment

Several risk factors of brucellosis associated with farm management and environment have been referred to in the literature as presented in Table 3.

Factors described Reference
Absence of calving paddock [14,43]
Age [75,77]
Breed [39,77]
Cleaning and disinfection [40,112,114,130]
Climatology [79]
Commingling with other animals [14,88,114,131]
Communal pastures [36,43,112,130]
Contact with wildlife [36,74,104]
Education [40,42,80]
Handling of aborted material [43,80]
Intensive management [104,132,133]
Herd size [36,40,75,77,88]
Lending males [112]
Main animal production (beef /dairy) [76]
Milking procedures [80]
Purchase/entrance of new animals [39,112]
Sex [77]
Specie [114]
Stocking rate [14,77,125]
Transhumance [104]
Veterinary services [43,104,112,117,131]
Water sources [40,125,130]
Handling of aborted material [43,80,134]

Table 3.

Risk factors of brucellosis infection in animals

Regarding the main seroprevalence, dairy animals have a much greater chance of not only contracting brucellosis but also of spreading it faster than beef animals. The reason is not a genetic or physiological factor but due to husbandry. Animals that live in concentrated smaller areas come into close contact when they are grazing and when they are milked [129]. The zoonotic transmission of brucellosis by improper milking procedures was observed [128] associated with skin lesions in hands. Thus, transmission through skin lesions of the udder is not a neglectable source of infection. In addition, it is considered that dairy animals are subjected to more stress conditions on farms, leading to a higher susceptibility to brucellosis infection [135]. The persistence of the infection of the udder and supramammary lymph nodes leads to a constant or intermittent excretion in milk in successive lactations. This fact constitutes an important source of infection for humans and for the young animals [136].

Animal purchase has been considered as a risk for brucellosis. Purchasing in larger herds has usually been associated with more animal movements on and off the farm, and this practice increases the risk of introducing an infected animal into a herd [81]. Introduction of animals from market fairs also presents a higher risk of infection. The majority of infections or reinfection in disease-free herds starts through buying infected animals of unknown status [128]. This has a higher importance in those endemic areas or countries where there is an absence of control programmes. However, in countries with test-and-slaughter control programmes, the movement of cattle are subjected to a compulsory pre-movement test that consists in the serological brucellosis diagnostics before an animal leaves the farm [42]. Moreover, animal movement restriction measures are applied in brucellosis positive herds to avoid spreading the disease [34].

The proximity to other infected herds or flocks has also been described an infection risk, although, small ruminant contact with other flocks was reported to have no impact on Brucella seropositivity in Spain [137].

The influence of the agro-ecological zone has been also referred to as a brucellosis risk factor, having a higher prevalence in dry zones [132]. Since pasture areas are scarce in dry zones, animals must seek pastures over large areas implying an unrestricted animal-to-animal contact with potential transmission as previously described. In addition, transmission due to aerosol inhalation of contaminated dust from foetal discharges or abortions is possible [138]. In contrast, a lower prevalence of brucellosis in these areas has been proposed by other authors [139] due to lower survival of Brucella spp. in aborted material in dry-zones.

Larger herds might be expected to be associated with intensive management practices that are typically more difficult to control and allow for closer contact between animals and their environment, which increases the potential for exposure to infectious excretions [130]. In addition, the stressful conditions of animals subjected to intensive production may make them more susceptible to the infection, as previously described. On the other hand, extensive management may also imply a risk of brucellosis and higher prevalence has been reported in small ruminants. Although difficult to explain, it could be associated with controlling abortions, observation of sick animals or contact with animals, among others [86]. Since extensive management implies rearing a large number of animals in large areas and/or sharing communal pastures, the contamination of pastures with placentas or abortions is a source of infection to other animals in the herds, as we described previously in the risk factors of brucellosis by the herd size.

Animal handling and environmental conditions are risk factors which influence the transmission of infection, such as births and breeding in semi-dark settings, confinement in closed spaces and high animal densities [130]. Another risk of intensive systems could be associated with airborne dust transmission indoors [138].

The season also has an impact on herd management and animal nutrition, mainly in production systems involving transhumance or nomadic practices [114]. Rainfall affects the development and the nutritional state of the pasture. These factors influence the reproduction of animals kept in extensive systems and thus the time of delivery/miscarriages. In intensive systems, isolation of post-parturient animals in maternity facilities reduces the spread of infection to the rest of the herd or flock [128].

Cleaning and disinfection of farm facilities and proper manure removal have been described as a protective factor against brucellosis infection [114,118,130]. This fact is associated with the low resistance of Brucella spp. to most disinfectant agents [115] although their effectiveness is based on the previous elimination of organic material since it decreases the bactericidal effect of the disinfectant [140]. A similar risk of brucellosis was reported in kennels [119,120]. Kennels with improper management of excrement and built with materials such as tile, wood and earthern floors were considered to have a higher risk for infection since they maintain exposure to urine, faeces, or reproductive secretions [120].

Insect rodents on dogs could act as a mechanical vector of brucellosis. Blood-sucking insects have been reported as disseminators of brucellosis. Brucella was isolated from the stomach contents of Stomoxys calcitrans, Ornithodoros and Musca autumnalis (stable fly). The stable fly is dipterous in contact with ruminants. The female lays eggs in the faeces of these animals and feeds on their blood, tears and placental secretions. It is thought that these insects and ticks contribute to disease transmission [92,138]. As mentioned earlier, dogs intermingling with large and small ruminants in farms have presented an important role in the epidemiology of brucellosis. However, stray dogs which remain free on the streets and travel long distances also act as disseminators of the agent and provide chances for infection of other animals and humans through environmental contamination [141].

Environmental factors that affect the ability of Brucella to survive outside mammalian hosts need to be considered in the epidemiology of brucellosis. High humidity, low temperatures and absence of direct sun light may favour the survival of Brucella for several months in water, aborted foetuses, placental membranes, liquid manure, hay, buildings, equipment and clothes [129].

The survival of Brucella outside a mammalian host is relatively persistent compared to other non-sporulating pathogenic bacteria in similar circumstances [142]. Favourable conditions are pH>4, low temperatures, absence of direct sunlight and high humidity. Brucella can persist for several months in water, aborted placentas, faeces, manure, wool, facilities, equipment and clothes [143]. Brucella can survive for 40 days in dry soil and 60 days in moist soils, 144 days at 20 °C and 40% relative humidity, for several months in drinking water at 4 °C to 8 °C and two and a half years at 0 °C, 30 days in urine, 75 days in aborted foetuses, more than 200 days in uterine secretions and several years in frozen tissues or culture media. Brucella resistance to different environmental conditions increases in the presence of abundant organic matter. The spread of the disease via waterways is not frequent and can only be effective over short distances [129].

2.5. Other factors associated with brucellosis

The role of farmers’ knowledge about brucellosis has been discussed in the literature. It was noted that knowledge ages equal to or older than 55 years was a protective factor for brucellosis prevention [40,42]. This observation is difficult to explain and may be due to younger farmers’ lack of experience. Older farmers have more familiarity with recognizing the clinical signs of the disease or the main route of transmission and can be more aware of the importance of preventive measures [67,144,145]. Farmers who had previously experienced brucellosis in their herds had a higher probability of having greater knowledge of bovine brucellosis, which is consistent with having experience with the disease. Producer’s associations, education and veterinary support have been recognized as protective factors [42,118]. Farmer’s lack of awareness about brucellosis, improper handling of aborted materials and the habit of consuming raw milk, among other factors, might contribute to further spread of brucellosis in their livestock and expose the community to a public health hazard [80].

Keypoint - Risk factors associated with farm management and environment

The risk factors of brucellosis associated with the herd are size and the number of animal species. The higher prevalence of brucellosis in large herds could be explained by the higher odds of detecting at least one seropositive animal, the increase of the transmission of the disease by contact among them, utilization of communal pasture areas or improper cleaning and disinfection procedures in large farms. Farming several species in the same herd has been described as a risk of infection due to multiple sources of infection. Thus, presence of dogs in large herds may spread Brucella spp. by both mechanical carriers or by the spread of the organisms into the environment through urine, vaginal secretions, aborted foetuses or faeces.

Dairy animals have a much greater chance of not only contracting brucellosis but also of spreading it faster than beef animals. Because animals that live in concentrated smaller areas come into close contact when they are grazing and when they are milked. In addition, it is considered that dairy animals (intensive production) are subjected to more stress conditions on farms, leading to a higher susceptibility to brucellosis infection. Purchasing in larger herds has usually been associated with more animal movements on and off the farm, and this practice increases the risk of introducing an infected animal of unknown status with special importance in areas with absence of control programmes.

Also the influence of the agro-ecological zone has been also referred as a brucellosis risk factor. High humidity, low temperatures and absence of direct sun light may favour the survival of Brucella for several months in the environment. In addition, cleaning and disinfection of farm facilities and proper manure removal have been described as a protective factor against brucellosis infection. This fact could be explained to the low resistance of Brucella spp. to the disinfectant agents.

2.6. Brucellosis in wild animals — A threat to farm animals

Brucella abortus and B. suis have been isolated worldwide from a great variety of wildlife species [15]. Some general risk factors, which can be identified in most of the wildlife diseases are wildlife overabundance, movements of wild and domestic animals and fomites [146]. Artificial management of wild species, including fencing, feeding and translocation, can also increase the risk of transmission of infectious brucellosis. [147] The risk of infection increases dramatically with increasing wildlife density and their exposure to Bucella abortus around feeding grounds [148]. Wild ruminants have been suggested as brucellosis carriers, but they are probably not true reservoirs [146,148]. Other works showed that wild ruminants do not play a relevant role in the maintenance of B. abortus and B. melitensis infections since limited cases of brucellosis have been reported in wild ruminants [79,149,150]. Only weak evidence for a direct relationship between brucellosis and size/density of the population of wild animals has been reported [151]. However, a potential risk for brucellosis infection of livestock by wild animals could be associated when artificial management such as winter feeding increases aggregation [146,151]. Thus, wild animals are often at risk as a consequence of contact with infected livestock, particularly in extensive breeding systems [79].

With regards to elk and bison, artificial feeding management during winter results in significant congregations in the feeding grounds and increases the risk of elk being exposed to B. abortus [15]. A possible risk factor for bison in the USA is environmental contamination by the RB51 vaccine strain, which is a rifampicin resistant strain released in the environment [15].

Rangiferine brucellosis (brucellosis in reindeer and caribou) is caused by B. suis biovar 4 in the Arctic regions of Siberia, Canada and Alaska, constituting a serious zoonosis. B. suis may also infect moose (Alces alces) and occasionally various carnivores [15]. In European wild boar B. suis biovar 2 was observed in all age categories [152,153].

2.7. Brucellosis in marine mammals — New threat?

Brucella was detected in free-ranging pinnipeds and cetaceans from America, Europe, Japan, New Zealand, the Solomon Islands and the Antarctic, as well as in captive bottlenose dolphin (Tursiops truncates) [154-157].

Brucella ceti and B. pinnipedialis prefer cetaceans and seal hosts respectively [157, 158]. Epidemiological studies of risk factors for Brucella infection in cetaceans and pinnipeds have not yet been performed, and the role of environmental factors in the emergence of marine mammal brucellosis is still unknown [157]. It seems unlikely that B. ceti could survive for long periods outside marine mammals.

The transmission of brucellosis in marine mammals is not totally understood [158]. The dilution of the agent in sea water may make transmission difficult due to a low infecting dose. It is likely that the mode of transmission is through close contact between hosts, such as sexual intercourse or maternal feeding, contact with aborted foetuses and placental tissues or through fish or helminth reservoirs [159]. A second alternative corresponds to vertical transmission from mother to foetus, which is feasible since foetuses and placenta from infected animals have been found to contain large quantities of Brucella [156]. In addition, the behaviour of assisting the births observed in several cetaceans could be a risk due to the close contact with foetal tissues and discharges [27]. This hypothesis should be considered since B. ceti have been found in aborted foetuses and the reproductive organs of captive bottlenose dolphins [156] and in the uterus of a stranded striped dolphin with placentitis [160]. B. ceti has been also associated with mastitis and endometritis in cetaceans [161]. Both B. ceti and B. pinnipedialis have also been isolated from the testes, uterus and mammary glands of cetaceans and pinnipeds without any apparent pathology [162-164]. A potential risk factor could be the infection through ingestion of Brucella contaminated fish or helminth vectors [165]. B. ceti and B. pinnipedialis have been isolated from lungworms (Pseudalius inflexus) in the lungs of cetaceans and pinnipeds and these parasites can be a reservoir and vector for Brucella in these animals [165].

2.8. Animal brucellosis and zoonotic risk

In endemic regions without brucellosis eradication programmes, zoonotic risk still represents an important public health threat [166]. Infection happens due to contact with infected animals or consumption of their products, mostly unpasteurized milk and milk products of sheep and goats [167]. It presents special importance in those regions where trading of raw milk and raw milk products is a common practice among farmers [168]. The survival of Brucella in milk and dairy products is related with curing methods, humidity, temperature and/or changes in pH. For milk, Brucella survival is inversely proportional to the pH [169]. Brucella can be responsible for milk-borne diseases, particularly since the appearance and taste of the milk are rarely affected by the presence of the bacteria [170]. Boiling or heating of milk at 80–85 ºC [176–185 ºF] for several minutes [approximately 10 minutes] will destroy the bacteria [30]. Bacteria cannot survive if the cheese is cured longer than 3 months [171]. In acidified soft cheeses and dry cheese, their survival is greater. Thus, European legislation requires that all cheeses made from raw milk be submitted to a cure period of not less than 60 days [172]. Survival time in meat is lower, except in frozen meat where the microorganism can survive for several years [173].

Although zoonotic brucellosis is mainly associated with farmers in high prevalence areas, even in low prevalence countries brucellosis represents an important threat as a work-acquired infection among dairy farmers, butchers, veterinary practitioners, meat inspectors, slaughterhouse personnel or artificial inseminators who do not take adequate biosafety precautions while performing their jobs [174-176]. In addition, brucellosis vaccines such as Rev-1 and RB51 are live dried living vaccines. Thus, needlestick accidents during their preparation or administration could also be a risk factor for human infection. Close contact with animals may occur when farmers or veterinarians assist animals during parturition or abortion or handling of stillbirth. In some parts of the world it is also common practice for farmers to separate the placenta manually, thereby increasing their exposition to tissues infected with Brucella [168].

Dairy farmers who milk with bare hands have a greater chance of becoming infected from Brucella infected animals [177] as do farmers or slaughterhouse workers who have skin lesions which provide an entry point for the bacteria [128]. Also, inhalation of Brucella has been previously reported in slaughterhouse workers where the concentration of Brucella can be high due to aerosol generation [129].

Zoonotic brucellosis from marine mammal includes individuals in traditional communities where products from whales and seals are still an important part of their diet [16]. In addition, occupational acquired infection in people handling stranded marine mammals, whale and seal hunters, marine researchers and other people handling raw products from the ocean could be exposed [25,178]. Also, it is suggested that marine avian species may harbour Brucella by eating infected fish and thus become vectors of zoonotic infections [158]. Tourists who swim and interact closely with captive dolphins can be at risk when Brucella spp. could be circulating in these colonies [163].

Keypoint: Emerging risk factors for brucellosis

Wild animals have been referred as reservoir of brucellosis and represent an important risk of infection to farm animals, particularly in extensive breeding systems.

The prevalence of brucellosis in wildlife varies worldwide and several species such as bison, reindeer, caribou or wild boar have been described as potential source of infection of livestock. However, their role as risk factors of infection is still discussed since the microbiological isolation of Brucella spp. has been reported in wild ruminants. The zoonotical potential of Brucella spp. still represents an important public health threat not only in areas without eradication control programmes but as a work-acquired infection among dairy farmers, veterinarians or meat inspectors among others while performing their jobs. The discovery of brucellosis in marine mammals also represents a public health threat with special interest in occupational acquired infection in people handling stranded marine mammals.

Foodborne brucellosis is an important biological hazard associated with dairy products. However, the presence of Brucella spp. in marine animals indicates that fish-borne brucellosis could be a future hazard to be considered.

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3. Conclusions

Brucella spp. is responsible for a contagious disease that results in reproductive failure and has an important economic impact, not only in animal health but also in public health because of its zoonotic characteristics. To achieve the control and eradication of brucellosis, the identification of all potential risks is necessary. Given the important role of domestic and wild animals as potential sources of Brucella infection, further risk assessment will require more complete and reliable data on the infection prevalence. Several risk factors have been described for brucellosis infection, although the herd or flock size, species and age have been cited as the most important. Brucellosis has traditionally been associated with farm animals, however, risks of brucellosis associated with wildlife and marine mammals could be a new threat and further epidemiological studies are necessary. In addition to animal sanitary measures, complementary measures such as good farm practices, biosecurity, training and education are necessary to control this old disease that is still of concern today.

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Acknowledgments

The work was supported by the strategic research project PEst-OE/AGR/UI0772/2014 financed by the Foundation for Science and Technology [FCT]. This study was supported by the Foundation for Science and Technology of Portuguese Ministry of Education and Science [FCT - Fundação para a Ciência e Tecnologia do Ministério Português para a Educação e Ciência] by a research grant SFRH/BD/85118/2012 given to the author J. García Díez.

References

  1. 1. Olsen S, Bellaire B. Brucella. In: McVey DS, Kennedy M, Chengappa MM, editors. Veterinary Microbiology. 3º ed. Willey-Blackwell. New Jersey; 2013.
  2. 2. Edmondson MA, Roberts JF, Baird AN, Bychawski S, Pugh DG. Theriogenology of sheep and goats. In: Pugh DG, Baird NN, editors. Sheep & Goat Medicine. Elsevier Health Sciences. Missouri; 2012. p. 150-230.
  3. 3. Neta AVC, Mol JP, Xavier MN, Paixão TA, Lage AP, Santos RL. Pathogenesis of bovine brucellosis. The Veterinary Journal. 2010;184:146-155.
  4. 4. Seleem MN, Boyle SM, Sriranganathan N. Brucellosis: a re-emerging zoonosis. Veterinary Microbiology. 2010;140:392-398.
  5. 5. McDermott J, Grace D, Zinsstag J. Economics of brucellosis impact and control in low-income countries. Revue Scientifique et Technique (International Office of Epizootics). 2013;32:249-261.
  6. 6. Banai M, Corbel M. Taxonomy of Brucella. Open Veterinary Science Journal. 2010;4:85-101.
  7. 7. Scholz HC, Nöckler K, Göllner C, Bahn P, Vergnaud G, Tomaso H, Al Dahouk S, Kämpfer P, Cloeckaert A, Maquart M, Zygmunt MS, Whatmore AM, Pfeffer M, Huber B, Busse HJ, De BK. Brucella inopinata sp. nov., isolated from a breast implant infection. International Journal of Systematic and Evolutionary Microbiology. 2010;60:801-808.
  8. 8. López-Olvera JR, Vidal D, Vicente J, Pérez M, Luján L, Gortázar C. Serological survey of selected infectious diseases in mouflon (Ovis aries musimon) from south-central Spain. European Journal of Wildlife Research. 2009;55:75-79.
  9. 9. Baek BK, Lim CW, Rahman MS, Kim CH, Oluoch A, Kakoma I. Brucella abortus infection in indigenous Korean dogs. Canadian Journal of Veterinary Research. 2003;67:312.
  10. 10. Aznar MN, Samartino LE, Humblet MF, Saegerman C. Bovine brucellosis in Argentina and bordering countries: update. Transboundary and Emerging Diseases. 2014;61:121-133.
  11. 11. Cvetnić Z, Spicić S, Toncić J, Majnarić D, Benić M, Albert D, Thiébaud M, Garin-Bastuji B. Brucella suis infection in domestic pigs and wild boar in Croatia. Revue scientifique et technique (International Office of Epizootics). 2009;28:1057-1067.
  12. 12. Fosgate GT, Adesiyun AA, Hird DW, Hietala SK, Ryan J. Isolation of Brucella abortus biovar 1 from cattle and water buffaloes on Trinidad. Veterinary Record. 2002;151:272-273.
  13. 13. Gul ST, Khan A, Ahmad M, Hussain I. Seroprevalence of brucellosis and associated hemato-biochemical changes in Pakistani horses. Pakistan Journal of Agricultural Sciences. 2013;50:745-750.
  14. 14. Omer MK, Skjerve E, Woldehiwet Z, Holstad G. Risk factors for Brucella spp. infection in dairy cattle farms in Asmara, State of Eritrea. Preventive Veterinary Medicine. 2000;46:257-265.
  15. 15. Godfroid J. Brucellosis in wildlife. Revue Scientifique et Technique-Office International des Epizooties. 2002;21:277-286.
  16. 16. Tryland M, Nesbakken T, Robertson L, Grahek-Ogden D, Lunestad BT. Human pathogens in marine mammal meat–a northern perspective. Zoonoses and Public Health. 2014;61:377-394.
  17. 17. Tiller RV, Gee JE, Frace MA, Taylor TK, Setubal JC, Hoffmaster AR, De BK. Characterization of novel Brucella strains originating from wild native rodent species in North Queensland, Australia. Applied and Environmental Microbiology. 2010;76:5837-5845.
  18. 18. Teshome H, Molla B, Tibbo M. A seroprevalence study of camel brucellosis in three camel-rearing regions of Ethiopia. Tropical Animal Health and Production. 2003;35:381-390.
  19. 19. Gyuranecz M, Erdélyi K, Makrai L, Fodor L, Szépe B, Mészáros AR, Dán A, Dencso L, Fassang E, Szeredi L. Brucellosis of the European brown hare (Lepus europaeus). Journal of Comparative Pathology. 2011;145:1-5.
  20. 20. Her M, Cho DH, Kang SI, Lim JS, Kim HJ, Cho YS, Hwang IY, Lee T, Jung SC, Yoo HS. Outbreak of brucellosis in domestic elk in Korea. Zoonoses and Public Health. 2010;57:155-161.
  21. 21. Cvetnic Z, Mitak M, Ocepek M, Lojkic M, Terzic S, Jemersic L, Humski A, Habrun B, Sostaric B, Brstilo, Krt B, Garin-Bastuji B. Wild boars (Sus scrofa) as reservoirs of Brucella suis biovar 2 in Croatia. Acta Veterinaria Hungarica. 2003;51:465-473.
  22. 22. Eisenberg T, Hamann HP, Kaim U, Schlez K, Seeger H, Schauerte N, Melzer F, Tomaso H, Scholz HC, Koylass MS, Whatmore AM, Zschöck M. Isolation of potentially novel Brucella spp. from frogs. Applied and Environmental Microbiology. 2012;78:3753-3755.
  23. 23. Junaidu AU, Salihu MD, Ahmed F, Ambursa MA, Gulumbe ML. Brucellosis in local chickens in North Western Nigeria. International Journal of Poultry Science. 2006;5:547-549.
  24. 24. Kudi AC, Kalla DJU, Kudi MC, Yusuf H. Serological survey of brucellosis in traditionally managed domestic fowl in northern Guinea savannah, Nigeria. World’s Poultry Science Journal. 1997;53:287-289.
  25. 25. Nymo IH, Tryland M, Godfroid J. A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Veterinary Research. 2011;42:1-14.
  26. 26. Rich KM, Perry BD. The economic and poverty impacts of animal diseases in developing countries: new roles, new demands for economics and epidemiology. Preventive Veterinary Medicine. 2011;101:133-147.
  27. 27. Guzmán-Verri C, González-Barrientos R, Hernández-Mora G, Morales JA, Baquero-Calvo E, Chaves-Olarte E, Moreno E. Brucella ceti and brucellosis in cetaceans. Frontiers in Cellular and Infection Microbiology. 2012;2.
  28. 28. Bourg G, O’Callaghan D, Boschiroli ML. The genomic structure of Brucella strains isolated from marine mammals gives clues to evolutionary history within the genus. Veterinary Microbiology. 2007;125:375-380.
  29. 29. Dawson CE, Perrett LL, Stubberfield EJ, Stack JA, Farrelly SSJ, Cooley WA, Davison NJ, Quinney S. Isolation and characterization of Brucella from the lungworms of a harbor porpoise (Phocoena phocoena). Journal of Wildlife Diseases. 2008;44:237-246.
  30. 30. Blasco JM, Molina-Flores B. Control and eradication of Brucella melitensis infection in sheep and goats. Veterinary Clinics of North America: Food Animal Practice. 2011;27:95-104.
  31. 31. Olsen S, Tatum F. Bovine brucellosis. Veterinary Clinics of North America: Food Animal Practice. 2010;26:15-27.
  32. 32. Greece. Brucellosis program in 2011. Ministry of Rural Development and Food. 2012. http://ec.europa.eu/food/committees/regulatory/scfcah/animal_health/docs/0304072012_brucellosis_greece.pdf
  33. 33. MAGRAMA – Ministério de Agricultura Alimentación y Médio Amniente. Programa Nacional de erradicación de la brucelosis ovina y caprina (B. melitensis) peresentado para su cofinanciación en 2013. España.
  34. 34. Portugal. Brucelose dos pequenos ruminantes. Programa de erradicação para o ano 2012. Direção Geral de Veterinária. Lisboa. 2012.
  35. 35. SANCO. Relazione su un audit condotto in Italia dal 7 al 15 ottobre 2013 al fine di valutare i programmi di eradicazione della brucellosi di bovini, ovini e caprini. 2013.
  36. 36. Cowie CE, Marreos N, Gortázar C, Jaroso R, White PCL, Balseiro A. Shared risk factors for multiple livestock diseases: a case study of bovine tuberculosis and brucellosis. Research in Veterinary Science. 2014;97:491-497.
  37. 37. Holt HR, Eltholth MM, Hegazy YM, El-Tras WF, Tayel AA, Guitian J. Brucella spp. infection in large ruminants in an endemic area of Egypt: cross-sectional study investigating seroprevalence, risk factors and livestock owner’s knowledge, attitudes and practices (KAPs). BMC Public Health. 2011;11:341.
  38. 38. Musallam II, Shehada MA, Omar M, Guitian J. Cross-sectional study of brucellosis in Jordan: prevalence, risk factors and spatial distribution in small ruminants and cattle. Preventive Veterinary Medicine. 2015;118:387-396.
  39. 39. Mikolon AB, Gardner IA, De Anda JH, Hietala SK. Risk factors for brucellosis seropositivity of goat herds in the Mexicali Valley of Baja California, Mexico. Preventive Veterinary Medicine. 1998;37:185-195.
  40. 40. Coelho AM, Coelho AC, Roboredo M, Rodrigues J. A case–control study of risk factors for brucellosis seropositivity in Portuguese small ruminants herds. Preventive Veterinary Medicine. 2007;82:291-301.
  41. 41. Coelho AM, Coelho AC, Góis J, Pinto ML, Rodrigues J. Multifactorial correspondence analysis of risk factors for sheep and goat brucellosis seroprevalence. Small Ruminant Research. 2008;78:181-185.
  42. 42. Díez JG, Coelho AC. An evaluation of cattle farmers’ knowledge of bovine brucellosis in northeast Portugal. Journal of Infection and Public Health. 2013;6:363-369.
  43. 43. Borba MR, Stevenson MA, Goncalves VSP, Neto JF, Ferreira F, Amaku M, Telles EO, Santana, SS, Ferreira JCA, Lobo JR, Figueiredo VCF, Dias RA. Prevalence and risk-mapping of bovine brucellosis in Maranhao State, Brazil. Preventive Veterinary Medicine. 2013;110:169-176.
  44. 44. Ahmed MO, Elmeshri SE, Abuzweda AR, Blauo M, Abouzeed YM, Ibrahim A, Salem H, Alzwam F, Abid S, Elfahem A, Elrais A. Seroprevalence of brucellosis in animals and human populations in the western mountains region in Libya, December 2006–January 2008. Eurosurveillance. 2010;15:19625-19628.
  45. 45. Rahman MS, Faruk MO, Her M, Kim JY, Kang SI, Jung SC. Prevalence of brucellosis in ruminants in Bangladesh. Veterinarni Medicina. 2011;56:379-385.
  46. 46. Mai HM, Irons PC, Kabir J, Thompson PN. A large seroprevalence survey of brucellosis in cattle herds under diverse production systems in northern Nigeria. BMC Veterinary Research. 2012;8:144.
  47. 47. Trangadia B, Rana SK, Mukherjee F, Srinivasan VA. Prevalence of brucellosis and infectious bovine rhinotracheitis in organized dairy farms in India. Tropical Animal Health and Production. 2010;42:203-207.
  48. 48. Miller R, Nakavuma JL, Ssajjakambwe P, Vudriko P, Musisi N, Kaneene JB. The prevalence of brucellosis in cattle, goats and humans in rural Uganda: a comparative study. Transboundary and Emerging Diseases. 2015:1-5
  49. 49. Bertu WJ, Ajogi I, Bale JOO, Kwaga JKP, Ocholi RA. Sero-epidemiology of brucellosis in small ruminants in Plateau State, Nigeria. African Journal of Microbiology Research. 2010;4:1935-1938.
  50. 50. Bonfoh B, Kasymbekov J, Dürr S, Toktobaev N, Doherr MG, Schueth T, Zinsstag J, Schuelling E. Representative Seroprevalences of Brucellosis in Humans and Livestock in Kyrgyzstan. EcoHealth. 2011;9:132-138.
  51. 51. Tahamtan Y, Namavari MM, Mohammadi G, Jula GM. Prevalence of brucellosis in horse north-east of Iran. Journal of Equine Veterinary Science. 2010;30:376-378.
  52. 52. Ehizibolo DO, Gusi AM, Ehizibolo PO. Serologic prevalence of brucellosis in horse stables in two northern states of Nigeria. Journal of Equine Science. 2011;22:17.
  53. 53. Wadood F, Ahmad M, Khan A, Gul ST, Rehman N. Seroprevalence of brucellosis in horses in and around Faisalabad. Pakistan Veterinary Journal. 2009;29:196-198.
  54. 54. Mosallanejad B, Najafabadi MG, Avizeh R, Mohammadian N. A serological survey on Brucella canis in companion dogs in Ahvaz. Iranian Journal of Veterinary Research. 2009;10:383-386.
  55. 55. López G, Ayala SM, Efron AM, Gómez CF, Lucero NE. A serological and bacteriological survey of dogs to detect Brucella infection in Lomas de Zamora, Buenos Aires province. Revista Argentina de Microbiologia. 2009;41:97-101.
  56. 56. Cadmus SIB, Adesokan HK, Ajala OO, Odetokun WO, Perrett LL, Stack JA. Seroprevalence of Brucella abortus and B. canis in household dogs in southwestern Nigeria: a preliminary report: short communication. Journal of the South African Veterinary Association. 2011;82:56-57.
  57. 57. Adesiyun AA, Abdullahi SU, Adeyanju JB. Prevalence of Brucella abortus and Brucella canis antibodies in dogs in Nigeria. Journal of Small Animal Practice. 1986;27:31-37.
  58. 58. Behzadi MA, Mogheiseh A. Epidemiological survey of Brucella canis infection in different breeds of dogs in Fars province, Iran. Pakistan Veterinary Journal. 2011;31:140.
  59. 59. Davis DS, Boeer WJ, Mims JP, Heck FC, Adams LG. Brucella abortus in coyotes I. A serologic and bacteriologic survey eastern Texas. Journal of Wildlife Diseases. 1979;15:367-372.
  60. 60. Leuenberger R, Boujon P, Thür B, Miserez R, Garin-Bastuji B, Rüfenacht J, Stärk KD. Prevalence of classical swine fever, Aujeszky’s disease and brucellosis in a population of wild boar in Switzerland. The Veterinary Record. 2007;160:362-368.
  61. 61. Van Der Leek ML, Becker HN, Humphrey P, Adams CL, Belden RC, Frankenberger WB, Nicoletti PL. Prevalence of Brucella sp. antibodies in feral swine in Florida. Journal of Wildlife Diseases. 1993;29:410-415.
  62. 62. Nielsen O, Stewart RE, Nielsen K, Measures L, Duignan P. Serologic survey of Brucella spp. antibodies in some marine mammals of North America. Journal of Wildlife Diseases. 2001;37:89.
  63. 63. Tryland M, Sørensen KK, Godfroid J. Prevalence of Brucella pinnipediae in healthy hooded seals (Cystophora cristata) from the North Atlantic Ocean and ringed seals (Phoca hispida) from Svalbard. Veterinary Microbiology. 2005;105:103.
  64. 64. Garín-Bastuji B. Brucelloses bovine, ovine et caprine: contrôle et prevention. Point Vet. 1993;25:15-22.
  65. 65. Estein SM, Cassataro J, Vizcaíno N, Zygmunt M, Cloeckaert A, Bowden RA. The recombinant Omp31 from Brucella melitensis alone or associated with rough lipopolysaccharide induces protection against Brucella ovis infection in BALB/c mice. Microbes and Infection. 2003;5:85-93.
  66. 66. OIE World Organisation for Animal Health. Porcine brucellosis. Chapter 2.8.5. OIE Terrestrial Manual. 2009. p. 1-7, Office International des Épizooties.
  67. 67. Memish Z. Brucellosis control in Saudi Arabia: prospects and challenges. Journal of Chemotherapy. 2001;13:11-17.
  68. 68. Paolicchi FA, Terzolo HR, Campero CM. Isolation of Brucella suis from the semen of a ram. Veterinary Record. 1993;132:67.
  69. 69. Metcalf HE, Luchsinger DW, Ray WC. Brucellosis. In: Beran GW, Steele JH, editors. Handbook of Zoonoses: Section A. Bacterial, Rickettsial, Chlamydial, and Mycotic. Florida: CRC Press; 1994. p. 9-38.
  70. 70. AHAW – Scientific Opinion of the Panel on Animal Health and Welfare (AHAW) on a request from the Commission on porcine brucellosis (Brucella suis). The EFSA Journal. 2009;1144:1-112.
  71. 71. Acha PN, Szyfres B, editors. Brucellosis. Zoonoses and Communicable Diseases Common to Man and Animals: Bacterioses and Mycoses. 3rd ed. Pan American Sanitary Bureau. Pan American Health Organization. Washington. 2001. p. 40-66.
  72. 72. Alton GG. Brucella melitensis. In: Nielsen K, Duncan JR, editors. Animal Brucellosis. Florida: CRC Press; 1990.
  73. 73. Ashagrie T, Deneke Y, Tolosa T. Seroprevalence of caprine brucellosis and associated risk factors in South Omo Zone of Southern Ethiopia. African Journal of Microbiological Research. 2011;5:1682-1685.
  74. 74. Muma JB, Samui KL, Siamudaala VM, Oloya J, Matop G, Omer MK, Munyeme M, Mubita C, Skjerve E. Prevalence of antibodies to Brucella spp. and individual risk factors of infection in traditional cattle, goats and sheep reared in livestock–wildlife interface areas of Zambia. Tropical Animal Health and Production. 2006;38:195-206.
  75. 75. Sanogo M, Abatih E, Thys E, Fretin D, Berkvens D, Saegerman C. Risk factors associated with brucellosis seropositivity among cattle in the central savannah-forest area of Ivory Coast. Preventive Veterinary Medicine. 2012;107:51-56.
  76. 76. Stringer LA, Guitian FJ, Abernethy DA, Honhold NH, Menzies FD. Risk associated with animals moved from herds infected with brucellosis in Northern Ireland. Preventive Veterinary Medicine. 2008;84:72-84.
  77. 77. Solorio-Rivera JL, Segura-Correa JC, Sánchez-Gil LG. Seroprevalence of and risk factors for brucellosis of goats in herds of Michoacan, Mexico. Preventive Veterinary Medicine. 2007;82:282-290.
  78. 78. Al-Majali AM, Al-Qudah KM, Al-Tarazi YH, Al-Rawashdeh OF. Risk factors associated with camel brucellosis in Jordan. Tropical Animal Health and Production. 2008;40:193-200.
  79. 79. Muñoz PM, Boadella M, Arnal M, de Miguel MJ, Revilla M, Martínez D, Vicente J, Acevedo P, Oleaga A, Ruiz-Fons F, Marín CM, Prieto JM, de la Fuente J, Barral M, Barberán M, de Luco DF, Blasco JM, Gortázar C. Spatial distribution and risk factors of Brucellosis in Iberian wild ungulates. BMC Infectious Diseases. 2010;10:46.
  80. 80. Bekele M, Mohammed H, Tefera M, Tolosa T. Small ruminant brucellosis and community perception in Jijiga district, Somali Regional State, eastern Ethiopia. Tropical Animal Health and Production. 2011;43:893-898.
  81. 81. Matope G, Bhebhe E, Muma JB, Oloya J, Madekurozwa RL, Lund A, Skjerve E. Seroprevalence of brucellosis and its associated risk factors in cattle from smallholder dairy farms in Zimbabwe. Tropical Animal Health and Production. 2011;43:975-982.
  82. 82. Petersen E, Rajashekara G, Sanakkayala N, Eskra L, Harms J, Splitter G. Erythritol triggers expression of virulence traits in Brucella melitensis. Microbes and Infection. 2013;15:440-449.
  83. 83. Alavi-Shoushtari SM, Zeinali A. Responses of female lambs to Rev-1 vaccination. Preventive Veterinary Medicine. 1995;21:289-297.
  84. 84. Megersa B, Biffa D, Abunna F, Regassa A, Godfroid J, Skjerve E. Seroprevalence of brucellosis and its contribution to abortion in cattle, camel, and goat kept under pastoral management in Borana, Ethiopia. Tropical Animal Health and Production, 2011;43:651-656.
  85. 85. Talukder BC, Samad MA, Rahman AKMA. Comparative evaluation of commercial serodiagnostic tests for the seroprevalence study of brucellosis in stray dogs in Bangladesh. Bangladesh Journal of Veterinary Medicine. 2012;9:79-83.
  86. 86. Coelho AM, Díez JG, Coelho AC. Brucelosis en pequeños rumiantes: efecto de la aplicación de un programa especial de vacunación en masa con REV-1. REDVET. Revista Electrónica de Veterinaria. 2013;14:1-16.
  87. 87. León F. Brucellosis ovina y caprina. Ed. Office International des Epizooties – OIE. Francia; 1993.451p
  88. 88. Jackson R, Pite L, Kennard R, Ward D, Stack J, Domi X, Rami A, Dedushaj I. Survey of the seroprevalence of brucellosis in ruminants in Kosovo. Veterinary Record. 2004;154:747-751.
  89. 89. Musallam II, Shehada MA, Omar M, Guitian J. Cross-sectional study of brucellosis in Jordan: prevalence, risk factors and spatial distribution in small ruminants and cattle. Preventive Veterinary Medicine. 2015;118:387-396.
  90. 90. OIE World Organisation for Animal Health. Caprine and Ovine brucellosis. In: Manual of Diagnostic Test and Vaccines for Terrestrial Animals; 2008. p. 974-982.
  91. 91. Blasco JM. Control and eradication programmes of brucellosis in small ruminants and cattle. Implementation of Control and Eradication Programs in Animals. Zaragoza; Curso de Epidemiologia; 2001.
  92. 92. Ferreira A, Ferreira C. Doenças infecto-contagiosas dos animais domésticos. Lisboa: Fundação Calouste Gulbenkian; 1990. p. 125-142.
  93. 93. Louzã AC. Brucelose - Modelo de zoonose de impacto sócio-económico. Parte I. Veterinária Técnica. 1993;43:21-28.
  94. 94. Young EJ. Brucella species. In: Mandell GL, Bennet JE, Dolin R, editors. Principles and Practice of Infectious Diseases. New York: Churchill Livingstone; 1995. p. 2053-2060.
  95. 95. Boadella M, Carta T, Oleaga Á, Pajares G, Muñoz M, Gortázar C. Serosurvey for selected pathogens in Iberian roe deer. BMC Veterinary Research. 2010;6:51.
  96. 96. Grégoire F, Mousset B, Hanrez D, Michaux C, Walravens K, Linden A. A serological and bacteriological survey of brucellosis in wild boar (Sus scrofa) in Belgium. BMC Veterinary Research. 2012;8:80.
  97. 97. Higgins J, Stuber T, Quance C, Edwards WH, Tiller RV, Linfield T, Rhyan J, Berte A, Harris B. Molecular epidemiology of Brucella abortus isolates from cattle, elk, and bison in the United States, 1998 to 2011. Applied and Environmental Microbiology. 2012;78:3674-3684.
  98. 98. Meng XJ, Lindsay DS, Sriranganathan N. Wild boars as sources for infectious diseases in livestock and humans. Philosophical Transactions of the Royal Society B: Biological Sciences. 2009;364:2697-2707.
  99. 99. Ahmed RA, Munir MA. Epidemiological investigations of brucellosis in horses, dogs, cats and poultry. Pakistan Veterinary Journal. 1995;15:85-88.
  100. 100. Sharma VD, Sethi MS, Yadav MP, Dube DC. Sero-epidemiologic investigations on brucellosis in the states of Uttar Pradesh (U.P.) and Delhi (India). International Journal of Zoonoses. 1979;6:75-81.
  101. 101. Grilló MJ, Barberán M, Blasco JM. Transmission of Brucella melitensis from sheep to lambs. Veterinary Record. 1997;140:602-605.
  102. 102. Edmondson MA, Roberts JF, Baird AN, Bychawski S, Pugh DG. Theriogenology of sheep and goats. In: Pugh DG, Baird AN, editors. Sheep and Goat Medicine. Missouri: Elsevier; 2012. p. 158-238.
  103. 103. Díaz AE. Epidemiology of brucellosis in domestic animals caused by Brucella melitensis, Brucella suis and Brucella abortus. Revue scientifique et technique (International Office of Epizootics). 2013;32:43-51.
  104. 104. Muma JB, Samui KL, Oloya J, Munyeme M, Skjerve E. Risk factors for brucellosis in indigenous cattle reared in livestock–wildlife interface areas of Zambia. Preventive Veterinary Medicine. 2007;80:306-317.
  105. 105. Nahar A, Ahmed MU. Sero-prevalence study of brucellosis in cattle and contact human in Mymensingh district. Bangladesh Journal of Veterinary Medicine. 2009;7:269-274.
  106. 106. Corbel MJ, Brinley-Morgan WJ. Genus Brucella. In: Krieg NR, Holt JG, editors. Bergey’s Manual of Systemic Bacteriology. London: Williams e Wilkins; 1994. p. 377-388.
  107. 107. Xiang F, Xia Z, Wu Q, Chen Y, Yu J, Wan J. Seroepidemiology of canine brucellosis in Beijing, China. Turkish Journal of Veterinary and Animal Sciences. 2013;37:28-42.
  108. 108. Cameron HS, Hughes EH, Gregory PW. Genetic resistance to brucellosis in swine. Journal of Animal Science. 1942;1:106-110.
  109. 109. Lovejoy GS, Carver HD, Moseley IK, Hicks M. Serosurvey of dogs for Brucella canis infection in Memphis, Tennessee. American Journal of Public Health. 1976;66:175-176.
  110. 110. Ibrahim N, Belihu K, Lobago F, Bekana M. Sero-prevalence of bovine brucellosis and its risk factors in Jimma zone of Oromia Region, South-western Ethiopia. Tropical Animal Health and Production. 2010;42:35-40.
  111. 111. Teklue T, Tolosa T, Tuli G, Beyene B, Hailu B. Sero-prevalence and risk factors study of brucellosis in small ruminants in Southern Zone of Tigray Region, Northern Ethiopia. Tropical Animal Health and Production. 2013;45:1809-1815.
  112. 112. Al-Majali AM, Majok AA, Amarin NM, Al-Rawashdeh OF. Prevalence of, and risk factors for, brucellosis in Awassi sheep in Southern Jordan. Small Ruminant Research. 2007;73:300-303.
  113. 113. Al-Majali AM. Seroepidemiology of caprine brucellosis in Jordan. Small Ruminant Research. 2005;58:13-18.
  114. 114. Reviriego FJ, Moreno MA, Domínguez L. Risk factors for brucellosis seroprevalence of sheep and goat flocks in Spain. Preventive Veterinary Medicine. 2000;44:167-173.
  115. 115. CFSPH-Center for Food Security and Public Health. Brucellosis, 2009. www.cfsph.iastate.edu/Factsheets/pdfs/brucellosis.pdf
  116. 116. Godfroid J, Scholz HC, Barbier T, Nicolas C, Wattiau P, Fretin D, Whatmore AM, Cloeckaert A, Blasco JM, Moriyon I, Saegerman C, Muma JB, Al Dahouk S, Neubauer H, Letesson JJ. Brucellosis at the animal/ecosystem/human interface at the beginning of the 21st century. Preventive Veterinary Journal. 2011;102:118–131.
  117. 117. Mainar-Jaime RC, Vázquez-Boland JA. Associations of veterinary services and farmer characteristics with the prevalences of brucellosis and border disease in small ruminants in Spain. Preventive Veterinary Medicine. 1999;40:193-205.
  118. 118. Blasco JM. A review of the use of B. melitensis Rev. 1 vaccine in adult sheep and goats. Preventive Veterinary Medicine. 1997;31:275-283.
  119. 119. Ramírez H, Calle E, Echevarría C, Morales C. Prevalencia de brucelosis canina en dos distritos de la Provincia Constitucional del Callao. Revista de Investigaciones Veterinarias del Perú. 2006;17:39-43.
  120. 120. Castrillón-Salazar L, Giraldo-Echeverri CA, Sánchez-Jiménez MM, Olivera-Angel M. Factors associated with Brucella canis seropositivity in kennels of two regions of Antioquia, Colombia. Cadernos de Saúde Pública. 2013;29:1955-1973.
  121. 121. Hollett RB. Canine brucellosis: outbreaks and compliance. Theriogenology. 2006;66:575-587.
  122. 122. Garin-Bastuji B, Hars J, Drapeau A, Cherfa MA, Game Y, Le Horgne JM, Rautureau S, Maucci E, Pasquier JJ, Jay M, Mick V. Reemergence of Brucella melitensis infection in wildlife, France. Emerging Infectious Diseases. 2014;20:1570.
  123. 123. Cvetnic Z, Spicic S, Curic S, Jukic B, Lojkic M, Albert D, Thiébaud M, Garin-Bastuji B. Isolation of Brucella suis biovar 3 from horses in Croatia. Veterinary Record-English Edition. 2005;156:584-585.
  124. 124. Corbel MJ. Brucellosis: an overview. Emerging Infectious Disease. 1997;3:213-221.
  125. 125. Aguiar DM, Cavalcante GT, Labruna MB, Vasconcellos SA, Rodrigues AAR, Morais ZM, Camargo LMA, Gennari SM. Risk factors and seroprevalence of Brucella spp. in cattle from western Amazon, Brazil. Arquivos do Instituto Biologico, Sao Paulo. 2007;74:301-305.
  126. 126. Fretin D, Mori M, Czaplicki G, Quinet C, Maquet B, Godfroid J, Saegerman C. Unexpected Brucella suis biovar 2 infection in a dairy cow, Belgium. Emerging Infectious Diseases. 2013;19:2053.
  127. 127. Al-Majali AM, Talafha AQ, Ababneh MM, Ababneh MM. Seroprevalence and risk factors for bovine brucellosis in Jordan. Journal of Veterinary Science. 2009;10:61-65.
  128. 128. Islam MA, Khatun MM, Werre SR, Sriranganathan N, Boyle SM. A review of Brucella seroprevalence among humans and animals in Bangladesh with special emphasis on epidemiology, risk factors and control opportunities. Veterinary Microbiology. 2013;166:317-326.
  129. 129. Sammartino LE, Gil A, Elzer P. Capacity building for surveillance and control of bovine and caprine brucellosis. In: FAO Animal Production and Health Proceedings - AO/WHO/OIE Expert and Technical Consultation. Rome. 2006; 7:55
  130. 130. Al-Talafhah AH, Lafi SQ, Al-Tarazi Y. Epidemiology of ovine brucellosis in Awassi sheep in Northern Jordan. Preventive Veterinary Medicine. 2003;60:297-306.
  131. 131. Kabagambe EK, Elzer PH, Geaghan JP, Opuda-Asibo J, Scholl DT, Miller JE. Risk factors for Brucella seropositivity in goat herds in Eastern and Western Uganda. Preventive Veterinary Medicine. 2001;52:91-108.
  132. 132. Silva I, Dangolla A, Kulachelvy K. Seroepidemiology of Brucella abortus infection in bovids in Sri Lanka. Preventive Veterinary Medicine. 2000; 46:51-59.
  133. 133. Mekonnen H, Kalayou S, Kyule M. Serological survey of bovine brucellosis in barka and arado breeds (Bos indicus) of Western Tigray, Ethiopia. Preventive Veterinary Medicine. 2010;94:28-35.
  134. 134. Makita K, Fèvre EM, Waiswa C, Eisler MC, Thrusfield M, Welburn SC. Herd prevalence of bovine brucellosis and analysis of risk factors in cattle in urban and peri-urban areas of the Kampala economic zone, Uganda. BMC Veterinary Research. 2011;7:60.
  135. 135. Kataria AK, Gahlot AK. Evaluation of oxidative stress in Brucella infected cows. Journal of Stress Physiology and Biochemistry. 2010;6:2.
  136. 136. Henriques HS. Epidemiologia da brucelose em pequenos ruminantes. Sociedade Portuguesa de Ovinotecnia e Caprinotecnia. Proceeding of II Jornadas sobre Sanidade Ovina e Caprina. Bragança. 1990;21-28.
  137. 137. Izquierdo de la Hoya S, Villanueva M. Transmisión de la brucelosis entre explotaciones ovinas próximas. Proceedings of the XXI Jornadas Científicas de la Sociedad Española de Ovinotecnia y Caprinotecnia (SEOC). Logroño, España 1996; 101-105.
  138. 138. Crespo-León F. Brucellosis ovina y caprina. Paris: OIE. 1994; p. 451.
  139. 139. Wickramasuriya UGJS, Peiris GS, Kendaragama KMT, Karunadasa WM. A survey on the incidence of bovine brucellosis in three districts in Sri Lanka. Sri Lanka Veterinary Journal. 1983;31:27-31.
  140. 140. Quinn PJ, Markey BK. Disinfection and disease prevention in veterinary medicine. In: Block SS, editor. Disinfection, Sterilization and Preservation. 5th ed. Philadelphia: Lippincott Williams and Wilkins; 2001. p. 1069-1104.
  141. 141. de Paula Dreer MK, Gonçalves DD, da Silva Caetano IC, Gerônimo E, Menegas PH, Bergo D, Lopes-Mori FM, Benitez A, Freitas JC, Evers F, Navarro I, Almeida Martins L. Toxoplasmosis, leptospirosis and brucellosis in stray dogs housed at the shelter in Umuarama municipality, Paraná, Brazil. Journal of Venomous Animals and Toxins including Tropical Diseases. 2013;19:23.
  142. 142. Garín-Bastuji B. Le dépistage de la brucellose des ruminants et ses difficultés. Les cas des sérologies atypiques en brucellose bovine. Point Veterinaire 1993;25:23-32.
  143. 143. Ferron A. Bactériologie Médicale à l’usage des étudients en médecine. La Madeleine Editions. 989.
  144. 144. Godfroid J, Käsbohrer A. Brucellosis in the European Union and Norway at the turn of the twenty-first century. Veterinary Microbiology. 2002;90:135-145.
  145. 145. Renukaradhya GJ, Isloor S, Rajasekhar M. Epidemiology, zoonotic aspects, vaccination and control/eradication of brucellosis in India. Veterinary Microbiology. 2002;90:183-195.
  146. 146. Gortázar C, Ferroglio E, Höfle U, Frölich K, Vicente J. Diseases shared between wildlife and livestock: a European perspective. European Journal of Wildlife Research. 2007;53:241-256.
  147. 147. Gortázar C, Acevedo P, Ruiz-Fons F, Vicente J. Disease risks and overabundance of game species. European Journal of Wildlife Research. 2006;2:81-87.
  148. 148. Godfroid J, Garin Bastuji B, Saegerman C, Blasco Martínez, JM. Brucellosis in terrestrial wildlife. Revue Scientifique et Technique. 2013;32:27-42.
  149. 149. Godfroid J, Cloeckaert A, Liautard JP, Kohler S, Fretin D, Walravens K, Garín Bastuji B, Letesson JJ. From the discovery of the Malta fever’s agent to the discovery of a marine mammal reservoir, brucellosis has continuously been a re-emerging zoonosis. Veterinary Research. 2005;36:313-326.
  150. 150. Garin-Bastuji B, Hars J, Drapeau A, Cherfa MA, Game Y, Le Horgne JM, Rautureau S, Maucci E, Pasquier JJ, Jay M, Mick V. Reemergence of Brucella melitensis in wildlife, France. Emerging Infectious Disease. 2014;20:157-1571.
  151. 151. Conner MM, Ebinger MR, Blanchong JA, Cross PC. Infectious disease in cervids of North America. Annals of the New York Academy of Sciences. 2008;1134:146-172.
  152. 152. Godfroid J. Brucellosis in wildlife. Revue Scientifique et Technique-Office International des Épizooties. 2002;21:277-286.
  153. 153. Godfroid J, Michel P, Uytterhaegen L, Desmedt C, Rasseneur F, Boelaert F, Saegerman C, Patigny X. Brucellose enzootique a Brucella suis biotype 2 chez le sanglier (Sus scrofa) en Belgique, 1994.
  154. 154. Ross HM, Foster G, Reid RJ, Jahans KL, MacMillan AP. Brucella species infection in sea-mammals. Veterinary Record. 1994;134:359-359.
  155. 155. Tachibana M, Watanabe K, Kim S, Omata Y, Murata K, Hammond T, Watarai M. Antibodies to Brucella spp. in Pacific bottlenose dolphins from the Solomon Islands. Journal of Wildlife Diseases. 2006;42:412-414.
  156. 156. Hernández-Mora G, González-Barrientos R, Morales JA, Chaves-Olarte E, Guzmán-Verri C, Baquero-Calvo E, De-Miguel MJ, Marín, CM, Blasco JM, Moreno E. Neurobrucellosis in stranded dolphins, Costa Rica. Emerging Infectious Diseases. 2008;14:1430.
  157. 157. Van Bressem MF, Raga JA, Di Guardo G, Jepson PD, Duignan PJ, Siebert U, Barrett T, Santos MC, Moreno IB, Siciliano S, Aguilar A, Van Waerebeek K. Emerging infectious diseases in cetaceans worldwide and the possible role of environmental stressors. Diseases of Aquatic Organisms. 2009;86:143-157.
  158. 158. Thakur SD, Vaid RK, Panda AK, Saini Y. Marine mammal brucellosis: a new dimension to an old zoonosis. Current Science. 2012;103:902-910.
  159. 159. Ewalt DR, Payeur JB, Rhyan JC, Geer PL. Brucella suis biovar 1 in naturally infected cattle: a bacteriological, serological, and histological study. Journal of Veterinary Research. 1997;53:405-410.
  160. 160. González-Barrientos R, Morales JA, Hernández-Mora G, Barquero-Calvo E, Guzmán-Verri C, Chaves-Olarte E, Moreno E. Pathology of striped dolphins (Stenella coeruleoalba) infected with Brucella ceti. Journal of Comparative Pathology. 2010;142:347-352.
  161. 161. Foster G, MacMillan AP, Godfroid J, Howie F, Ross HM, Cloeckaert A, Reid RJ, Brew S, Patterson IAP. A review of Brucella sp. infection of sea mammals with particular emphasis on isolates from Scotland. Veterinary Microbiology. 2002;90:563-580.
  162. 162. Foster G, Jahans KL, Reid RJ, Ross HM. Isolation of Brucella species from cetaceans, seals and an otter. Veterinary Record. 1996;138:583-586.
  163. 163. Muñoz PM, García-Castrillo G, López-García P, González-Cueli JC, De Miguel MJ, Marín CM, Barberán M, Blasco JM. Isolation of Brucella species from a live-stranded striped dolphin (Stenella coeruleoalba) in Spain. Veterinary Record. 2006;158:450.
  164. 164. Ross HM, Jahans KL, MacMillan AP, Reid RJ, Thompson PM, Foster G. Brucella species infection in North Sea seal and cetacean populations. Veterinary Record. 1996;138:647-648.
  165. 165. Dawson CE, Perrett LL, Stubberfield EJ, Stack JA, Farrelly SSJ, Cooley WA, Davison NJ, Quinney S. Isolation and characterization of Brucella from the lungworms of a harbor porpoise (Phocoena phocoena). Journal of Wildlife Diseases. 2008;44:237-246.
  166. 166. Moreno E. Retrospective and prospective perspectives on zoonotic brucellosis. Frontiers in Microbiology. 2014;5:213.
  167. 167. Tabak F, Hakko E, Mete B, Ozaras R, Mert A, Ozturk R. Is family screening necessary in brucellosis?. Infection. 2008;36:575-577.
  168. 168. Lindahl E, Sattorov N, Boqvist S, Sattori I, Magnusson U. Seropositivity and risk factors for Brucella in dairy cows in urban and peri-urban small-scale farming in Tajikistan. Tropical Animal Health and Production. 2014;46:563-569.
  169. 169. El-Daher N, Na’Was T, Al-Qaderi S. The effect of the pH of various dairy products on the survival and growth of Brucella melitensis. Annals of Tropical Medicine and Parasitology. 1990;84:523-528.
  170. 170. Dhanashekar R, Akkinepalli S, Nellutla A. Milk-borne infections. An analysis of their potential effect on the milk industry. Germs. 2012;2:101.
  171. 171. Nicoletti P. Relationship between animal and human disease. In: Young EJ, Corbel MJ, editors. Brucellosis: Clinical and Laboratory Aspects. Boca Raton: CRC Press; 1989.
  172. 172. Regulation (EC) Nº 853/2004 of the European Parliament and the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. Official Journal of the European Union. 2004; L 39.
  173. 173. Pessegueiro P, Barata C, Correia J. Brucelose-uma revisão sistematizada. Medicina Interna. 2003;10:91-100.
  174. 174. Ali S, Ali Q, Neubauer H, Melzer F, Elschner M, Khan I, Nji Abatih E, Ullah N, Irfan M, Akhter M. Seroprevalence and risk factors associated with brucellosis as a professional hazard in Pakistan. Foodborne Pathogens and Disease. 2013;10:500-505.
  175. 175. Luce R, Snow J, Gross D, Murphy T, Grandpre J, Daley WR, Brudvig JM, Ari MD, Harris L, Clark TA. Brucellosis seroprevalence among workers in at-risk professions: Northwestern Wyoming, 2005 to 2006. Journal of Occupational and Environmental Medicine. 2012;54:1557-1560.
  176. 176. Traxler RM, Lehman MW, Bosserman EA, Guerra MA, Smith TL. A literature review of laboratory-acquired brucellosis. Journal of Clinical Microbiology. 2013;51:3055-3062.
  177. 177. Lachapelle JM. Biologic causes of occupational dermatoses. In: Kanerva’s Occupational Dermatology. Berlin: Springer; 2012. p. 231-245.
  178. 178. Waltzek TB, Cortés-Hinojosa G, Wellehan Jr JFX, Gray GC. Marine mammal zoonoses: a review of disease manifestations. Zoonoses and Public Health. 2012;59:521-535.

Written By

Ana Cláudia Coelho, Juan García Díez and Adosinda Maria Coelho

Submitted: 15 December 2014 Reviewed: 24 August 2015 Published: 19 November 2015