The background and Terms of Reference (ToR) as provided by the European Commission for the present document are reported in section 1.2 of the scientific opinion on the ad hoc methodology followed for the assessment of the disease to be listed and categorised according to the criteria of Article 5, Annex IV according to Article 9, and 8 within the Animal Health Law (AHL) framework (EFSA AHAW Panel, ).
Interpretation of the Terms of ReferenceThe interpretation of the ToR is as in section 1.2 of the scientific opinion on the ad hoc methodology followed for the assessment of the disease to be listed and categorised according to the criteria of Article 5, Annex IV according to Article 9, and 8 within the Animal Health Law (AHL) framework (EFSA AHAW Panel, ).
The present document reports the results of assessment on the infection with Brucella abortus, Brucella melitensis and Brucella suis according to the criteria of the AHL articles as follows:
- Article 7: the infection with B. abortus, B. melitensis and B. suis profile and impacts;
- Article 5: eligibility of the infection with B. abortus, B. melitensis and B. suis to be listed;
- Article 9: categorisation of the infection with B. abortus, B. melitensis and B. suis according to disease prevention and control rules as in Annex IV;
- Article 8: list of animal species related to the infection with B. abortus, B. melitensis and B. suis.
The methodology applied in this opinion is described in detail in a dedicated document about the ad hoc method developed for assessing any animal disease for the listing and categorisation of diseases within the AHL framework (EFSA AHAW Panel, ).
Assessment Assessment according to Article 7 criteriaThis section presents the assessment of the infection with B. abortus, B. melitensis and B. suis according to the Article 7 criteria of the AHL and related parameters (see Table of the opinion on methodology (EFSA AHAW Panel, )), based on the information contained in the fact-sheet as drafted by the selected disease scientist (see section 2.1 of the scientific opinion on the ad hoc methodology) and amended by the EFSA Panel on Animal Health and Welfare (AHAW).
Article 7(a) Disease Profile Article 7(a)(i) Animal species concerned by the disease Susceptible animal speciesParameter 1 – Naturally susceptible wildlife species (or family/orders)
B. abortus/B. melitensis
Most if not all wild mammals are theoretically susceptible, but ungulates are the most frequently affected wild animals, usually as a consequence of contact with infected livestock in extensive breeding systems. Infections have been reported in the one-humped (Camelus dromedarius) and two-humped (Camelus bactrianus) camels, llama (Lama glama), alpaca (Vicugna pacos), guanaco (Lama guanicoe), vicuña (Vicugna vicugna), water buffalo (Bubalus bubalis), European (Bison bonasus) and American bison (Bison bison), yak (Bos grunniens), African buffalo (Syncerus caffer), red deer (Cervus elaphus), moose (Alces alces), wild boar (Sus scrofa) and several species of African antelope, such as Kafue lechwe antelope (Kobus leche kafuensis), Arabian oryx (Oryx leucoryx) and sable antelope (Hippotragus niger) (Díaz-Aparicio, ; Godfroid et al., ). Sporadic cases have been reported also in carnivores like opossums (family Didelphidae), raccoons (Procyon lotor), coyotes (Canis latrans), foxes (Vulpes vulpes) and wolves. In the European Union (EU), brucellosis due to both bacterial species has been reported only sporadically in wild ungulates such as ibex (Capra ibex), chamois (Rupicapra sp.), Spanish ibex (Capra pyrenaica) and red deer (Cervus elaphus) (Gortázar et al., ; Muñoz et al., ; Mick et al., ). However, these wild animals are considered occasional end hosts of brucellosis transmitted from infected livestock, rather than a true reservoir of the disease (Gortázar et al., ).
B. suis
This bacterial species is composed by five biovars (named from 1 to 5), with biovars 1, 2 and 3 causing brucellosis in domestic swine. This complexity accounts for the different types of epidemiological situations occurring in non-porcine and wild species. B. suis infection can occur in animals that are not the natural host of the particular infection through the ingestion of contaminated materials or by cohabitation with infected natural hosts. As examples, arctic foxes (Vulpes lagopus) and wolves (Canis lupus) may be infected by B. suis biovar 4 after eating infected reindeer. B. suis biovar 4 is a zoonotic agent and also causes a serious disease in wild or domesticated reindeer or caribou (Rangifer tarandus and its various subspecies) throughout the Arctic region, including Siberia, Canada and Alaska. Dogs and rodents, such as rats and mice, may acquire other B. suis biovars by cohabitation with infected hosts. In some cases, wildlife species are natural hosts for some B. suis biovars, as it has been reported in the former Soviet Union and the Baltic countries, where small rodents are infected by B. suis biovar 5 (EFSA, ; OIE, ). Infection by B. suis biovar 2 (which is a very rare zoonotic agent, see below) is reported frequently in the EU affecting the Eurasian wild boar (Sus scrofa) and the European brown hare (Lepus europaeus). Both wild species can transmit the infection to domestic pigs in outdoor farms, thus playing a relevant role as a reservoir of porcine brucellosis (EFSA, ; Muñoz et al., ). Outside the EU, feral pigs and peccaries (Tayassuidae) may maintain B. suis biovars 1 and 3 (both are important zoonotic agents) with the ensuing risks for both pigs and humans. These two last biovars are considered not to exist in the EU, with a unique and very rare exception reported for biovar 3 in horses in Croatia (Cvetnic et al., ), although this strain was finally identified as belonging to the biovar 1 (Fretin et al., ).
Parameter 2 – Naturally susceptible domestic species (or family/orders)
B. abortus
Cattle (primarily) and sheep and goats (very rarely). Sporadic cases have been reported also in farmed water buffalo (Bubalus bubalis) and, even more rarely, in horses and pigs (Cvetnic et al., ; OIE, ). Dogs belonging to infected herds are also found infected frequently. Outside the EU, in addition to the above domestic species, yak (Bos grunniens) and camels (both species) can be also found infected in mixed breeding systems (OIE, ).
B. melitensis
Sheep and goats (primarily) and cattle (less frequently and only when bovines and cattle cohabit with small ruminants (Verger et al., ; OIE, )). Sporadic cases have been reported in farmed water buffaloes (Bubalus bubalis) and, more rarely, in horses and pigs (Cvetnic et al., ; OIE, ). Dogs belonging to infected flocks are also found infected frequently. Outside the EU, in addition to these domestic species, yak (Bos grunniens) and camels (both species) can be also found infected (OIE, ).
B. suis
As indicated above, the biovars 1, 2 and 3 infect domestic swine and are responsible for porcine brucellosis. B. suis biovar 2 infection is restricted to Continental Europe, and widespread in wildlife (see above) causing sporadic outbreaks in domestic swine reared in outdoor breeding systems. Very rare cases of B. suis biovar 2 infection have been reported in cattle, not followed by clinical signs (Fretin et al., ; Szulowski et al., ) and horses (Quaranta et al., ). B. suis biovars 1 and/or 3 are widespread in pigs in America, Asia, Oceania and probably Africa, causing also human brucellosis (unlike biovar 2, both biovars are important zoonotic agents). Infections by these biovars have been reported also in domestic dogs (Ramamoorthy et al., ). Biovar 3 is considered absent from the EU, while biovar 1 is very rare, it has been reported once in horses in Croatia (Fretin et al., ) and a clinical case has been reported in cattle in the USA (Ewalt et al., ).
Parameter 3 – Experimentally susceptible wildlife species (or family/orders)
Experimental infections have succeeded in several wild species, and probably both B. abortus and B. melitensis can be transmitted experimentally to most if not all wild mammals.
The experimental susceptibility of wild species to B. suis biovars remain to be established.
Parameter 4 – Experimentally susceptible domestic species (or family orders)
B. abortus and B. melitensis naturally induced infections have been reported in practically all domestic mammal species. Thus, both infections can be probably transmitted experimentally to most if not all domestic mammals.
Apart from pigs, cattle and horses, the domestic species experimentally susceptible to B. suis biovars remain to be properly established (with the exception of infection by biovar 4 in moose (Dieterich et al., )).
However, infections in cattle by B. suis biovar 2 seem to be extremely rare, and in this case, at least considering the reported information, it seems that the infection is not followed by clinical (i.e. pathological) events (Fretin et al., ).
Reservoir animal speciesParameter 5 – Wild reservoir species (or family/orders)
B. abortus
No wild species have been proven as a natural reservoir. However, when human activity has impacted wildlife population dynamics, and where the infection is widespread in wildlife (i.e. the case of the bison and elk in the Yellowstone Park in the US – see comments in Section 3.1.2.4), some wild species could behave as a reservoir for both domestic cattle and wildlife (Cross et al., ).
B. melitensis
No wild species have been proven as a natural reservoir. In general, and particularly in Europe, wild ruminants are not regarded as reservoirs (maintenance hosts) for Brucella (Muñoz et al., ). However, exceptions may be found when human actions alter wildlife dynamics, such as in the Bargy Ibex case (Mick et al., ).
B. suis
This complex species is composed by five biovars, which reflects the different types of epidemiological occurrence in wild species. Wild boar is the natural reservoir of B. suis biovar 2. The infection is also frequent in European hares, although non-existent in other native hare species at least in the Iberian Peninsula (Muñoz et al., ), but the epidemiological role of hares remains unclear (Muñoz et al., ). The epidemiological relevance of the rare cases of B. suis biovar 2 in cattle and horses is unknown.
Feral pigs (Sus scrofa) and peccaries (Tayassuidae) are considered the natural reservoirs of B. suis biovars 1 and 3. These two last biovars are not present in the EU, with a rare exception for biovar 1 reported in horses (Fretin et al., ), and whose epidemiological significance is unknown.
Arctic foxes (Vulpes lagopus) and wolves (Canis lupus) may be infected by B. suis biovar 4 after eating infected reindeer (considered the reservoir of this biovar), but it is unknown if these carnivores are a reservoir or mere dead-end hosts. In the former Soviet Union and the Baltic countries, small rodents have been considered the natural reservoir of B. suis biovar 5, an infection of little epidemiological significance (EFSA, ; OIE, ). However, no recent reports are available.
Parameter 6 – Domestic reservoir species (or family/orders)
B. abortus: cattle (Bos taurus)
B. melitensis: sheep (Ovis aries) and goats (Capra hircus)
B. suis
- biovar 1, 2 and 3: pigs;
- biovar 4: domesticated reindeer/caribou;
- biovar 5: small rodents.
Parameter 1 – Prevalence/incidence
B. abortus / B. melitensis
B. abortus is found worldwide in cattle-raising regions except Japan, Canada, most European countries, most USA states, Australia and New Zealand, where it has been eradicated. B. melitensis is found in the Mediterranean countries, the Middle East, the Arabian Gulf, Latin America, Africa and Asia. Data on the prevalence and incidence of B. abortus or B. melitensis infections in domestic animals not submitted to official control are very difficult to get. The prevalence and incidence in domestic naïve populations which are neither vaccinated nor participating in any official sanitary intervention are usually very high, and depend largely on the time that has elapsed after the onset of disease in a given herd or flock. As example, in the early phases (before 1990) of official eradication programmes in Spain, herd prevalence ranged between 20% and 62% depending on the animal species and the regions considered. The individual prevalence (0.3–18.5%) depended on the region, animal species involved, and the technical characteristics of the programme (Blasco, , ).
In contrast, when official interventions are applied, the prevalence/incidence figures are much lower but highly variable depending on the countries, the species, and the characteristics and degree of application of the programmes implemented. Suitable information on these parameters is available in EU Member States (MS) in which control and eradication campaigns are performed.
The last data available for 2016 (
Herd prevalence and incidence in cattle, sheep and goat herds/flocks infected with Brucella in the EU Member State areas in which eradication programmes are cofinanced by the EU, hence do not include all herds and flocks in the country (in particular those of OBF areas) (year 2016)
| Country | Bovine | Small ruminants | ||||
| Herds tested | % Prevalence | % Incidence | Flocks tested | % Prevalence | % Incidence | |
| Portugal | 33,560 | 0.18 | 0.12 | 60,452 | 0.62 | 0.38 |
| Spain | 110,564 | 0.03 | 0.02 | 65,719 | 0.09 | 0.06 |
| Italy | 33,822 | 0.48 | 0.48 | 38,158 | 0.78 | 0.61 |
| Greece | Nd | Nd | Nd | 22,950 | 0.02 | 0.01 |
| Croatia | Nd | Nd | Nd | 20,176 | 0.1 | 0.1 |
7Including buffaloes (1,282 herds; prevalence 1.01%; incidence 0.62%). Nd: not indicated.
Source:
Individual prevalence/incidence is zero in the brucellosis officially free countries. The last data available (2016) on the expected individual prevalence are summarised in Table .
Expected animal prevalence of Brucella infection in cattle, sheep and goat in the EU Member State areas in which eradication programmes are co-financed by the EU (year 2016)
| Country | Bovine | Small ruminants | ||
| No. animals to be tested individually | % Prevalence | No. animals to be tested individually | % Prevalence | |
| Portugal | 899,600 | 0.02 | 1,558,000 | 0.1 |
| Spain | 3,874,200 | 0.002 | 8,490,600 | 0.01 |
| Italy | 1,004,279 | 0.37 | 2,302,009 | 0.69 |
| Greece | Nd | Nd | 4,279,000 | 0.02 |
| Croatia | Nd | Nd | 450,000 | 0.01 |
9Including buffaloes (260,375 animals; expected prevalence: 0.81%). Nd: not indicated.
Source:
In the absence of anthropogenic interventions in wildlife management that can modify the wildlife population dynamics (e.g. artificial winter feeding that can lead to increase of wildlife density and facilitates the animal contacts and the ensuing transmission), the prevalence of B. abortus/B. melitensis infections in wildlife species in the EU is considered very low or null (Muñoz et al., ; Garin-Bastuji et al., ; Mick et al., ).
B. suis
Infections caused by B. suis biovars 1 and 3 have been eradicated from domestic swine in several countries, including Canada, Australia and the USA. However, these infections still occur in wild and feral pigs, and can spread to domestic herds. In some studies, the individual prevalence in wild and feral swine ranged from 14% to 44%, and varied over time (CDC, ).
As the EU is considered as officially free from porcine brucellosis, data on the natural prevalence and incidence of B. suis biovar 2 infection in pigs are also scanty. The prevalence/incidence in intensive herds is considered insignificant (EFSA, ). However, outbreaks can be important in outdoor breeding herds due to spillover from infected wild boar. The percentage of infected pigs in naïve herds affected by a new outbreak is usually very high (15% to over 50%). The apparent prevalence of B. suis biovar 2 infection in wild boar is extremely high (25–45%) in the several EU Member States (Garin-Bastuji and Hars, , ; EFSA, ; Muñoz et al., ).
Parameter 2 – Case-morbidity rate (% clinically diseased animals out of infected ones)
B. abortus / B. melitensis
As indicated above, suitable data on the natural case morbidity rate of brucellosis in naïve domestic animal populations are not available. Accordingly, only data obtained from artificially exposed animals are available. The most frequent clinical manifestation of B. abortus/B. melitensis infections is abortion. When brucellosis-free and unvaccinated cows are artificially exposed at the critical period of pregnancy (usually mid pregnancy) to B. abortus virulent challenge doses (5 × 107 – 5 × 108 CFU), 80–100% of the animals develop severe infections resulting in abortions in 75–100% of cows exposed (Moriyón et al., ). When challenge exposure is performed with similar B. melitensis doses in pregnant sheep and goats, the clinical consequences are very similar, with infection/abortion rates close to 100% (Verger et al., ; Barrio et al., ).
B. suis
In B. suis, biovar 2 naturally infected swine naïve herds, intraherd prevalence can be as high as 75–80%, with a very high proportion of abortions (25–60%) and infertility (30–80%) (Garin-Bastuji and Hars, , ; EFSA, ; Dieste et al., ).
MortalityParameter 3 – Case-fatality rate
The case-fatality rate in naturally induced infections in domestic or wild animals is very low. Deaths are very rare in adult animals of most species; however, high B. abortus doses can be lethal in experimentally infected moose, and possibly also in bighorn sheep (Forbes et al., ). Fatality rate in humans is also very low (Pappas et al., ).
Article 7(a)(iii) The zoonotic character of the disease PresenceParameter 1 – Report of zoonotic human cases (anywhere)
Situation worldwide
Brucellosis is probably the commonest zoonotic infection worldwide, and whose global incidence has changed over the past decade because of various sanitary, socioeconomic, and political reasons, together with the evolution of international immigration and travel. Areas traditionally considered to be endemic (EU Mediterranean countries for example) have significantly improved the control of the disease, but the disease is still present. However, brucellosis is emerging strongly in the Near East and Asia (Pappas et al., ), and probably also in Africa (Ducrotoy et al., ). The incidence of human brucellosis worldwide was summarised in Dean et al. (), with European estimates of 4-32 per 100,000 per year in Greece, 0.03 in Germany, 1.40 in Italy, and global reported maximum of 52-269 in Iraq.
Situation in the EU (see also Section 3.1.1.7 below)
A total of 437 confirmed human cases were reported in 2015 (EFSA, ) with a notification rate of 0.08 cases per 100,000 inhabitants. These primarily occurred in Greece (110 cases), Italy (106), Portugal (47), Spain (n = 39), Germany (n = 44), Bulgaria (37), France (n = 19), Sweden (n = 13) and the United Kingdom (n = 12) while other MS had less than 10 cases.
Brucella species information was missing for 71.5% of the 347 confirmed cases reported. Of cases in which bacterial isolation was conducted, 85.6% were due to B. melitensis, 2.1% to B. abortus and 12.4% to other Brucella species. In contrast to B. suis biovars 1, 3 and 4, B. suis biovar 2 has rarely been isolated from humans and non-porcine animal species. It can be considered less pathogenic to humans than other biovars and its zoonotic role is questioned in non-immunocompromised hosts (Godfroid et al., ; Mailles et al., ). Similarly, in cattle as well as in small ruminants, this biovar has been only isolated in singleton serological reactors in brucellosis officially free EU member states (Belgium (Fretin et al., ), France, Poland (Szulowski et al., )), in the absence of any clinical sign or spread to other ruminants. However, precise information on the Brucella in cause is available only after its typing at biovar level; therefore at the initial confirmation of human or animal brucellosis, this will be difficult to assess and the control measures should be taken as it would be dealt with other more pathogenic species/biovars.
Article 7(a)(iv) The resistance to treatments, including antimicrobial resistanceParameter 1 – Resistant strain to any treatment even at laboratory level
In contrast to other bacterial pathogens, selection for antibiotic resistance seems unimportant in brucellosis. This may relate to the absence of plasmids and lysogenic phages in the genus Brucella (Moreno, ). Moreover, due to economical, epidemiological and public health reasons, antibiotic treatment of brucellosis has been precluded in domestic animals, thus limiting the development of antibiotic resistance. Accordingly, resistance is not considered a significant issue in treating human brucellosis (Maves et al., ).
Article 7(a)(v) The persistence of the disease in an animal population or the environment Animal populationParameter 1 – Duration of infectious period in animals
Brucellae remain confined to the lymph nodes close to entry sites for 2–3 weeks, and then reach the blood via the efferent lymphatics; bacteraemia then leads to a generalised infection in reticuloendothelial organs, lymph nodes distant from entry sites, genital and extragenital organs and accessory sexual glands.
The precise duration of B. abortus, B. melitensis and B. suis infections has not been properly established in the different domestic species, but it is widely accepted that only a low proportion (10–15%) of infected animals develop a self-cure mechanism, while most remain infected for life, excreting the bacteria intermittently to the environment (Nicoletti, ; EFSA, ).
Parameter 2 – Presence and duration of latent infection period
The duration of the latent status until the animals develop the disease is highly variable, usually showing an abortion during their first or second pregnancy (Plommet et al., ; Lapraik and Moffat, ).
Brucella-induced latent infections are transmitted from infected dams to offspring either during pregnancy or perinatally (usually through milk). Latently infected animals are apparently healthy and show negative responses in the indirect immunological diagnostic tests, being thus very dangerous epidemiologically. Latent infections have been reported in up to up to 10% of the offspring born to B. abortus infected cattle (Plommet et al., ; Lapraik and Moffat, ), and also in B. melitensis infected goats (Renoux, ) and sheep (Grilló et al., ). Latent infections have not been reported in B. suis infected pigs, but they are believed to also occur these with variable frequency (EFSA, ).
Despite its low frequency, latent infection is one of the most frequent and dangerous causes of brucellosis transmission. If the objective is eradicating the infection, keeping replacements from Brucella positive animals should be avoided.
Parameter 4 – Length of survival (dpi) of the agent and/or detection of DNA in selected matrices (soil, water, air) from the environment (scenarios: high and low T)
Some Brucella species can survive for long periods outside the host. Dryness, high temperatures and direct sunlight exposure are very unfavourable for Brucella survival. Under favourable conditions, such as pH > 4, low temperatures, high humidity and the absence of direct sunlight, Brucella spp. may survive for relatively long periods in aborted fetuses and fetal membranes, faeces and liquid manure, water, wool and hay, as well as on equipment and clothes. Brucella spp. are able to withstand drying particularly in the presence of organic material and can then remain viable in dust and soil for relatively long periods. Survival is prolonged at low temperatures, especially in snow and ice. Since the presence of DNA in selected matrixes or the environment is not representative of the true survival ability of Brucella, no comments will be made on this topic. As an example, the persistence of B. suis on fomites varies from 4 h to 56 days (Ryan, ; US-EPA, ,b; Calfee and Wendling, ).
Brucella species can persist for several weeks in soil (Franz et al., ; Charters, ) and in dust (Franz et al., ). B. abortus was reported to persist 66 days in wet soil, 48–73 days in soil at 90% humidity and < 4 days in dried soil (Nicoletti, ). B. abortus can persist in fetal tissues, soil or vegetation for several weeks or even months depending upon the season, temperature and sunlight (Aune et al., ). In bovine and bison fetuses deployed in February, March, April and May, B. abortus persistence was 81, 77, 69 and 25 days, respectively (Aune et al., ). B. abortus persisted 10–43 days at B. abortus contaminated sites associated with bison births or abortions for 7–26 days (Aune et al., ).
B. suis can persist at least 28 days in soil held at 5°C or 22°C (US-EPA, ,b). However, in some study, this pathogen has been reported, surprisingly, to survive for 4 years in soil (Mollaret and Bourdin, ).
Depending on temperature and pH, B. abortus can persist in water from less than 1 to 77 days in water (Nicoletti, ; Falenski et al., ). B. melitensis and B. suis can persist for 1–7 days in dechlorinated water (Gilbert and Rose, ).
The survival of Brucella in milk and dairy products is highly variable from only few seconds to more than 4 months, depending on the Brucella species, the pH and temperature of preservation (for a review, see Garin-Bastuji and Blasco, ). Disinfectants reported to kill Brucella on contaminated surfaces include 2.5% sodium hypochlorite, quaternary ammonium compounds, 2–3% caustic soda, 20% freshly slaked lime suspension or 2% formaldehyde solution (all tested for 1 h). Ethanol, isopropanol, iodophores, substituted phenols or diluted hypochlorite solutions can be used on contaminated skin; alkyl quaternary ammonium compounds are not recommended for this purpose. Autoclaving (moist heat of 121°C for at least 15 min) can be used to kill Brucella species on contaminated equipment. These organisms can also be inactivated by dry heat (160–170°C) for at least 1 h. Boiling for 10 min is usually effective for liquids. Xylene (1 mL/L) and calcium cyanamide (20 kg/m3) are reported to decontaminate liquid manure after 2–4 weeks. Brucella species can also be inactivated by gamma irradiation and pasteurisation (Ryan, ; Garin-Bastuji and Blasco, ).
Article 7(a)(vi) The routes and speed of transmission of the disease between animals, and, when relevant, between animals and humans Routes of transmissionParameter 1 – Types of routes of transmission from animal to animal (horizontal, vertical)
The main routes of transmission between animals and between animals and humans are summarised in Figure .
Fetuses can be infected vertically, allowing the development of latent carriers. The heavily contaminated placenta and aborted fetuses become the main source of infection for humans (direct contact) and other animal hosts. Humans may also acquire infection eating unpasteurised dairy products, primarily or, exceptionally, raw or undercooked contaminated animal organs (like liver, blood and spleen) and meat.
Parameter 2 – Types of routes of transmission between animals and humans (direct, indirect, including food-borne)
See Figure above.
Speed of transmissionParameter 3 – Incidence between animals and, when relevant, between animals and humans
Data on the incidence of animal brucellosis have been commented above (see Section 3.1.1.2). In the absence of vaccination, the risk of transmission of brucellosis between animals in infected environments is very high. The incidence in humans has been reported to be highly correlated (r = 0.82) to the incidence of brucellosis in animals (Lee et al., ). Accordingly, when the disease is controlled in the animal hosts, a significant decrease is seen in human brucellosis incidence achieved.
Parameter 4 – Transmission rate (beta) (from R 0 and infectious period) between animals and, when relevant, between animals and humans
Several statistical methods have been applied to the quantitative study of brucellosis transmission in animals and humans. These methods have provided the basis for identifying key epidemiological parameters as the basic reproductive ratio (R0) or the effective reproductive ratio (Re), that indicates the number of secondary infections for each infectious individual during ongoing transmission (for a review see Heffernan et al. ()). Several R0 values have been reported or hypothesised for brucellosis (Table ) but these figures are not straightforward because transmission dynamics is complicated by multiple interactions (Beauvais et al., ; Hou and Sun, ).
Examples of reproductive ratio (R0) figures calculated or hypothesised for animal brucellosis in different scenarios
| R0 values | Species | Country | Reference |
| 1.75 | Bison | USA | Hobbs et al. () |
| 1.2 | Sheep | Mongolia | Zinsstag et al. () |
| 1.7 | Cattle | Mongolia | Zinsstag et al. () |
| 2 | Sheep | Hypothesised | Moreno () |
| < 1 – > 3 | Sheep/cattle | Mongolia | Racloz et al. () |
Parameter 1 – Map where the disease is present in EU
Presence in animals
Bovine brucellosis
The list of countries and regions Officially Brucellosis-Free (OBF) is laid down in Annex II of the current version of Commission Implementing Decision (EU) 2016/168.
‘not OBF yet’
For 2015, 938 positive or infected cattle herds were reported in total in the non-OBF regions of the non-OBF MS (967 in 2014), i.e. a herd prevalence of 0.28%.
Sheep and goat brucellosis
The list of countries and regions Officially Brucella melitensis-free (ObmF) is laid down in Annexes I and II to Commission Decision 2010/695/EU.
Maps are provided in the European Union summary report on zoonoses (EFSA, ).
During the period 2005–2013, the overall proportion of sheep and goat flocks positive to B. melitensis in the EU showed a decreasing trend. In 2014, the decline continued from 0.11% in 2013 to 0.09% in 2014, the lowest prevalence ever reported. In the non-ObmF regions of the non-OBmF MSs, the overall prevalence of B. melitensis-positive sheep and goat flocks decreased from 0.45% in 2012 to 0.29% in 2015.
Porcine brucellosis
The EU is considered as officially free from this infection in domestic swine, although B. suis biovar 2 cases have been reported sporadically in several MSs in outdoor pig farms, in particular: Belgium, Croatia, Finland, France, Germany, Italy and Poland. Moreover, a relevant number of samples from wild boar (1,393 in Germany, 252 in Italy and 156 in Spain in 2014) and hares (16 in Germany in 2014) were reported to be infected by B. suis biovar 2. Maps are provided in the European Union summary report on zoonoses (EFSA, ).
Presence in humans
A total of 449 human brucellosis cases (of which 437 were confirmed, and most due to B. melitensis and B. abortus), were reported in the EU in 2015 (EFSA, ).
Parameter 2 – Type of epidemiological occurrence (sporadic, epidemic, endemic) at MS level
See above in Sections 3.1.1.1 and 3.1.1.7 Parameter 1.
Risk of introductionNot applicable. The animal disease is already present in several European countries. Control measures keep other countries Member States officially free.
Article 7(a)(viii) The existence of diagnostic and disease control tools Diagnostic toolsParameter 1 – Existence of diagnostic tools
Brucellosis caused by B. abortus (cattle and buffaloes), B. melitensis (small ruminants) and B. suis (swine) lacks pathognomonic symptoms and its diagnosis is based on the existing direct and indirect tests (OIE, ) (see Sections 3.1.4.1 and Tables , and in Appendix A), the latter being those applied routinely in surveillance and control and eradication programmes. Detailed information of the availability, feasibility and effectiveness of the diagnostic tests is given below in Section 3.1.4.1.
Control toolsParameter 2 – Existence of control tools
There are two possible strategies which exist to fight against brucellosis in ruminants: (1) a control programme based on mass (whole-flock/herd) vaccination or (2) an eradication programme based on test and cull, combined with vaccination. In both cases, the use of adequate vaccination procedures and diagnostic tests is of paramount importance. A detailed description is made in Section 3.1.4.2.
Blasco and Molina-Flores () provide considerable detail on control and eradication of Brucellosis stating that Brucellosis can be first controlled (essentially by vaccination), and once the prevalence has decreased to reasonable levels the disease can be eradicated from a herd/flock by test and culling procedures (combined or not with vaccination), or by full depopulation. The authors provide a simple decision tree which should be taken into consideration by decision makers to select the most appropriate strategy according the different epidemiological situations. Independent of the prevalence of infection, the quality and degree of organisation of the national veterinary services is the limiting factor.
Article 7(b) The impact of diseases Article 7(b)(i) The impact of the disease on agricultural and aquaculture production and other parts of the economy The level of presence of the disease in the UnionParameter 1 – Number of MSs where the disease is presence
See above in Section 3.1.1.7.
The loss of production due to the disease
Parameter 2 – Proportion of production losses (%) by epidemic/endemic situation (milk, growth, semen, meat, etc.)
There are very few well-documented studies on the production losses and the economic impact of brucellosis that take into account all aspects of the disease impacting the animal industry. Production losses can be divided broadly in direct (due to the pathological condition itself) and indirect (due to associated causes).
A summarised description of brucellosis losses is made in Figure .
Little is known about how brucellosis affects animal production quantitatively. A standardised methodology has been applied to the estimation of the direct disease costs and the human health and animal welfare impacts associated with 34 endemic diseases of livestock in Great Britain, but unfortunately, this study did not include brucellosis (Bennett and Ijpelaar, ).
The main clinical feature of brucellosis is late abortion in cattle, pigs, sheep and goats. Among the seropositive cattle, it has been estimated empirically that 10–50% abort and 20% of these remain infertile (Bernués et al., ). Having aborted, animals are often not milked and the entire lactation is lost. Besides abortions, perinatal mortality was also estimated empirically between 5% and 20%, and moreover, it was hypothesised that 1% of cows with abortions may die (Bernués et al., ). These authors estimated also theoretically a loss of 10–25% of total milk yield among the seropositive cows. These theoretical values were established many years ago in cattle in a particular epidemiological situation in the north of Spain. Despite this, these figures have been classically considered as the reference standard for losses caused for brucellosis no matter the animal species and the epidemiological conditions considered. In a study on bovine brucellosis (Santos et al., ), and based in part on these theoretical considerations, the following losses were estimated:
- 15% incidence of abortions in infected heifers and cows;
- an average of 2 months of temporary infertility for each infected cow and heifer, considering that 20% of cows that abort become sterile;
- an incidence rate of perinatal mortality of 10% for calves born from infected cows or heifers;
- 15% loss of the total milk yield of infected cows;
- 5% loss in meat production by infected cows;
- 1% mortality risk for infected cows that aborted (i.e. 0.15% of infected cows and heifers);
- an increase in the rate of replacement corresponding to 15% of the infected cows and heifers;
- replacement costs of infected bulls, considering roughly half of the seroprevalence of heifers, an average bull/cow ratio of 1/25, and same approach for calculating replacement as for females.
In summary, the direct production losses due to brucellosis have been estimated empirically, and only in cattle. Accordingly, the available losses reported are probably inaccurate, and precise information is lacking in the case of small ruminants and pigs.
Regarding porcine brucellosis, although it has been eradicated from the domestic pig population in Europe for decades, B. suis biovar 2 infection in wild boar (which is a sustainable infection in almost all European wild boar populations) is of major concern for pigs reared outdoors, should brucellosis control programmes in domestic pigs be implemented in the EU Member States (Godfroid et al., ).
Article 7(b)(ii) The impact of the disease on human health Transmissibility between animals and humansParameter 1 – Types of routes of transmission between animals and humans
Brucella is easily transmitted from animals to humans. Humans become infected either through direct contact with infected animals or consumption of unpasteurised contaminated dairy products and selected raw or undercooked contaminated animal organs (like liver, blood and spleen). As the infectious dose is very low for humans, infection is usually an occupational risk for farmers, veterinarians, abattoir workers, laboratory personnel and others who work with animals and a risk for those who consume unpasteurised products. The increase in business and leisure travel to brucellosis-endemic countries has led to the importation of the human disease into non-endemic areas.
Parameter 2 – Incidence of zoonotic cases
The prevalence of brucellosis in humans depends upon several factors such as dietary habits, methods of processing milk and milk products, husbandry practices and environmental hygiene. Brucellosis causes more than 500,000 human infections per year worldwide. The disease has a limited geographic distribution, but it remains a major public health problem in the Mediterranean region, Western Asia, parts of Africa and Latin America (Pappas et al., ). The situation in the EU has been described in detail in Section 3.1.1.3.
Transmissibility between humansParameter 3 – Human to human transmission is sufficient to sustain sporadic cases or community-level outbreak
See comments in the next Parameter.
Parameter 4 – Sporadic, endemic, epidemic or pandemic potential
Human to human transmission of brucellosis is exceptional, and these exceptional cases have been reported. As an example, two physicians who assisted the surgical delivery of a placenta in an infected woman developed Brucella melitensis infection (Mesner et al., ). Sexually transmitted cases have been suspected but never really proven (Meltzer et al., ). Humans are considered thus a dead-end host of the disease.
The severity of human forms of the diseaseA specific meta-analysis has been conducted on this topic (Dean et al., ). Brucellosis is a multisystemic disease with a broad spectrum of symptoms. Asymptomatic infections are common. In symptomatic cases, the disease is extremely variable and the clinical signs may appear insidiously or abruptly. Typically, brucellosis begins as an acute febrile illness with nonspecific flu-like signs. Splenomegaly, hepatomegaly, coughing and pleuritic chest pain are sometimes seen. Gastrointestinal signs including anorexia, nausea, vomiting, diarrhoea and constipation occur frequently in adults but less often in children.
The disease is considered non-fatal (mortality rate of around 1% or less). However, when the diagnosis or treatments are not made properly, severe complications are common. Brucellosis causes one case of endocarditis and four neurological cases per 100 patients. One in 10 infected males suffers from epididymo-orchitis. Arthralgia, myalgia and back pain affect around half of the patients (65%, 47% and 45%, respectively).
Parameter 5 – Disability-adjusted life year (DALY)
DALY for a given disease are calculated by summing the years of life lost due to premature mortality (YLL) in the population and the equivalent healthy years lost due to disability for incident cases of the health condition (YLD). DALY estimates for brucellosis are based on the fact that is a non-fatal disease. So, the YLL part of calculations goes to zero. A brucellosis disability weighting of 0.2 has been proposed for DALY calculation, based on the pain and impaired productivity known to result from infection, and a median duration of untreated brucellosis of 3.1 years (Roth et al., ). Under this assumption, the cost-effectiveness and economic benefit for human society and the agricultural sector of a mass vaccination programme against ruminant brucellosis was modelled (Roth et al., ). The intervention consisted of a 10-year mass vaccination of Mongolian livestock using Rev.1 vaccine in small ruminants and S19 vaccine in cattle. Cost-effectiveness, expressed as cost per DALY averted, was the primary outcome. In a scenario of 52% reduction of brucellosis transmission between animals achieved by mass vaccination, it was estimated that a total of 49,027 DALY could be averted.
A DALY estimation was made in Kenya (
Another DALY estimate in Sudan using a 0.2 disability weight, concluded that the healthy years lost by an infected person accounted 7.5 DALY (Elkhansaa and Angara, ).
The availability of effective prevention or medical treatment in humansParameter 6 – Availability of medical treatment and their effectiveness (therapeutic effect and any resistance)
There are suitable treatments for human brucellosis. The prophylaxis of human brucellosis has to be based on three essential measures:
- awareness campaigns to educate the population on the major transmission risks (essentially, direct contact with animals and eating raw milk products);
- suitable food safety legislation and implementing measures avoiding the arrival to the markets of contaminated dairy products;
- the reduction/elimination of the infection in the animal hosts through suitable control and eradication campaigns. This last measure is, without any doubt, the most relevant for the definitive eradication of human brucellosis.
In addition, the antibiotic treatment is prolonged. A review of the efficacy of the FAO/WHO recommendations is reported by Ariza et al. ().
Parameter 7 – Availability of vaccines and their effectiveness (reduced morbidity)
No vaccines are available for human brucellosis.
Article 7(b)(iii) The impact of the disease on animal welfareParameter 1 – Severity of clinical signs at case level and related level and duration of impairment
Brucellosis is considered as a major contributor to animal suffering, causing fever, abortions, stillbirths and the birth of weak offspring, with the ensuing increase of perinatal mortality. Animals that abort may retain the placenta and develop endometritis and infertility. Animals usually abort only once, but subsequent chronic infertility is quite frequent. Milk yield is significantly reduced in infected animals but clinical signs of mastitis are uncommon. Acute orchitis and epididymitis can occur in males, and may result also in infertility. Arthritis and hygromas are seen occasionally. Deaths are very rare except in the fetus or new-born.
Studies on the impact of brucellosis on animal welfare beyond the clinical symptoms described above are lacking.
Article 7(b)(iv) The impact of the disease on biodiversity and the environment BiodiversityParameter 1 – Endangered wild species affected: listed species as in CITES and/or IUCN list
In the EU, brucellosis due to B. abortus or B. melitensis have been reported only sporadically in wild ungulates such as ibex (Capra ibex), chamois (Rupicapra sp.) and red deer (Cervus elaphus) (Gortázar et al., ; Mick et al., ). However, these wild animals are considered occasional end hosts of brucellosis transmitted from infected livestock, rather than a true reservoir of the disease (Gortázar et al., ). Moreover, both infections are usually non-lethal in these wild species, which appear as of ‘Least concern’ in the IUCN list.
Brucellosis due to B. suis biovar 2 is reported frequently in the EU affecting the Eurasian wild boar (Sus scrofa) and the European brown hare (Lepus europaeus), which are considered the natural reservoirs of porcine brucellosis in Continental Europe. This infection is non-lethal in these wild species. Moreover, none of these two wild species appear as endangered or vulnerable in the IUCN list.
Parameter 2 – Mortality in wild species
Brucellosis is a non-fatal disease, being this issue of minor concern.
EnvironmentParameter 3 – Capacity of the pathogen to persist in the environment and cause mortality in wildlife
B. suis biovar 2 infection is well established and persists naturally in the Eurasian wild boar (Sus scrofa) and the European brown hare (Lepus europaeus), these wild species being the natural reservoir of this infection in Continental Europe, and the main reservoir for domestic pigs. This infection is non-lethal in any of these wild species.
It has been questioned if B. abortus and B. melitensis can persist naturally in wildlife, being thus a reservoir for both human and domestic animals (Rhyan et al., ).
Article 7(c) Its potential to generate a crisis situation and its potential use in bioterrorismBrucella species can be easily cultured from infected animals. Also, these bacteria can be transferred, multiplied and stored easily. An intentional contamination of food or water with pathogenic Brucella species could pose a threat with a low mortality rate but with a very high attack rate. Some Brucella (particularly B. melitensis and B. suis biovars 1 and 3) are highly infectious through oral/aerosol routes and, moreover, low doses are infective for humans and also for animals. Altogether, these characteristics make of this pathogen an attractive candidate to be used as a potential agent for biological warfare purposes (Doganay and Doganay, ).
Parameter 1 – Listed in OIE/CFSPH classification of pathogens
The Brucella genus is listed in the OIE list of notifiable terrestrial and aquatic animal diseases and in the CFSPH bioterrorism pathogens. See
Parameter 2 – Listed in the Encyclopaedia of Bioterrorism Defence of Australia Group
Pathogenic Brucellae are listed in the Encyclopaedia of Bioterrorism Defence of Australia Group. See:
Parameter 3 – Included in any other list of potential bioagroterrorism agents
Pathogenic Brucella are specified in the select agent rules implemented by USDA APHIS and the Centers for Disease Control and Prevention (CDC) of the Department of Health and Human Services (HHS) of the US and overlap with diseases and agents/toxins listed by APHIS, CDC and Code of Federal Regulations of the US (CFR) 121.4. See:
Parameter 1 – Officially/internationally recognised diagnostic tool, OIE certified
As indicated above (see Section 3.1.1.8), several diagnostic tests are available, recognised by the OIE, and used for surveillance/eradication in most countries worldwide (EFSA, ). These OIE tests and their main applications are summarised in Tables , and (Appendix A).
Direct bacteriological isolation is the most specific test for the confirmation of Brucella. Both molecular and microbiological tests can be used for identification and typing. The vaccine strains (B. abortus strains S19 and RB51 and B. melitensis Rev.1) can be distinguished from their corresponding virulent field counterparts by both molecular (polymerase chain reaction (PCR) and related molecular tests) and classic microbiological criteria. Despite their usefulness for identification and typing, molecular tests are not fully suitable for the direct diagnosis from field samples. Serology is the most adequate for diagnosis at population level and is used for a presumptive diagnosis or for surveillance to screen herds/flocks. Serological tests used in sheep, goats, cattle and pigs include the buffered Brucella antigen tests (Rose Bengal and buffered plate agglutination tests), complement fixation, indirect or competitive enzyme-linked immunosorbent assays (ELISAs) and the fluorescence polarisation assay (FPA) (EFSA, 2006; EFSA, ; OIE, ). Other serological tests include gel precipitation tests with Native Hapten (NH) or cytosolic proteins (suitable for ruminants), the serum agglutination test (a test used in all animal species with controversial results), and the brucellin skin test (for use in all animal species). ELISAs or the Brucella milk ring test (MRT – this only for use in cattle) can be used also to screen dairy herds/flocks by detecting antibodies in milk (OIE, ).
In vaccinated cattle, the NH-based gel precipitation tests are sometimes used to diagnose infected animals in vaccination contexts (OIE, ).
The brucellin allergic skin test can be used to test unvaccinated animals for discriminating the true brucellosis infected animals from those giving false positive serological reactions (FPSR) in serological tests (generally due to cross-reactions with other gram-negative bacteria) (OIE, ).
EffectivenessParameter 2 – Se and Sp of diagnostic test
Direct tests (see Table ) are very specific (particularly the classical bacteriology) for the diagnosis of brucellosis. However, since only the indirect tests are used for surveillance/eradication programmes, comments on diagnostic accuracy (diagnostic sensitivity (DSe) and diagnostic specificity (DSp)) will be focused exclusively in the immunological tests.
Because of different background flora, sera from Brucella-free animals can produce significantly different background reactivity depending upon their origin. Therefore, cut-offs obtained with animals from Brucella-free countries and infected animals from endemic areas as negative and positive controls, respectively (Nielsen et al., , ), must be interpreted bearing in mind this problem.
Tests for diagnosing brucellosis in small ruminants and cattle (B. melitensis and B. abortus infections)
The EFSA meta-analytic report (EFSA, 2006) as well as literature data (using essentially the same inclusion/exclusion criteria that those used in EFSA (2006)) were used to produce the diagnostic accuracies summarised in Tables (Appendix A – sheep), (Appendix A – cattle) and (Appendix A – goats). Sensitive enough and reasonably specific tests are available, with the possibility to combine more than one of these tests for a suitable diagnosis and culling policy (EFSA, 2006).
OIE test methods available for the diagnosis of B. abortus, B. melitensis and B. suis infections (Source: adapted from OIE (). Infection with Brucella abortus, B. melitensis and B. suis)
| Method | OIE test prescription | Purpose | |||||
| Population freedom from infection | Individual animal freedom from infection | Efficiency of eradication policies | Confirmation of clinical cases | Confirmation of suspect cases | Herd/flock prevalence of infection – surveillance | ||
| Direct | Agent identification | ||||||
| Staining methods | – | – | – | – | + | – | – |
| Culture | – | – | – | – | +++ | +++/++ | – |
| PCR | – | – | – | – | + | +/+ | – |
| Indirect | Detection of immune response , | ||||||
| BBAT (RBT, BPAT, Card test) | Prescribed for trade | +++ | ++ | +++ | + | + | +++ |
| FPA | Prescribed for trade | ++ | ++ | + | ++ | + | ++ |
| CFT | Prescribed for trade | ++ | ++ | +++/+ | ++ | + | ++ |
| I-ELISA | Prescribed for trade | +++ | ++ | +++ | ++ | + | +++ |
| C-ELISA | Prescribed for trade | + | – | – | + | + | + |
| BST | Other tests | +++ | – | + | +++ | +++ | ++ |
| SAT | Other tests | + | + | + | – | – | + |
| NH and cytosol protein-based tests | Other tests | – | – | +/++ | ++ | ++ | – |
|
Bulk milk tests Milk I-ELISA or Milk ring-test |
Other tests | +++ | – | +++ | – | – | +++ |
+++ = recommended method; ++ = suitable method; + = may be used in some situations, but cost, reliability, or other factors severely limits its application; – = not appropriate for this purpose. CFT: complement fixation test; I-/C-ELISA: indirect/competitive enzyme-linked immunosorbent assay; FPA: fluorescence polarisation assay; BST: Brucellin skin-test; SAT: standard tube agglutination test; NH: native hapten.
12This applies only to herds/flocks, countries or zones free from infection with Brucella.
13In order to improve the efficiency of eradication policies in infected herds/flocks, it is recommended to associate tests in parallel to increase the sensitivity of the diagnosis, i.e. two serological tests at least, e.g. BBAT or FPA and CFT or I-ELISA. The sensitivity is further increased by a parallel testing in both serology and BST.
14In low-prevalence or almost-free zones, the predictive value of positive results to serological tests may be very low. In such situation, the agent identification is usually needed for confirming clinical cases.
15In infected herds/flocks, a positive result to any serological test may be considered as a confirmation of a clinical case: (1) In infected herds/flocks, any reactor in any serological test should be considered as infected, (2) In low-prevalence or almost-free zones, singleton serological reactors may be confirmed by culture or BST (BST individual sensitivity is not 100%; BST is, however, highly effective when interpreted at herd/flock level), (3) In free countries or zones, suspect animals are those positive to both a screening and a confirmatory serological test (tests in series) and may be confirmed by culture (and or PCR) and/or BST.
16False-positive and false negative results may occur.
17The sensitivity and specificity of serological tests are far lower in pigs than in ruminants. Therefore, it is almost impossible to implement a large-scale serosurveillance in a pig population (due to the lack of specificity). In addition, in non-endemic areas, clinical or serological suspicions must almost always be confirmed by culture (and or PCR) and/or BST.
18In zones where subcutaneous S19 or Rev.1 vaccination is practiced, NH test may help in differentiating antibodies due to vaccination from those due to infection. In free countries or zones affected by the FPSR, both NH and cytosol-based tests are suitable for differentiating FPSR from true infections.
19Dairy cattle only.
20NH tests particularly useful for testing and slaughtering purposes when adult vaccination with S19 (cattle) or Rev 1 (small ruminants) is performed. Cytosol-protein based tests particularly useful when false positive serological reactions occur.
21Of limited efficacy when testing pigs.
22The best selective culture media are the Farrell's and CITA's media (see De Miguel et al., ); PCR: polymerase chain reaction; BBAT: buffered Brucella antigen tests (i.e. Rose Bengal test (RBT) and buffered plate agglutination test (BPAT)).
Tests for brucellosis in pigs (B. suis infection)
Comments on diagnostic performance of the OIE tests in pigs are based on the meta-analytical EFSA estimates (EFSA, ), as well as on more recent work (Muñoz et al., ; Dieste-Pérez et al., ). Highly sensitive and reasonably specific tests with the potential to combine more than one are available (EFSA, ). However, serological testing in pigs is mainly useful to monitor herd status but is not reliable enough for identifying individual animals infected. Evidence from the systematic review suggests that indirect and competitive ELISAs could be suitable candidates because of their high DSe and DSp (EFSA, ). However, these ELISA tests have not been fully evaluated and standardised in pigs, and highly variable results are obtained when applied in the same population.
A major concern in porcine brucellosis officially free countries is the presence of false positive serological reactions (FPSR) in S-LPS-based tests. Little is known about the causes of FPSR in pigs, but infections by Yersinia enterocolitica O:9 are considered the main responsible (EFSA, ). Neither S-LPS- nor R-LPS-based tests are fully specific for differentiating porcine brucellosis from FPSR (Appendix A). In addition to bacteriology and molecular tools, the brucellin skin test (BST) is considered the only confirmatory test discriminating between brucellosis and the infections caused by Y. enterocolitica O:9 or other cross-reacting bacteria (EFSA, ; Dieste-Pérez et al., ). However, some serological tests based on cytosolic proteins can be a suitable and more practical alternative to the BST (Dieste-Pérez et al., ).
FeasibilityParameter 3 – Type of sample matrix to be tested (blood, tissue, etc.)
A large variety of sample matrices can be cultured. Milk samples and vaginal swabs from aborted animals are particularly useful for diagnosis in live animals. Brucella can also be cultured from aborted fetuses (stomach contents, spleen and lung) or the placenta. The spleen, the whole lymph nodes, udder and late pregnant or early post-parturient uterus, testis/epididymides, and accessory male sex glands are the most reliable samples to collect at necropsy (De Miguel et al., ). These samples are also suitable for direct PCR diagnostic procedures.
Article 7(d)(ii) Vaccination AvailabilityParameter 1 – Types of vaccines available on the market (live, inactivated, DIVA, etc.)
Three live attenuated vaccines are currently available: B. abortus S19 and B. abortus RB51 (for brucellosis cattle) and B. melitensis Rev.1 (for brucellosis in sheep and goats).
There are no vaccines against brucellosis induced by B. abortus/B. melitensis in camels, water buffaloes and yaks, which are important domestic species cohabiting with small ruminants and cattle in several breeding systems outside the EU.
The B. abortus S19 but not RB51 has been also proven effective against B. melitensis infection in cattle (Jiménez de Bagüés et al., ; Peniche Cardeña et al., ) and partially protective in red deer (Arenas-Gamboa et al., ). B. abortus S19 vaccine is used empirically in water buffalo and yak for the prophylaxis of brucellosis in some countries (e.g. Mongolia). However, no protection experiments have been conducted in camel, water buffalo, yak, swine and other domestic livestock. Developments in this area are required urgently. A major drawback of the S19 vaccine is that it is difficult to distinguish between cattle naturally infected from those vaccinated as adults, which is possible with the RB51 vaccine (Yang et al., ). Another disadvantage of the S19 and RB51 vaccines is that they can cause abortion if given to pregnant cows (Smith and Ficht, ; Yang et al., ) and their virulence for humans (Spink et al., ; Ashford et al., ). Another disadvantage of RB51 is that it is resistant to rifampicin, which is often used for treating brucellosis (Gulsun et al., ).
Large-scale Rev.1 vaccination programmes proved its capacity to reduce the Brucella seroprevalence (Ward et al., ; SCOFCAH, ). On the other hand, Brucella has been occasionally detected in milk of Rev.1-vaccinated goats (Banai, ), the vaccine strain is virulent to humans (Blasco and Diaz, ) and differentiating naturally infected with B. melitensis and B. ovis from Rev.1-vaccinated animals might be difficult in vaccine is applied subcutaneously or in adults (Fensterbank et al., ).
The general characteristics of the currently available vaccines for the prophylaxis of animal brucellosis are summarised in Table .
General characteristics of currently available brucellosis vaccines (Adapted from Blasco et al. ())
| Vaccine | Advantages | Disadvantages | Comments |
| B. melitensis Rev.1 |
Proved efficacy in control/eradication programmes (France, Italy, Portugal, Spain) Effective against both B. melitensis and B. ovis Safe in young replacements (males and females) Single dose affords useful protection for life Biological quality control feasible (OIE protocol) |
Highly abortifacient when used in pregnant animals Serological interference in classical serological tests (RBT, CFT), indirect and competitive ELISAs, fluorescence polarisation assay, and other S-LPS tests Low virulence for humans; streptomycin resistant |
Safety issues minimised by avoiding use in mid-pregnancy animals by the conjunctival route Serological interference is minimised when applied to young replacements by the conjunctival route Human infections can be diagnosed using standard serological tests; treatment requires regimes that do not include streptomycin |
| B. abortus S19 |
Proved efficacy in control/eradication programmes (EU countries, USA and Australia) Protects cattle against both B. abortus and B. melitensis Single dose affords useful protection for life Biological quality control feasible (OIE protocol) |
Depending on the dose and vaccination route can be abortifacient when used in pregnant cattle Used subcutaneously is not safe in bulls (unknown when applied by the conjunctival route) Serological interference in classical serological tests (RBT, CFT), indirect and competitive ELISAs, fluorescence polarisation assay, and other S-LPS tests Low virulence for humans |
Serological interference is minimised when reduced doses are applied to young animals (particularly by the conjunctival route) Abortive effect minimised when reduced doses are applied by the conjunctival route Human infections can be diagnosed using standard serological tests; standard antibiotic treatment effective |
| B. abortus RB51 |
|
|
|
B. suis
With the exception of a live attenuated Chinese vaccine (Xin, ), whose efficacy for brucellosis has been disproven in controlled experiments in ruminants (Bosseray and Plommet, ; Blasco et al., ; Verger et al., ), no vaccines are available against brucellosis in pigs.
Parameter 2 – Availability/production capacity (per year)
The three vaccines currently available are widely produced worldwide with important regional differences.
In the EU, the production capacity of the S19 vaccine is limited (only three manufacturing companies exist in Spain), as it is also the case of RB51 (only one company exists in Spain). In the case of B. melitensis Rev.1 vaccine, the situation is similar with a single manufacturing company in France (Hungary) and three more companies in Spain. Italy produces also a reduced amount of Rev.1 manufactured by a single official laboratory but not by private companies. As a consequence of the effective control/eradication of brucellosis in the EU MS, these manufacturing companies have reduced significantly the overall production capacity, which is essentially maintained for the export market. However, manufacturing technology is currently well implemented and the production capacity of these remaining companies could be significantly increased to cover an emergency situation, at least at medium term.
EffectivenessParameter 3 – Field protection as reduced morbidity (as reduced susceptibility to infection and/or to disease)
B. abortus S19 and B. melitensis Rev.1 remain the most effective vaccines, and when combined with test and slaughter have been instrumental in almost all successful cases of eradication. A single dose of these vaccines confers from 50% to 100% protection against challenges infecting 80–100% of unvaccinated controls (Nicoletti, ; Jacques et al., ; Barrio et al., ; Dorneles et al., ). However, quality of product is essential and thus there are internationally accepted quality control protocols for both vaccines (Grilló et al., ; OIE, ).
Although RB51 vaccine also protects cattle against mild B. abortus challenges (Moriyón et al., ; Dorneles et al., ), the protective life span of this vaccine is unknown, and field infections in vaccinated animals have been observed even in revaccinated cattle (Moriyón et al., ; Herrera-López et al., ). Under controlled conditions, the few valid comparisons strongly suggest that RB51 is inferior to S19 (Moriyón et al., ).
Whether RB51 protection is useful under field conditions has been a matter of debate.
Parameter 4 – Duration of protection
It has been proven experimentally that Rev.1 induces suitable protection against B. melitensis in sheep for at least two consecutive pregnancies (Verger et al., ). The protection lapse span of Rev.1 against B. melitensis in goats is very long at 4–5 years (Alton, ; Díaz-Aparicio et al., ).
The duration of immunity induced by S19 in cattle vaccinated as calves has been proven to be also quite long, covering almost the entire productive lifespan of the animals, and it has been reported that the immunity in cattle vaccinated between 6 and 8 months of age does not decrease from the first through the fifth pregnancy (Dorneles et al., ). Revaccination with S19 demonstrated no apparent benefit in cattle and as in the case of the Rev.1 vaccine, a single vaccination is considered effective enough for the whole productive lifespan of the animals (Dorneles et al., ).
The protective lapse span of RB51 vaccine is unknown.
Article 7(d)(iii) Medical treatments AvailabilityFor economic, epidemiological and public health reasons, treatment with antibiotics has been generally precluded in animals infected with brucellosis. However, several therapeutic regimens have been evaluated successfully for brucellosis in cattle, sheep, pigs and dogs (Nicoletti et al., ; Marín et al., ; Jiménez de Bagüés et al., ; Grilló et al., ; Dieste et al., ; Dieste-Pérez et al., ).
The therapeutic effect has been reported as 67% using oxytetracycline combined with streptomycin, and as approximately 20% using oxytetracycline alone (Nicoletti et al., ).
Article 7(d)(iv) Biosecurity measures AvailabilityParameter 1 - Available biosecurity measures
Brucellosis is mainly spread through:
- animals moving between and within farms and, in particular, the introduction of new animals with unknown or poorly certified officially free status (the entry of latent carriers in particular);
- direct contact with neighbours’ animals/farms infected with brucellosis;
- sharing equipment, feed, water and bedding between farms;
- direct contacts with wildlife (relevant in the case of porcine brucellosis due to B. suis biovar 2).
Measures avoiding these risk factors should contribute to minimise brucellosis spread between infected and healthy herds/flocks. Biosecurity would be focused essentially on controlling and reducing movements of animals (particularly the purchase of replacements avoiding latent carriers), feed, water, people and equipment to and from areas where livestock is kept.
EffectivenessParameter 2 – Effectiveness of biosecurity measures in preventing the pathogen introduction
While the above measures are feasible and effective for minimising brucellosis spread in highly intensified farming systems (usually ruminant dairy herds/flocks and swine reared intensively), they are very difficult to implement in outdoor or fully extensive/transhumant breeding systems, in particular for preventing porcine brucellosis. In the case of brucellosis in domestic ruminants, and at least in the EU, rules on zoning and on restriction of animal movements according the available EU Directives, have been proven very effective to minimise the spread of B. abortus and B. melitensis infections.
In contrast, biosecurity measures minimising the spread of porcine brucellosis due B. suis biovar 2 in the EU are very difficult (if not impossible) to implement. As this infection is widespread in wildlife, the only feasible biosecurity measures are: (i) reducing the wildlife density and (ii) avoiding the contacts between wildlife and domestic swine though suitable fencing (EFSA, ).
FeasibilityParameter 3 – Feasibility of biosecurity measures
Biosecurity measures for avoiding the spread of B. abortus and B. melitensis infections in domestic ruminants based on the current rules on zoning and on restriction of animal movements according the available EU Directives, have been proven feasible and very effective.
However, biosecurity measures minimising the spread of porcine brucellosis due B. suis biovar 2 in the EU are very difficult (if not impossible) to implement. Reducing the density of wild boar (the main reservoir of infection) can be attempted but results are uncertain given the high capacity for movements of these wild animals. The total depopulation of wild reservoir species seems neither feasible nor ethically justified. The most effective way to prevent contacts between wild boar and domestic pigs is a suitable fencing system (EFSA, ). However, while this suitable (usually very expensive) fencing is feasible for some particular backyard farms and industrial outdoor breeding holdings, it cannot be implemented in fully extensive systems like those typical for Iberian pigs in the Iberian Peninsula and other similar outdoor pig breeding systems.
Article 7(d)(v) Restrictions on the movement of animals and products AvailabilityParameter 1 – Available movement restriction measures
Council Directive 64/432/EEC, Council Directive 91/68/EEC and Commission Decisions lay down conditions applying to imports of live animals and products from third countries. The SPS Agreement recognises the OIE as the relevant international organisation responsible for the development and promotion of international animal health standards, guidelines, and recommendations affecting trade in live animals and animal products. These internationally accepted rules are contained in the OIE Terrestrial Animal Health Code (
Parameter 2 – Effectiveness of restriction of animal movement in preventing the between farm spread
The existing EU Directives on the restriction of movements have proven to be highly effective in preventing the spread of brucellosis between farms in the MS in which the disease yet exists. However, these rules allow that animals born from infected dams but showing false negative results in the official tests and that may be latently infected may qualify for OBF status. To avoid this possibility, MS currently involved in the EU official eradication programmes state generally require animals born from infected dams to be also culled in the infected holdings that are not submitted to full depopulation.
FeasibilityParameter 3 – Feasibility of restriction of animal movement
The Council Directives dealing with restrictions of animal movement (see Parameter above) have been successfully implemented by MS many years ago, and have proven to be of paramount importance in the successful eradication of brucellosis and to reduce the spread of the disease in the countries in which the disease is yet present. Accordingly, these measures have a wide acceptance in the EU MS and have been proven feasible. Computerised management of livestock movements constitutes a further step in the management of health hazards associated with the movement of animals. To facilitate such control, the EU require national computerised registers containing basic details about any national movement of animals and, in some cases, international movement. Furthermore, the Trade Control and Expert System (TRACES) has been widely implemented in EU MS. This is an on-line system which comprises a network of Veterinary Authorities and economic operators of Member States (Commission Decision 2003/623/EC).
Article 7(d)(vi) Killing of animals AvailabilityParameter 1 – Available methods for killing animals
Brucellosis eradication requires the identification of infected animals, their progressive elimination from the herd/flock and replacement with non-infected animals (Crespo Léon et al., ). Council Directives 64/432/EEC (amended and updated) – for bovines – and 91/68/EEC – for sheep and goats – establish the procedures for gaining, maintaining, suspending, withdrawing or regaining the OBF status in the EU. The culling of infected animals (and even the full depopulation of the affected herd/flock) is properly stated and justified in both Directives, and this has been a tool of critical importance for the successful eradication of brucellosis in some MS, as well as for the significant reduction of spread in those MS in which brucellosis yet exists.
In the case of identifying and confirming B. suis infection in holdings belonging to MS, the slaughter of infected pigs is recommended. However, in these cases it is more advisable to adopt whole-herd depopulation (the measure currently applied in the few cases in which B. suis outbreaks have been confirmed in EU MS) as this would reduce the risk of spread to other holdings (EFSA, ).
EffectivenessParameter 2 – Effectiveness of killing animals (at farm level or within the farm) for reducing /stopping spread of the disease
The killing of infected animals or the whole depopulation of infected holdings has been successfully implemented in EU MS for many years, and proven to be of paramount importance in the successful eradication of brucellosis in some MS as well as to reduce the spread of the disease in MS in which the disease is still present.
FeasibilityParameter 3 – Feasibility of killing animals
These measures have a wide acceptance in the EU and have been proven effective and feasible after many years of application.
Article 7(d)(vii) Disposal of carcasses and other relevant animal by-products AvailabilityParameter 1 – Available disposal option
At the EU level, the killing of infected animals (or the whole herd/flock) can be made by several procedures, all proven feasible and effective after many years of application of the official eradication programmes. The slaughter of infected animals/whole holdings can be made at field level in the affected holding or, alternatively, in selected places authorised for this purpose. Once killed, the animals have to be sent to authorised disposal centres, according the rules stated in Regulation (EC) No 1069/2009. Alternatively, the infected animals (or the whole herd/flock affected) can be sent to specially authorised slaughterhouses, and the carcasses can be authorised for human consumption according the rules described in Regulations (CE) No 853/2004 and (EC) No 854/2004. In the EU Food Law, brucellosis in animals is listed as a specific hazard and detailed provisions for the disease to ensure safety of meat and to protect public health have been established therein. Chapter IX (F) of Section IV of Annex I to Regulation (EC) No 854/2004 lays down specific rules for the organisation of official controls on products of animal origin intended for human consumption.
EffectivenessParameter 2 – Effectiveness of disposal option
The above options have been successfully applied by EU MS for many years and proven safe and effective enough for the disposal of brucellosis infected animals/holdings.
FeasibilityParameter 3 – Feasibility of disposal option
The above options have been successfully applied in EU MS for many years, and proven feasible for the disposal of brucellosis infected animals/holdings.
Article 7(e) The impact of disease prevention and control measures Article 7(e)(i) The direct and indirect costs for the affected sectors and the economy as a wholeThere are very few well-documented studies on the production losses and the economic impact of brucellosis taking into account all aspects of the disease. In particular, little is known about how brucellosis affects animal production quantitatively, and the figures used as a reference were established empirically many years ago (Bernués et al., ). Moreover, well-documented studies on the indirect costs of brucellosis are also scarce. A review of the studies available concludes that brucellosis is in all likelihood a major problem in low-income countries of Africa and Asia (McDermott et al., ).
An overall brucellosis framework that considers costs of illness, costs of prevention, and opportunity costs (both public and private) at household, livestock sector, health sector and broader societal levels is shown in Table .
It can be concluded that the cost estimates published for brucellosis are of limited value.
Costs to be considered and estimated when planning brucellosis control and eradication programmes (McDermott et al., )
Dark grey boxes: market prices available and commonly included in economic assessments of disease. Light grey boxes: market prices not available so costs need to be estimated through other methods. White boxes: prevention costs reflect efficiency and effectiveness of public and private service provision. Usually there are few data and only rough estimates are made. Black box: included in health metrics (DALYs: disability-adjusted life years).
24A number of costs (for example, vaccination) produce benefits for both the private sector (better livestock production) and the public sector (fewer human infections).
Parameter 1 – Cost of control (e.g. treatment/vaccine, biosecurity)
In rich countries, an important part of successful brucellosis eradication has been the official compensations given to farmers for the culled livestock. However, in high prevalence conditions and in most resource-limited countries, eradication is not feasible, and applying control programmes is the only suitable option (Blasco and Molina-Flores, ). To attempt control (usually through mass vaccination of the whole susceptible population), the benefits to public health and society need to be demonstrated, particularly in countries with limited resources. The costs of these control programmes are highly variable and depend essentially of the country, the animal species involved, the vaccination programme selected (for a review see Blasco and Molina-Flores () and Blasco et al. ()), and the vaccine used. Accordingly, well-documented economic analyses of brucellosis control programmes are also scarce.
An interesting cost-benefit study of a control programme based on vaccination of small ruminants with the Rev.1 vaccine was conducted in Portugal (Coelho et al., ). The most relevant costs saved and expensed when applying a mass-vaccination programme with Rev.1 are shown in Table .
Total incremental costs in US$ for Brucella control using a strategy based on mass vaccination of small ruminant with Rev.1 vaccine in Trás-os-Montes e Alto Douro (2000–2005), Portugal (Coelho et al., )
| Difference between the years | Compensation costs paid to farmers | Vaccine costs | Cost of patient hospitalisation | Total | ||||
| Spent | Saved | Spent | Saved | Spent | Saved | Spent | Saved | |
| 2000–2001 | 115,357 | – | 19,592 | – | – | 24,451 | 110,498 | – |
| 2000–2002 | – | 331,148 | 29,843 | – | – | 89,411 | – | 390,716 |
| 2000–2003 | – | 1,069,300 | 39,681 | – | – | 206,507 | – | 1,236,125 |
| 2000–2004 | – | 1,870,307 | 55,826 | – | – | 341,399 | – | 2,155,879 |
| 2000–2005 | – | 2,577,002 | 60,788 | – | – | 502,356 | – | 3,018,569 |
| Mean/year | – | 515,400 | 12,158 | – | – | 100,741 | – | 603,714 |
In the five years of study, more than US$ 3,000,000 were saved after mass vaccination with Rev.1 with respect to the costs generated by an eradication programme (consisting in the vaccination of only young replacements and testing and culling the adult sheep and goats) with an annual average reduction in monetary costs of US$ 603,714. The annual average saving in costs of compensation paid to farmers and cost of patient hospitalisation in hospitals were US$ 515,400 and US$ 100,471, respectively (Coelho et al., ).
Parameter 2 – Cost of eradication (culling, compensation)
Due to the important variations in the prevalence and in the costs of diagnostic tools/vaccines and of the operative costs of the involved private/public veterinary services in the different countries, no internationally recognised costs have been defined for eradication, monitoring and surveillance. However, precise figures, updated yearly and available on line (
Sheep and goats
As an example, the costs of the eradication programme for brucellosis in small ruminants submitted to the EU by Portugal (
Cattle
The total cost of the brucellosis eradication programme to be carried out in bovines in Italy for year 2016 is €11,219,302. This was calculated considering the following relevant figures: 33,822 flocks to be tested, 0.71% expected collective (herd) prevalence, 1,004,279 animals to be tested, and 0.37% expected individual prevalence.
Between 2007 and 2011, the total cost incurred by the Health Service of Lazio Region (Italy) for the eradication of brucellosis in cattle was estimated in 5,996.809 EUR, of those 4,797,389 were the cost of the veterinarians labour, 8,864 for the transport, 23,908 for disposal and compensation for culled animals (Caminiti et al., ).
Parameter 3 – Cost of surveillance and monitoring
See above.
Parameter 4 – Trade loss (bans, embargoes, sanctions) by animal product
See next Parameter.
Parameter 5 – Importance of the disease for the affected sector (% loss or € lost compared to business amount of the sector)
Economic losses due to a serious and unexpected brucellosis outbreak occurring in an officially free MS could be large and widespread if no official intervention is conducted. First, losses would include the value of lost production, the cost of destroying diseased or potentially diseased animals, and the costs of containment (diagnostics, compensation to producers for destroyed animals, disposal costs and costs of veterinary services). Second, and very important, export markets could be lost if importing countries place restrictions on products to prevent the possibility of disease spread. Third, multiplier effects could ripple through the economy due to decreased sales by agriculturally dependent businesses (farm input suppliers, food manufacturing, transportation, retail grocery, and food service). Finally, as brucellosis is a zoonosis, tourism could be affected also if negative perceptions for food or personal safety exist. Depending on the erosion of consumers’ confidence and export sales, market prices of the affected commodities (essentially live animals and meat) may drop. This would affect not only to the owners of the affected area but also to producers whose herds were not directly infected, making the event national in scale even if the disease itself is contained to a small region.
Fortunately, the expected impact of a brucellosis outbreak in a given officially free MS in the current epidemiological situation should not be very high due to the existence of zoning or regionalisation in the EU, and the continuous surveillance of the brucellosis free areas, allowing an early response in the eventual detection of any brucellosis outbreak. Zone/region means a clearly defined part of a country containing an animal subpopulation with a distinct health status with respect to a specific disease (brucellosis in this case) for which required surveillance, control and biosecurity measures have been applied for trade purposes. Accordingly, the EU defines clearly and regularly the MS regions with the different brucellosis status inside the national boundaries for the purposes of international trade or disease control strategies. Having in consideration the favourable evolution of brucellosis even in the MS in which infection persists, and the epidemiological nature of brucellosis (low capacity of spreading at the short term), any unexpected local brucellosis outbreak should not have important consequences for the sector if interventions are applied over a short period. An exception could be porcine brucellosis since the EU is the main exporter of swine/swine meat to the international markets (around 37% of the total exports worldwide). If trade were limited by third countries, the consequences for the EU swine industry could be very important.
Article 7(e)(ii) The societal acceptance of disease prevention and control measuresConsumer confidence in government may be tested depending on the scale of the eradication effort and the means used for the disposal the animals culled. The need to slaughter thousands of animals could generate public criticism if culling methods are considered inhumane or if the destruction of carcasses is questioned environmentally. This should thus be avoided. Fortunately, the currently applied culling and disposal systems used in the EU eradication programmes for brucellosis have been widely accepted by the affected owners and the society in general.
Article 7(e)(iii) The welfare of affected subpopulations of kept and wild animalsParameter 1 – Welfare impact of control measures on domestic animals
Whenever properly managed by competent veterinarians, the measures implemented for controlling brucellosis (usually through vaccination), do not pose a relevant issue from the animal welfare standpoint.
Parameter 2 – Wildlife depopulation as control measure
This is not an issue in the case of B. abortus and B. melitensis infections since wild animals are very rarely affected and, in the case of sporadic infections, this does not have any epidemiological significance. In the very rare event that high prevalence of these infections is found in wildlife (i.e. the case of the Alpine Ibex infected by B. melitensis in a very restricted area of the French Alps (Mick et al., ), the depopulation of the affected wild animals could be considered whenever this be feasible, socially acceptable, and the animal species involved is not endangered.
In contrast, this could be considered in the case of the infection caused by B. suis biovar 2 since both wild boar and hares are the wild reservoir of porcine brucellosis in the EU and the prevalence is very high in both species (EFSA, ; Muñoz et al., ). The precise role played by hares in the transmission of infection to swine remains unclear (EFSA, ). However, available evidence suggests that wild boar is the main source of infection for domestic pigs bred in outdoor rearing systems, even on fenced premises (EFSA, ; Muñoz et al., ). This outdoor housing is used in open air semi-intensive systems or in extensive systems (as the free ranging Iberian pig system), which have a moderate to high but permanent risk of infection via contacts with infected wild boar (EFSA, ; Muñoz et al., ). As full depopulation of wild boar in the EU is unfeasible, reducing the population density of wild boar could be a suitable alternative to reduce the risk of transmission of B. suis biovar 2 to domestic pigs reared in these outdoor breeding systems.
Article 7(e)(iv) The environment and biodiversity EnvironmentParameter 1 – Use and potential residuals of biocides or medical drugs in environmental compartments (soil, water, feed, manure)
No drugs/chemicals other than the common and legally accepted disinfectants are used in the current control/eradication campaigns in the EU.
BiodiversityParameter 2 – Mortality in wild species
Wild animals are not affected significantly by the disease in the EU, with the exception of B. suis biovar 2 affecting wild boar and hares. However, brucellosis is a non-fatal disease for wildlife and domestic animals.
Assessment according to Article 5 criteriaThis section presents the results of the expert judgement on the criteria of Article 5 of the AHL about the infection with B. abortus, B. melitensis and B. suis (Table ). The expert judgement was based on Individual and Collective Behavioural Aggregation (ICBA) approach described in detail in the opinion on the methodology (EFSA AHAW Panel, ). Experts have been provided with information of the disease fact-sheet mapped into Article 5 criteria (see supporting information, Annex A), based on that the experts indicate their Y/N or ‘na’ judgement on each criterion of Article 5, and the reasoning supporting their judgement.
The minimum number of judges in the judgement was 10. The expert judgement was conducted as described in the methodological opinion (EFSA AHAW Panel, ). For details on the interpretation of the questions, see Appendix B of the methodological opinion (EFSA AHAW Panel, ).
Outcome of the expert judgement on the Article 5 criteria for the infection with Brucella abortus, B. melitensis and B. suis
| Criteria to be met by the disease: According to AHL, a disease shall be included in the list referred to in point (b) of paragraph 1 of Article 5 if it has been assessed in accordance with Article 7 and meets all of the following criteria | Final outcome | |
| A(i) | The disease is transmissible | Y |
| A(ii) | Animal species are either susceptible to the disease or vectors and reservoirs thereof exist in the Union | Y |
| A(iii) | The disease causes negative effects on animal health or poses a risk to public health due to its zoonotic character | Y |
| A(iv) | Diagnostic tools are available for the disease | Y |
| A(v) | Risk-mitigating measures and, where relevant, surveillance of the disease are effective and proportionate to the risks posed by the disease in the Union | Y |
| At least one criterion to be met by the disease: In addition to the criteria set out above at point A(i)-A(v), the disease needs to fulfil at least one of the following criteria | ||
| B(i) | The disease causes or could cause significant negative effects in the Union on animal health, or poses or could pose a significant risk to public health due to its zoonotic character | Y |
| B(ii) | The disease agent has developed resistance to treatments and poses a significant danger to public and/or animal health in the Union | N |
| B(iii) | The disease causes or could cause a significant negative economic impact affecting agriculture or aquaculture production in the Union | Y |
| B(iv) | The disease has the potential to generate a crisis or the disease agent could be used for the purpose of bioterrorism | Y |
| B(v) | The disease has or could have a significant negative impact on the environment, including biodiversity, of the Union | N |
Colour code: green = consensus (Yes/No).
Outcome of the assessment of the infection with Brucella abortus, B. melitensis and B. suis according to criteria of Article 5(3) of the AHL on its eligibility to be listedAs from the legal text of the AHL, a disease is considered eligible to be listed as laid down in Article 5 if it fulfils all criteria of the first set from A(i) to A(v) and at least one of the second set of criteria from B(i) to B(v). According to the assessment methodology (EFSA AHAW Panel, ), a criterion is considered fulfilled when the outcome is ‘Yes’. According to the results shown in Table , the infection with B. abortus, B. melitensis and B. suis complies with all criteria of the first set and with three criteria of the second set, therefore it is considered eligible to be listed as laid down in Article 5 of the AHL.
Assessment according to Article 9 criteriaThis section presents the results of the expert judgement on the criteria of Annex IV referring to categories as in Article 9 of the AHL about the infection with B. abortus, B. melitensis and B. suis (Tables , , , and ). The expert judgement was based on ICBA approach described in detail in the opinion on the methodology. Experts have been provided with information of the disease fact-sheet mapped into Article 9 criteria (see supporting information, Annex A), based on that the experts indicate their Y/N or ‘na’ judgement on each criterion of Article 9, and the reasoning supporting their judgement.
The minimum number of judges in the judgement was ten. The expert judgement was conducted as described in the methodological opinion (EFSA AHAW Panel, ). For details on the interpretation of the questions see Appendix B of the methodological opinion (EFSA AHAW Panel, ).
Outcome of the expert judgement related to the criteria of Section 1 of Annex IV (category A of Article 9) for the infection with Brucella abortus, B. melitensis and B. suis
| Criteria to be met by the disease: The disease needs to fulfil all of the following criteria | Final outcome | |
| 1 | The disease is not present in the territory of the Union OR present only in exceptional cases (irregular introductions) OR present in only in a very limited part of the territory of the Union | N |
| 2.1 | The disease is highly transmissible | N |
| 2.2 | There be possibilities of airborne or waterborne or vector-borne spread | Y |
| 2.3 | The disease affects multiple species of kept and wild animals OR single species of kept animals of economic importance | Y |
| 2.4 | The disease may result in high morbidity and significant mortality rates | N |
| At least one criterion to be met by the disease: In addition to the criteria set out above at point 1-2.4, the disease needs to fulfil at least one of the following criteria | ||
| 3 | The disease has a zoonotic potential with significant consequences on public health, including epidemic or pandemic potential OR possible significant threats to food safety | N |
| 4 | The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals | NC |
| 5(a) | The disease has a significant impact on society, with in particular an impact on labour markets | N |
| 5(b) | The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals | NC |
| 5(c) | The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it | N |
| 5(d) | The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds | N |
Colour code: green = consensus (Yes/No), yellow = no consensus (NC).
Outcome of the expert judgement related to the criteria of Section 2 of Annex IV (category B of Article 9) for the infection with Brucella abortus, B. melitensis and B. suis
| Criteria to be met by the disease: The disease needs to fulfil all of the following criteria | Final outcome | |
| 1 | The disease is present in the whole OR part of the Union territory with an endemic character AND (at the same time) several Member States or zones of the Union are free of the disease | Y |
| 2.1 | The disease is moderately to highly transmissible | Y |
| 2.2 | There be possibilities of airborne or waterborne or vector-borne spread | Y |
| 2.3 | The disease affects single or multiple species | Y |
| 2.4 | the disease may result in high morbidity with in general low mortality | Y |
| At least one criterion to be met by the disease: In addition to the criteria set out above at point 1-2.4, the disease needs to fulfil at least one of the following criteria | ||
| 3 | The disease has a zoonotic potential with significant consequences on public health, including epidemic potential OR possible significant threats to food safety | Y |
| 4 | The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals | NC |
| 5(a) | The disease has a significant impact on society, with in particular an impact on labour markets | N |
| 5(b) | The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals | NC |
| 5(c) | The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it | N |
| 5(d) | The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds | N |
Colour code: green = consensus (Yes/No), yellow = no consensus (NC).
Outcome of the expert judgement related to the criteria of Section 3 of Annex IV (category C of Article 9) for the infection with Brucella abortus, B. melitensis and B. suis
| Criteria to be met by the disease: The disease needs to fulfil all of the following criteria | Final outcome | |
| 1 | The disease is present in the whole OR part of the Union territory with an endemic character | Y |
| 2.1 | The disease is moderately to highly transmissible | Y |
| 2.2 | The disease is transmitted mainly by direct or indirect transmission | Y |
| 2.3 | The disease affects single or multiple species | Y |
| 2.4 | The disease usually does not result in high morbidity and has negligible or no mortality AND often the most observed effect of the disease is production loss | Y |
| At least one criterion to be met by the disease: In addition to the criteria set out above at point 1-2.4, the disease needs to fulfil at least one of the following criteria | ||
| 3 | The disease has a zoonotic potential with significant consequences on public health, or possible significant threats to food safety | Y |
| 4 | The disease has a significant impact on the economy of the Union, mainly related to its direct impact on certain types of animal production systems | N |
| 5(a) | The disease has a significant impact on society, with in particular an impact on labour markets | N |
| 5(b) | The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals | NC |
| 5(c) | The disease has a significant impact on the environment, due to the direct impact of the disease OR due to the measures taken to control it | N |
| 5(d) | The disease has a significant impact on a long-term effect on biodiversity or the protection of endangered species or breeds, including the possible disappearance or long-term damage to those species or breeds | N |
Colour code: green = consensus (Yes/No), yellow = no consensus (NC).
Outcome of the expert judgement related to the criteria of Section 4 of Annex IV (category D of Article 9) for the infection with Brucella abortus, B. melitensis and B. suis
| Criteria to be met by the disease: The disease needs to fulfil all of the following criteria | Final outcome |
| The risk posed by the disease in question can be effectively and proportionately mitigated by measures concerning movements of animals and products in order to prevent or limit its occurrence and spread | Y |
| The disease fulfils criteria of section 1, 2, 3 or 5 of Annex IV of AHL | Y |
Colour code: green = consensus (Yes/No).
Outcome of the expert judgement related to the criteria of Section 5 of Annex IV (category E of Article 9) for the infection with Brucella abortus, B. melitensis and B. suis
| Diseases in category E need to fulfil criteria of section 1, 2 or 3 of Annex IV of AHL and/or the following: | Final outcome | |
| E | Surveillance of the disease is necessary for reasons relating to animal health, animal welfare, human health, the economy, society or the environment (If a disease fulfils the criteria as in Article 5, thus being eligible to be listed, consequently category E would apply.) | Y |
Colour code: green = consensus (Yes/No).
Non-consensus questionsThis section displays the assessment related to each criterion of Annex IV referring to the categories of Article 9 of the AHL where no consensus was achieved in form of tables (Tables , and ). The proportion of Y, N or ‘na’ answers are reported, followed by the list of different supporting views for each answer.
Outcome of the expert judgement related to criterion 2.1 of Article 9
| Question | Final outcome | Response | |||
| Y (%) | N (%) | na (%) | |||
| 2.1 (cat.A) | The disease is highly transmissible | NC | 50 | 50 | 0 |
| 2.1 (cat.B,C) | The disease is moderately to highly transmissible | NC | 50 | 50 | 0 |
Number of judges: 10; NC: non-consensus.
Reasoning supporting the judgement
supporting Yes for 2.1 (cat.A):
- Within-herd animal prevalence rapidly reaches 30–100% when infection is first introduced into a herd or flock.
- The infective dose is low and thus it is the most frequent and easily acquired zoonotic occupational infection.
- Latency with negative serology and disease recrudescence during pregnancy are common and responsible for many incidents of transmission to large numbers of animals.
- The estimation of R0 is not straightforward because transmission dynamics are complicated by multiple interactions between animals.
- supporting Yes for 2.1 (cat.B,C):
- Published R (R0, Re) values are relatively low (less than 2 in most cases).
After discussion, the AHAW Panel reached consensus about the disease being at least moderately transmissible.
Outcome of the expert judgement related to criterion 4 of Article 9
| Question | Final outcome | Response | |||
| Y (%) | N (%) | na (%) | |||
| 4 (cat.A,B) | The disease has a significant impact on the economy of the Union, causing substantial costs, mainly related to its direct impact on the health and productivity of animals | NC | 90 | 10 | 0 |
Number of judges: 10; NC: non-consensus.
27At the time of the collective judgement, the assessment of the current impact considering the control measures in place was considered.
Reasoning supporting the judgement
supporting Yes:
- The disease has a substantial impact in infected areas, as a consequence of abortion and infertility.
- The disease can affect all productions systems for each susceptible species.
- The loss of the officially free status may have important economic consequences due to the ban on trade of live animals for breeding or slaughter (breeders in particular) as well as semen, embryos and raw-milk products (OIE code provisions).
supporting No:
- In the current situation and given the control measures in place in the EU, the impact is not significant on the economy of the whole Union due to actual low prevalence and incidence in MSs (maximum 0.78% prevalence and 0.61% incidence in Italy in 2016 in small ruminants (expected).
Outcome of the expert judgement related to criterion 5(b) of Article 9
| Question | Final outcome | Response | |||
| Y (%) | N (%) | na (%) | |||
| 5(b) | The disease has a significant impact on animal welfare, by causing suffering of large numbers of animals | NC | 70 | 30 | 0 |
Number of judges: 10; NC: non-consensus.
29At the time of the collective judgement, the assessment of the current impact considering the control measures in place was considered.
Reasoning supporting the judgement
supporting Yes:
- Brucellosis is considered a major contributor to animal suffering, causing fever, abortions, stillbirths and the birth of weak offspring, with the ensuing increase of perinatal mortality.
- It is present in more than in 3 countries.
supporting No:
- In the current situation and given the control measures in place in the EU, there is no welfare impact on large number of animals because of the low prevalence.
As from the legal text of the AHL, a disease is considered fitting in a certain category (A, B, C, D or E corresponding to point (a) to point (e) of Article 9(1) of the AHL) if it is eligible to be listed for Union intervention as laid down in Article 5(3) and fulfils all criteria of the first set from 1 to 2.4 and at least one of the second set of criteria from 3 to 5(d) as shown in Tables –. According to the assessment methodology (EFSA AHAW Panel, ), a criterion is considered fulfilled when the outcome is ‘Yes’.
A description of the outcome of the assessment of criteria in Annex IV for the infection with B. abortus, B. melitensis and B. suis for the purpose of categorisation as in Article 9 of the AHL is presented in Table .
Outcome of the assessment of criteria in Annex IV for the infection with Brucella abortus, B. melitensis and B. suis for the purpose of categorisation as in Article 9 of the AHL
| Category | Article 9 criteria | ||||||||||
| 1°set of criteria | 2°set of criteria | ||||||||||
| 1 | 2.1 | 2.2 | 2.3 | 2.4 | 3 | 4 | 5a | 5b | 5c | 5d | |
| Geographical distribution | Transmissibility | Routes of transmission | Multiple species | Morbidity and mortality | Zoonotic potential | Impact on economy | Impact on society | Impact on animal welfare | Impact on environment | Impact on biodiversity | |
| A | N | N | Y | Y | N | N | NC | N | NC | N | N |
| B | Y | Y | Y | Y | Y | Y | NC | N | NC | N | N |
| C | Y | Y | Y | Y | Y | Y | N | N | NC | N | N |
| D | Y | ||||||||||
| E | Y | ||||||||||
According to the assessment here performed, the infection with B. abortus, B. melitensis and B. suis complies with the following criteria of the sections 1–5 of Annex IV of the AHL for the application of the disease prevention and control rules referred to in points (a) to (e) of Article 9(1):
- For being assigned to category A, a disease needs to comply with all criteria of the first set (1, 2.1–2.4) and according to the assessment brucellosis complies with criteria 2.2, 2.3, but not with 1, 2.1 and 2.4. For being eligible for category A, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a–d) and brucellosis does not comply with criteria 3, 5a, 5c and 5d and the assessment is inconclusive on compliance with criteria 4 and 5b.
- For being assigned to category B, a disease needs to comply with all criteria of the first set (1, 2.1–2.4) and according to the assessment brucellosis complies with all criteria. For being eligible for category B, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a–d) and brucellosis complies with criterion 3, does not comply with criteria 5a, 5c and 5d and the assessment is inconclusive on compliance with criteria 4 and 5b.
- For being assigned to category C, a disease needs to comply with all criteria of the first set (1, 2.1–2.4) and according to the assessment brucellosis complies with all criteria. For being eligible for category C, a disease needs to comply additionally with one of the criteria of the second set (3, 4, 5a–d) and brucellosis complies with criterion 3, does not comply with criteria 4, 5a, 5c and 5d and the assessment is inconclusive on compliance with criterion 5b.
- For being assigned to category D, a disease needs to comply with criteria of section 1, 2, 3 or 5 of Annex IV of the AHL and with the specific criterion D of section 4, which brucellosis complies with.
- For being assigned to category E, a disease needs to comply with criteria of section 1, 2 or 3 of Annex IV of the AHL and/or the surveillance of the disease is necessary for reasons relating to animal health, animal welfare, human health, the economy, society or the environment. The latter is applicable if a disease fulfils the criteria as in Article 5, which brucellosis complies with.
This section presents the results of the assessment on the criteria of Article 8(3) of the AHL about the infection with B. abortus, B. melitensis and B. suis. The Article 8(3) criteria are about animal species to be listed, as it reads below:
‘3. Animal species or groups of animal species shall be added to this list if they are affected or if they pose a risk for the spread of a specific listed disease because:
- they are susceptible for a specific listed disease or scientific evidence indicates that such susceptibility is likely; or
- they are vector species or reservoirs for that disease, or scientific evidence indicates that such role is likely’.
For this reason, the assessment on Article 8 criteria is based on the evidence as extrapolated from the relevant criteria of Article 7, i.e. the ones related to susceptible and reservoir species or routes of transmission, which cover also possible role of biological or mechanical vectors. According to the mapping, as presented in Table , section 3.2 of the scientific opinion on the ad hoc methodology (EFSA AHAW Panel, ), the main animal species to be listed for the infection with B. abortus, B. melitensis and B. suis according to the criteria of Article 8(3) of the AHL are as displayed in Tables and .
Animal species to be listed for the infection with Brucella abortus and B. melitensis according to criteria of Article 8 (source: data reported in Section 3.1.1.1)
| Order | Family | Genus/species | |
| Susceptible | Artiodactyla | Camelidae | Camelus dromedarius, Camelus bactrianus, Lama glama, Vicugna pacos, Lama guanicoe, Vicugna vicugna |
| Cervidae | Cervus elaphus, Alces alces | ||
| Suidae | Sus scrofa | ||
| Bovidae | Bos taurus, Bubalus bubalis, Bison bonasus, Bison bison, Bos grunniens, Syncerus caffer, Capra hircus, Ovis aries, Capra ibex, Rupicapra spp., Capra pyrenaica, Kobus leche kafuensis, Hippotragus niger, Oryx leucoryx | ||
| Carnivora | Canidae | Canis lupus, Canis latrans, Vulpes vulpes | |
| Procyonidae | Procyon lotor | ||
| Didelphimorphia | Didelphidae | Not specified | |
| Perissodactyla | Equidae | Equus caballus | |
| Reservoir | Artiodactyla | Bos taurus (B. abortus) Ovis aries, Capra hircus (B. melitensis) | |
| Vectors | None | ||
Animal species to be listed for the infection with Brucella suis according to criteria of Article 8 (source: data reported in Section 3.1.1.1)
| Order | Family | Genus/species | |
| Susceptible | Artiodactyla | Suidae | Sus scrofa |
| Bovidae | Not specified | ||
| Cervidae | Rangifer tarandus | ||
| Tayassuidae | Peccaries (all genera) | ||
| Perissodactyla | Equidae | Equus caballus | |
| Carnivora | Canidae | Vulpes lagopus, Canis lupus | |
| Rodentia | Not specified | ||
| Lagomorpha | Leporidae | Lepus europaeus | |
| Reservoir | Artiodactyla | Suidae | Sus scrofa (biovars 1, 2 and 3) |
| Tayassuidae | Peccaries (all genera) (biovars 1 and 3) | ||
| Cervidae | Rangifer tarandus (biovar 4) | ||
| Rodentia | Small rodents (several species) (biovars 2 and 5) | ||
| Vectors | None | ||
TOR 1: for each of those diseases an assessment, following the criteria laid down in Article 7 of the AHL, on its eligibility of being listed for Union intervention as laid down in Article 5(3) of the AHL;
- According to the assessment here performed, the infection with B. abortus, B. melitensis and B. suis complies with all criteria of the first set and with three criteria of the second set and therefore can be considered eligible to be listed for Union intervention as laid down in Article 5(3) of the AHL.
TOR 2a: for each of the diseases which was found eligible to be listed for Union intervention, an assessment of its compliance with each of the criteria in Annex IV to the AHL for the purpose of categorisation of diseases in accordance with Article 9 of the AHL;
- According to the assessment here performed, the infection with B. abortus, B. melitensis and B. suis meets the criteria as in sections 2, 3, 4, and 5 of Annex IV of the AHL, for the application of the disease prevention and control rules referred to in points (b), (c), (d), and (e) of Article 9(1) of the AHL.
TOR 2b: for each of the diseases which was found eligible to be listed for Union intervention, a list of animal species that should be considered candidates for listing in accordance with Article 8 of the AHL.
- According to the assessment here performed, the animal species that can be considered to be listed for the infection with B. abortus, B. melitensis and B. suis according to Article 8(3) of the AHL are several mammal species, as reported in Tables and in Section 3.4 of the present document.
1007Commission Implementing Decision (EU) 2016/168 of 5 February 2016 amending the Annexes to Decision 2003/467/EC establishing the official tuberculosis, brucellosis and enzootic-bovine-leukosis-free status of certain Member States and regions of Member States as regards bovine herds. OJ L 32, 9.2.2016, p. 153–157.
1008Commission Decision of 17 November 2010 amending the Annexes to Decision 93/52/EEC as regards the recognition of Estonia, Latvia and the Autonomous Community of the Balearic Islands in Spain as officially free of brucellosis (B. melitensis) and amending Annexes I and II to Decision 2003/467/EC as regards the declaration of Estonia as officially tuberculosis-free and officially brucellosis-free as regards bovine herds. OJ L 303, 19.11.2010, p. 14–17.
1009Council Directive 64/432/EEC of 26 June 1964 on animal health problems affecting intra-Community trade in bovine animals and swine. OJ 121, 29.7.1964, p. 1977–2012.
1010Council Directive 91/68/EEC of 28 January 1991 on animal health conditions governing intra-Community trade in ovine and caprine animals. OJ L 46, 19.2.1991, p. 19–36.
10112003/623/EC: Commission Decision of 19 August 2003 concerning the development of an integrated computerised veterinary system known as Traces. OJ L 216, 28.8.2003, p. 58–59.
1012Regulation (EC) No 1069/2009 of the European Parliament and of the Council of 21 October 2009 laying down health rules as regards animal by-products and derived products not intended for human consumption and repealing Regulation (EC) No 1774/2002 (Animal by-products Regulation). OJ L 300, 14.11.2009, p. 1–33.
1013Regulation (EC) No 853/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific hygiene rules for food of animal origin. OJ L 139, 30.4.2004, p. 55–205.
1014Regulation (EC) No 854/2004 of the European Parliament and of the Council of 29 April 2004 laying down specific rules for the organisation of official controls on products of animal origin intended for human consumption. OJ L 139, 30.4.2004, p. 206–320.
1015A vector is a living organism that transmits an infectious agent from an infected animal to a human or another animal. Vectors are frequently arthropods. Biological vectors may carry pathogens that can multiply within their bodies and be delivered to new hosts, usually by biting. In mechanical vectors the pathogens do not multiply within the vector, which usually remains infected for shorter time than in biological vectors.
Abbreviations
- AHAW
- EFSA Panel on Animal Health and Welfare
- AHL
- Animal Health Law
- BBAT
- Buffered Brucella antigen test
- BPAT
- buffered plate agglutination test
- BST
- Brucellin skin-test
- CDC
- Centers for Disease Control and Prevention
- CFSPH
- Center for Food Security and Public Health
- CFR
- Code of Federal Regulations of the US
- CFT
- complement fixation test
- CFU
- colony forming unit
- CITES
- the Convention on International Trade in Endangered Species of Wild Fauna and Flora
- DALY
- Disability-adjusted life year
- DSe
- diagnostic sensitivity
- DSp
- diagnostic specificity
- ELISA
- enzyme-linked immunosorbent assay
- FAO
- Food and Agriculture Organization of the United Nations
- FPA
- fluorescence polarisation assay
- FPSR
- false positive serological reactions
- ICBA
- Individual and Collective Behavioural Aggregation
- IUCN
- International Union for Conservation of Nature
- HHS
- Department of Health and Human Services
- MRT
- milk ring test
- MS
- Member State
- NH
- native hapten
- OBF
- Officially Brucellosis-Free
- ObmF
- Officially Brucella melitensis-free
- OIE
- World Health Organization for Animal Health
- PCR
- polymerase chain reaction
- RBT
- Rose Bengal test
- R0
- basic reproductive ratio
- Re
- effective reproductive ratio
- SAT
- standard tube agglutination test
- ToR
- Terms of Reference
- TRACES
- Trade Control and Expert System
- WHO
- World Health Organization
- YLD
- years lost due to disability
- YLL
- years of life lost due to premature mortality
- USDA APHIS
- US Department of Agriculture's Animal and Plant Health Inspection Service
| Tests | % DSe (no. tested) [95% CI] with sera from | %DSp (no. tested) [95% CI] with sera from | |||
| Brucella infected | Brucella free | S19 vaccinated (no. calves/months after vaccination) [95% CI] | Reference | Affected by FPSR (data from Muñoz et al. 2004) | |
| stRBT | 100 (112) [95.9–100] | 100 (95) [95.2–100] | n.d. | Díaz-Aparicio et al. () | n.d. |
| BPAT | 97.8 (636) [96.2–98.7] | 98.7 (1,446) [97.9–99.2] | 48.7 (261/n.d.) [42.5–54.9] | Nielsen et al. () | n.d. |
| n.d. | n.d | 50 (56/4) [36.5–63.5] | Lord and Cherwonogrodzky () | n.d. | |
| SAT | 81.5 (146) [74.1–87.3] | 98.9 (995) [98.0–99.4] | n.d. | McGiven et al. () | n.d. |
| n.d. | n.d. | 81 (56/4) [67.2–89.3] | Lord and Cherwonogrodzky () | n.d. | |
| CFT | 91.8 (146) [85.8–95.5] | 99.9 (995) [99.3–100] | n.d. | McGiven et al. () | n.d. |
| 97.6 (636) [96.0–98.6] | 99.9 (1,446) [99.6–100] | n.d. | Nielsen et al. () | n.d. | |
| 94.5 (147) [89.2–97.4] | 100 (640) [99.3–100] | n.d. | Stack et al. () | n.d. | |
| n.d. | n.d | 49 (56/4) [34.8–61.8] | Lord and Cherwonogrodzky () | n.d. | |
| 100 (112) [95.9–100] | 100 (95) [95.2–100] | 48 (40/2 [31.8–63.7] | Díaz-Aparicio et al. () | n.d. | |
| iELISA -NH | 100 (75) [93.9–100] | 97.7 (130) [92.9–99.4] | 85.2 (61/3) [73.3–92.6] | Abalos et al. () | n.d. |
| iELISA -S/LPS | 97.2 (146) [92.7–99.1] | 97.8 (6,957) [97.4–98.1] | n.d. | McGiven et al. () | n.d. |
| 100 (424) [99.0–100] | 99.7 (15,715) [99.6–99.8] | 56.3 (261/n.d.) [50.1–62.4] | Nielsen et al. () | n.d. | |
| 100 (98–100 [189]) | 100 (96.7–100 [112]) | n.d. | Muñoz et al. (2004) | 58.4 (49.2–67.1 [125]) | |
| cELISA-S/LPS | 95.2 (146) [90.0–97.9] | 99.7 (1,440) [99.2–99.9] | n.d. | McGiven et al. () | n.d. |
| 100 (636) [99.3–100] | 99.7 (1,446) [99.2–99.9] | 100 (261/n.d.) [98.2–100] | Nielsen et al. () | n.d. | |
| 84.4 (78.3–89.4 [180]) | 100 (95.9–100 [90]) | n.d. | Muñoz et al. (2004) | 88.8 (81.9.3–93.7 [125]) | |
| FPA | 96.6 (146) [91.8–98.7] | 99.1 (1,947) [98.5–99.4) | n.d. | McGiven et al. () | n.d. |
| 99.3 (1,084) [98.5–99.7] | 100 (23,755) [99.98–100] | n.d. | Nielsen and Gall () | n.d. | |
| n.d. | n.d | 99.2 (248/n.d.) [96.8–99.9] | Nielsen et al. () | n.d. | |
| GD-S/LPS | n.d. | n.d. | 81 (56/4) [67.2–89.3] | Lord and Cherwonogrodzky () | n.d. |
| GD-NH | n.d. | n.d. | 100 (432/6) [98.9–100] | Lord et al. () | n.d. |
| RID-NH | 92.0 (112) [84.9–96.0] | 100 (95) [95.2–100] | 100 (40/2) [89.1–100] | Díaz-Aparicio et al. () | 100 (97.1–100 [125]) |
| Reference | Test | % DSp (no./age in months/months after Rev 1 vaccination) [95% CI] | |||
| %DSe | Brucella free | Conjunctival | Subcutaneous | ||
| Stournara et al. () | RBT | 90.3 | 99.6 | 100 (48/≤ 3/4) [90.8–100] | n.d. |
| 64 (106/≥ 24/4) [54.2–73.1] | n.d. | ||||
| mRBT | 97.5 | 98.1 | 100 (48/≤ 3/4) [90.8–100] | n.d. | |
| 47 (106/≥ 24/4) [37.5–57.0] | n.d. | ||||
| CFT | 98.7 | 100 | 100 (48/≤ 3/4) [90.8–100] | n.d. | |
| 86.0 (106/≥ 24/4) [77.4–91.6] | n.d. | ||||
| iELISA | 97.5 | 100 | 100 (48/≤ 3/4) [90.8–100] | n.d. | |
| 50.0 (106/≥ 24/4) [40.2–59.8] | n.d. | ||||
| cELISA | 96.3 | 99.4 | 100 (48/≤ 3/4) [90.8–100] | n.d. | |
| 90 (106/≥ 24/4) [81.8–94.5] | n.d. | ||||
| FPA | 97.5 | 98.9 | 98 (48/≤ 3/4) [87.5–99.9] | n.d. | |
| 81 (106/≥ 24/4) [72.1–87.8] | n.d. | ||||
| Salih-Alj Debbarh et al. () | iELISA CP28 | 89 | 100 | 100(10/3/1) [65.5–100] | n.d. |
| Díaz-Aparicio et al. () | RID-NH | 93.4 | 100 | 100 (11/3/4) [67.9–100] | n.d. |
| 90 (10/adults/4) [54.1–99.5] | 10/adults/4) [44.2–96.5] | ||||
250Taken from the corresponding study.
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Abstract
The infection with Brucella abortus, Brucella melitensis and Brucella suis has been assessed according to the criteria of the Animal Health Law (
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