Next Article in Journal
Short- and Long-Term Evaluation of a Fixed Dose of Beauveria bassiana Strain MS-8 Diluted in Various Doses of Kaolin as a Powder Formulation Applied to Rice Grains to Control Almond Moth, Ephestia cautella Walker (Lepidoptera: Pyralidae)
Previous Article in Journal
Longitudinal Study on Extended-Spectrum Beta-Lactamase-E. coli in Sentinel Mallard Ducks in an Important Baltic Stop-Over Site for Migratory Ducks in Germany
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Microorganisms
Volume 10
Issue 10
10.3390/microorganisms10101970
microorganisms-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Spatio-Temporal Distribution of Brucellosis in European Terrestrial and Marine Wildlife Species and Its Regional Implications

by
Tariq Jamil
1,
Kadir Akar
2,
Sevil Erdenlig
3,
Jayaseelan Murugaiyan
4,
Vassilios Sandalakis
5,
Evridiki Boukouvala
6,
Anna Psaroulaki
5,
Falk Melzer
1,
Heinrich Neubauer
1 and
Gamal Wareth
1,*
1
Institute of Bacterial Infections and Zoonoses, Fredrich-Loeffler-Institut, 07743 Jena, Germany
2
NRL for Brucellosis, Pendik Veterinary Control Institute, 34890 Istanbul, Turkey
3
Faculty of Veterinary Medicine, Harran University, 63300 Şanlıurfa, Turkey
4
Department of Biological Sciences, SRM University AP, Mangalagiri 522240, India
5
Department of Clinical Microbiology and Microbial Pathogenesis, School of Medicine, University of Crete, 71110 Heraklion, Greece
6
Hellenic Agricultural Organization—DIMITRA, Veterinary Research Institute, 57001 Thessaloniki, Greece
*
Author to whom correspondence should be addressed.
Microorganisms 2022, 10(10), 1970; https://doi.org/10.3390/microorganisms10101970
Submission received: 8 September 2022 / Revised: 29 September 2022 / Accepted: 29 September 2022 / Published: 5 October 2022
(This article belongs to the Section Veterinary Microbiology)
Browse Figures
Versions Notes

Abstract

:
Brucellosis is an important bacterial zoonosis of domestic and wildlife species. This disease has a significant public health concern and is characterized by reproductive failure resulting in economic losses in the livestock industry. Among thirteen known species, B. abortus, B. melitensis, B. suis, and B. canis are human pathogens. Brucellosis has been extensively investigated in humans and domestic animals. However, the situation in wildlife is still not completely reported and studied. Therefore, a systematic literature search and screening were done to clarify the situation of brucellosis in wildlife in Europe. Sixty-five articles from a total of 13,424 reports published between 1991 and 2021 were selected, applying defined inclusion criteria. Wild boars and brown hares were the most often studied terrestrial wildlife species, whereas seals and porpoises were the most often investigated marine wildlife. Poland, Croatia, and Belgium showed the highest seroprevalences of wild boars caused by B. suis biovar 2. In marine wildlife, brucellosis was mainly caused by B. ceti and B. pinnipedialis. Most samples were from carcasses. Thus, sera could not be collected. It is worrisome that B. abortus and B. melitensis were reported from both terrestrial and marine wild animals, posing a zoonotic threat to people exposed to wild animals. Currently, there is no approved vaccine available for wild animals. The main challenges are the development of specific diagnostics and their validation for use in wildlife.

1. Introduction

Brucellosis is a major zoonotic infection of domestic animals and wildlife species worldwide [1,2]. Currently, there are 13 valid species of the genus Brucella (B.), including B. abortus, B. melitensis, B. suis, B. canis, B. ovis, B. neotomae, the “marine” B. pinnipedialis, B. ceti [3], B. inopinata [4], B. microti [5], B. papionis [6], B. vulpis [7], and the recently described B. pseudogrignonensis [8]. All these species are closely related, and the genus Brucella itself is closely related to Ochrobactrum [9], leading to the proposal to rename Ochrobactrum. This could result in 38 Brucella species. The disease has significant public health and economic impacts, particularly in middle- and low-income countries [10]. Brucellosis is mainly associated with reproduction failure in livestock and nonspecific symptoms in humans. Transmission occurs mainly via direct routes, i.e., contact with infected animals, or indirectly via contaminated fomites [11] and the consumption of contaminated unpasteurized dairy milk and products [12]. Despite the fact that brucellosis is a potential biological agent and occupational health hazard, treating the disease in farm animals is of limited practice due to the chronic nature of the disease. Resistance development in human isolates is still not well investigated [13]. A safe vaccine for use in humans is not available [14]. Human brucellosis is mainly reported in Latin America, the Middle East, Central Asia, and Mongolia [15,16], whereas it is sporadic in Europe and North America [17]. No reliable data are available for the African continent.
In the European Union (EU), livestock brucellosis caused by B. abortus, B. melitensis, and B. suis has been eradicated in farm animals in many countries [18]. In Croatia and Spain, eradication is nearly achieved, whereas in Greece, Italy, and Portugal, brucellosis remains a veterinary and public health concern with declining incidence rates [19,20]. In 2020, only six infected herds (extremely low prevalence (<0.001)) were reported in the officially brucellosis-free regions of the EU [19]. However, 0.38% (603/157,000) of bovine herds and 0.22% (349/160,000) of small ruminant herds still tested positive in brucellosis-affected regions of the EU (the lowest annual count since 2012) [19]. Overall, livestock brucellosis remained a rare event. On the other hand, canine brucellosis caused by B. canis showed an increasing trend in detectable cases, especially in Italy and the United Kingdom [19,21]. In contrast, human cases occurred due to infection transmission from wild animals and in travelers returning from disease-endemic areas after exposure. A total of 128 confirmed human cases were reported in 2020, with a decreasing trend since 2016 [19]. The notification rate was 0.03 cases per 100,000 people. In cases in which speciation could be confirmed, B. melitensis was the primary etiology in hospitalized patients, followed by B. suis [19]. Notifying livestock and human brucellosis is mandatory in at least 25 European countries, whereas a number of other countries have different/unspecified surveillance systems. Despite the efforts and money that have been spent, the infection persists in livestock and pet animals, and consequently, transmission to human occurs. On the other hand, the role of wildlife species is of great importance, but is often largely neglected. Brucellosis in wildlife has been a topic of interest for the past few decades since brucellae have been isolated in various terrestrial (e.g., wild boars, ruminants, canines, rodents, and reptiles) and marine (e.g., dolphins, whales, seals, and porpoises) animals, which possibly serve as reservoirs of brucellosis; spillover infections to domestic animals and humans [22,23]. Hence, wildlife brucellosis is not mandatory at all and data are scarce.
This review aimed to get insights into the occurrence and epidemiological situation of brucellosis in European wildlife species.

2. Materials and Methods

2.1. Literature Source and Search Strategy

An initial literature search was conducted online by using the search words “brucellosis, Brucella, wild,” on Google Scholar (Google LLC, Mountain View, CA, USA), PubMed, Web of Science, Scopus, and the Centre for Agriculture and Bioscience International (CABI) (Wallingford, UK) search bar from November to December 2021. The countries’ names comprised fifty sovereign states in Europe. These countries were grouped into Eastern, South-Eastern, Central, Northern, Southern, and Western Europe. Dependent and extra-continental territories were not included except for Greenland, which was included in the literature search criteria based on socio-political context. Duplicates, conference abstracts and proceedings, reviews, and non-English articles were excluded. Only peer-reviewed original articles published between January 1991 and December 2021 were selected and analyzed (Figure 1).

2.2. Data Acquisition and Analysis

In total, 13,424 records were scrutinized (Google Scholar (n = 13,206); PubMed (n = 85); Web of Science (n = 21); Scopus (n = 19); CABI (n = 93)) for being relevant, original, full-length, and written in English language. Four hundred and three (403) articles were selected and screened. In total, sixty-five articles were found to be qualified and were included in this review (Figure 1). Information regarding geographical areas, host species, and seroprevalence reported was extracted, analyzed, and presented in Table 1 and Table 2. To have a spatial idea of the presence of Brucella spp. and the seroprevalence in Europe, maps were generated using open-source MapChart (https://www.mapchart.net/europe.html) (Figure 2 and Figure 3).

3. Results

3.1. Data Analysis

The data represented a total of 65 wildlife brucellosis reports from 25 European countries (42 reports from 20 countries for terrestrial wildlife and 23 reports from 11 countries for marine wildlife). Countries with only terrestrial wildlife brucellosis reports are Poland (n = 5), Czech Republic (n = 5), Austria (n = 3), Switzerland (n = 3), France (n = 2), and one report each from Serbia, Bulgaria, Slovenia, Ukraine, Denmark, Latvia, Iberian Peninsula (Spain and Portugal), Belgium, and Greenland. Countries reporting brucellosis in both terrestrial and marine wildlife are Germany (four in terrestrial and two in marine), Croatia (two in terrestrial and one in marine), Norway (one in terrestrial and three in marine), Sweden (one each in terrestrial and marine), Italy (seven in terrestrial and one in marine), and the Netherlands (one in terrestrial and two in marine). Russia, Finland, Spain, Iceland and the UK showed brucellosis only in marine wildlife, consisting of two, one, two, one and eight reports, respectively. It is worth mentioning that the article of Winkelmayer et al., 2005 [24], investigated brucellosis in the European hare at the Austrian–Czech border region and contains results for both countries. Therefore, this article is included twice—in the row of Austria and also in the row of the Czech Republic in Table 1. In the same context, in reporting marine wildlife brucellosis in the 10 aforementioned countries, the article of Sonne et al., 2018 [25], includes results of two countries, i.e., Norway and Sweden. Therefore, this study was included in rows of both countries in Table 2.
Most reports detected anti-Brucella antibodies by serology, e.g., the Rose Bengal test (RBT) and enzyme-linked immunosorbent assay (ELISA), especially in living terrestrial and marine animals. In contrast, isolation was a preferred choice in tissues from dead animals. Most isolation reports confirmed brucellosis only at the genus level, and species and subspecies levels were confirmed/typed only in recent reports. B. suis biovar (bv) 2 was the main finding in wild pigs. B. abortus bv 1 and B. melitensis bv 1 were isolated from red deer and Iberian wild goats described in one report from the Iberian Peninsula [26], while B. melitensis was isolated from Alpine ibex noted in two reports from France [27,28]. In one report from Croatia, B. suis bv 3 was listed for wild boars [29], and the isolation of B. canis was described for golden jackals in one report from Serbia [30]. In marine mammals, B. pinnipedialis was the main species found in seals, and B. ceti in dolphins and whales. The highest number of reports were published in 2018 (nine), followed by 2017 (seven), 2007 (five), 2014, 2015, and 2009 (four each), and 2021 (three).

3.2. Spatio-Temporal Distribution of Brucellosis in European Terrestrial Wildlife

3.2.1. Eastern and South-Eastern Europe

Four countries, i.e., Russia, Belarus, Ukraine, and Moldova, were grouped into Eastern Europe in the study (Figure 2). Only one report from Ukraine was found describing 4.98% seroprevalence in wild boars in 2019 [31]. No evidence was found for PCR-based detection. Eleven countries, i.e., Slovenia, Croatia, Albania, Bosnia and Herzegovina, Bulgaria, Cyprus, Kosovo, Montenegro, North Macedonia, Romania, and Serbia, were grouped as South-Eastern European countries (Figure 2). Five reports described brucellosis in wild boars, golden jackals, and wild birds in this region. Wild boars showed the highest seroprevalence of 28.03% in 2003 and 23.11% in 2009 in Croatia, where B. suis bv 2 and 3 were confirmed by PCR [29,32]. In Serbia and Bulgaria, B. canis and Brucella spp. were detected in golden jackals [30] and wild birds [33], respectively, by PCR, while serology was not carried out. No evidence of anti-Brucella antibodies was found, and no amplifiable Brucella DNA was detected in wild boars of Slovenia in 2006 [34]. The prevalence and distribution of brucellosis in wild boars in Europe are shown in Figure 3.

3.2.2. Central Europe

A total of eight countries comprising Poland, Slovenia, Czech Republic, Hungary, Austria, Switzerland, Liechtenstein, and Germany were grouped as central Europe (Figure 2). No reports were found for Slovenia, Liechtenstein, and Hungary. Again, wild boars were the most tested animals in this region, contributing to more than 75% of the animals tested. The highest seroprevalences reported came from Switzerland, i.e., 35.83% in 2011 [35], and was 9.8% in two rounds and 11.05% by ELISA in two studies in 2007 [36,37]. In Poland, it was 24.44% in 2015 [38] and, in Germany, was 22.02% in 2005 [39] and 12.09% in 2006 [40]. According to the National Reference Laboratory for Animal Brucellosis in Germany, B. suis bv 2 has been isolated many times from wild boar and hares in Germany during the period under review (unpublished data). Czech wild boars showed seroprevalences of 6.25% in 1993 [41] and 8.7% in 2002 [42]. By PCR, B. suis bv 2 was confirmed in Poland [43] and Switzerland [37] (Figure 3).
The brown hare was the second most studied wild animal in the region, constituting 14% of tested animals. The highest seroprevalence (3.54%) was found in Austria in 2005 [24]. In the Czech Republic, zero prevalence was reported in two studies in 1993 [41] and 2005 [24], and 1.62% seroprevalence was reported in 2007 [44]. In Germany, seroprevalence was reported at 0% in 2003 [45]. No serological report existed for Poland; however, B. suis bv 2 was confirmed by molecular detection in 2013 [43].
Other significantly tested terrestrial wildlife species were wild rodents, e.g., mice, common voles, and shrews, which showed a seroprevalence of 17.05%, 15.25%, and 7.96%, respectively, in 2017 [46]. Brucella spp. was confirmed by PCR in Czech voles and German shrews in 2007 [47] and 2017 [46], respectively. Various reports existed for wild deer and European bison populations in Poland [43,48,49,50,51] and the Czech Republic [41] but did not report detectable antibody levels and, hence, assumed zero seroprevalences in this wildlife. In Austria, B. microti and B. vulpis were identified by molecular testing in red foxes from mandibular lymph nodes in 2009 [52] and 2016 [7], respectively.

3.2.3. Northern Europe

Norway, Sweden, Finland, Denmark, Estonia, Latvia, and Lithuania were grouped into Northern Europe (Figure 2). A total of three reports from Denmark, Latvia, and Sweden were found for wild boars, as well as one report from Norway on samples collected from reindeer. A seroprevalence of 22.51% was reported in Latvian wild boars in 2018, where B. suis bv 2 was identified by culture and PCR [53]. No antibodies were detected in Swedish and Danish wild boars in 2018 [54] and 2020 [55], respectively, and the same finding was reported for Norwegian reindeer in 1999 [56].

3.2.4. Southern Europe

Seven countries, including Portugal, Spain, Italy, San Marino, Vatican City, Malta, and Greece, were grouped as Southern Europe, out of which three had reports of brucellosis in terrestrial wildlife (Figure 2). A seroprevalence of 33% was found in Iberian (Spain and Portugal) wild boars, where B. suis bv 2 was detected in all seropositive animals by isolation and molecular identification for ten years (1999–2009) [26]. Barbary sheep, mouflons, roe deer, and fallow deer did not show seropositivity. However, chamois and red deer showed 0.78% and 0.4% seropositivity, respectively. In addition, B. melitensis bv 1 and B. abortus bv 1 were found in one Iberian wild goat and one red deer, respectively [26].
In Italy, 19.76% seroprevalence was reported in 2,267 wild boars sampled between 2001–2007 [57]. All seropositive boars yielded B. suis bv 2 in culture. A 6.1% seroprevalence was reported without confirming the etiology in 2015 [58]. B. suis bv 2 was confirmed in 2017 [59]. A seroprevalence of 13.5% was found without confirming the etiology in 2020 [60]. B. suis bv 2 was confirmed recently with a seroprevalence of 5.74% in wild boars in 2021 [61]. Di Francesco et al. (2015) reported a 9.09% seroprevalence in Marsican brown bears in 2015 [62]. No detectable Brucella DNA was reported in wild birds’ fecal samples in 2021 [63]. No anti-Brucella antibodies were found in 236 chamois and 207 roe deer sampled in Italy between 1998–2001 [64].

3.2.5. Western Europe

Nine countries, including the United Kingdom, Ireland, Iceland, the Netherlands, Belgium, Luxembourg, Monaco, Andorra, and France, were grouped into Western Europe (Figure 2). In Belgium, an apparent seroprevalence of 54.88% was reported in 1168 wild boars sampled between 2003–2007 [65]. In the Netherlands, 6.36% seroprevalence was reported in 2057 wild boars sampled between 2010–2015 [66]. Both studies confirmed B. suis bv 2 by culture and molecular typing. In France, anti-Brucella antibodies were detected in red deer, chamois, and alpine ibex [27], and B. melitensis was confirmed in Alpine ibex [28].

3.2.6. Special Territories

Greenland was grouped as a special territory. A seroprevalence of 6.25% was reported in 96 polar bears, and 0% was reported in 32 muskoxen examined by serology and without confirmation by culture examination in 2018 [67].
Microorganisms 10 01970 g002 550
Figure 2. Map showing Brucella species and biovars isolated from European wildlife.
Figure 2. Map showing Brucella species and biovars isolated from European wildlife.
Microorganisms 10 01970 g002
Microorganisms 10 01970 g003 550
Figure 3. A map showing the prevalence of brucellosis in wild boars in Europe.
Figure 3. A map showing the prevalence of brucellosis in wild boars in Europe.
Microorganisms 10 01970 g003
Table
Table 1. Brucellosis in European terrestrial wildlife.
Table 1. Brucellosis in European terrestrial wildlife.
No.CountriesRegionHostSerologyMolecular IdentificationCitation
No. TestedNo.
Positive		%Prev.
1UkraineEastern EuropeWild boars1344674.98 [31]
2CroatiaSouth-Eastern EuropeWild boars2647428.03B. suis bv 2[32]
4249823.11B. suis bv 2 and bv 3[29]
3SerbiaGolden Jackals216----B. canis[30]
4BulgariaWild birds706----Brucella spp.[33]
5SloveniaWild boars17800 [34]
6 AustriaCentral EuropeRed foxes B. microti[52]
B. vulpis[7]
Brown hare311113.54 [24]
7Czech RepublicWild boars204188.7 [42]
3226.25 [41]
Brown hare7300 [24]
1051171.62 [44]
2300 [41]
Roe deer3300 [41]
Red deer2400
Fallow deer400
Mouflon200
Common vole4----Brucella spp.[47]
8GermanyWild boars76316822.02 [39]
88510712.09 [40]
Brown hare32100 [45]
Shrews11397.96Brucella spp.[46]
Voles2954515.25
Mouse1292217.05
9PolandEuropean bison6000 [48]
12200 [49]
24000 [51]
Deer183----No isolate was achieved[50]
Wild boars235----B. suis bv 2
4407107724.44 [38]
10SwitzerlandWild boars8109011.05No isolate was achieved[36]
* 611274.42B. suis bv 2[37]
+ 121515312.59
± 4626614.28
2408635.83[35]
11DenmarkNorthern EuropeWild boars24000 [55]
12LatviaWild boars104423522.51B. suis bv 2[53]
13NorwayReindeer579200 [56]
14SwedenWild boars28600 [54]
15Iberian Peninsula
(Spain and Portugal)		Southern EuropeBarbary sheep800 [26]
Mouflon7500
Iberian wild goat108610.09B. melitensis bv 1
Chamois1410110.78
Roe deer28500
Fallow deer34200
Red deer582119≤0.4B. abortus bv 1
Wild boars4454147033B. suis bv 2
16ItalyWild boars570356.1 [58]
Wild boars226744819.76B. suis bv 2[57]
Brown bears2229.09 [62]
Wild boars389----B. suis bv 2[59]
Wild boars4345813.5 [60]
Wild Birds121 [63]
Wild boars287165.74B. suis bv 2[61]
17BelgiumWestern EuropeWild boars116864154.88B. suis bv 2[65]
18FranceRoe deer44 [27]
Red deer301
Chamois551 B. melitensis
Alpine ibex2412
Alpine ibex33988 B. melitensis[28]
19NetherlandsWild boars20571316.36B. suis bv 2[66]
20GreenlandSpecial territoryPolar bears9666.25 [67]
Greenland muskoxen3200
* First round; + Second round; ± Included in both rounds; (--) = Not performed.

3.3. Spatio-Temporal Distribution of Brucellosis in European Marine Wildlife

3.3.1. Eastern and South-Eastern Europe

On the Russian Bering Island, DNA sequences from rectal-swabs matched B. abortus, B. melitensis, and B. pinnipedialis in 3 of 78 Asian sea otters [68]. Another study reported seropositive samples in 5.63% of Caspian seals and 75% of Beluga whales, whereas seven Baikal seals and six Ringed seals were seronegative on Russian territory in 2018 [69]. In the Croatian Adriatic Sea, B. ceti ST27 was isolated and identified from one of five bottlenose dolphins in 2016 [70].

3.3.2. Central Europe

Two studies were found for Germany. In the German North Sea in 2008, Brucella isolates were recovered from common seals (47/426), harbor porpoises (2/298), and grey seals (1/34). Based on PCR-restriction fragment length polymorphism (PCR-RFLP), 47 were classified as B. pinnipedialis and the other 2 as B. ovis based on the presence of the “omp2b” gene pattern [71]. In another study, 2105 harbor seals were sampled between 1996–2014, and 359 Brucella spp. isolates were recovered and 47 isolates were confirmed as B. pinnipedialis [72]. No studies on brucellosis in marine species were reported in other central European countries.

3.3.3. Northern Europe

A total of nine seropositive animals were detected from 29 tested and apparently healthy Norwegian hooded seals. Eleven B. pinnipedialis isolates were obtained from seropositive animals and two seronegative animals. No isolates were found in ringed seals [73]. A seroprevalence of 15.57% was found in Norwegian hooded seals with one B. pinnipedialis isolate in 2013 [74]. No seropositive animals were detected in harp and hooded seals from Norway in 2018 [25]. The same study reported 2 out of 12 seropositive ringed seals in Sweden [25]. B. pinnipedialis was isolated from 3 out of 122 Baltic grey seals in Finnish samples from 2013 to 2015 [75].

3.3.4. Southern Europe

On the Spanish Mediterranean coast, two out of sixteen striped and one out of two bottlenose dolphins were reported as seropositive. Four Risso’s dolphins, one short-beaked dolphin, and one fin whale tested seronegative in 2001 but the culture was not conducted [76]. However, three B. ceti isolates were reported, two from striped dolphins and one from a bottlenose dolphin (all were seropositive by RBT) on the Catalonian Mediterranean coast in 2014 [77]. In Italy, eight B. ceti isolates were reported from one seropositive and seven seronegative striped dolphins in 2020 [78].

3.3.5. Western Europe

B. ceti ST23 was isolated and confirmed in 7 out of 112 harbor porpoises stranded on Dutch coasts between 2008 and 2011 [79]. B. pinnipedialis ST25 was isolated from 16 out of 40 seropositive harbor seals in 2018 [80]. A total of 49% (69/140) of harbor seals, 32% (10/31) of grey seals, 28% (5/18) of harbor porpoises, 0% (0/45) of Baikal seals, and one short-beaked common dolphin were reported seropositive by RBT in the North Sea in 1996, resulting in eight isolates of Brucella spp. from harbor porpoises, harbor seals, and the dolphin [81]. Atypical isolates of Brucella spp. were isolated from nine seals, eight cetaceans, and one otter [82]. Another study reported seropositivities of 9.68% (6/62) in grey seals, 8.33% (1/12) in common seals, 31.42% (11/35) in harbor porpoises, 31.03% (9/29) in common dolphins, one striped dolphin, one bottlenose dolphin, one killer whale, and one pilot whale on English and Welsh coasts without culture examination in 1997 [83]. Two B. ceti isolates were obtained from one long-finned pilot whale and one of ten Sowerby’s beaked whales found on Scottish coasts in 2015 [84]. 25.36% (87/343) harbor seals tested positive by ELISA between 1997–2012 [85]. B. ceti was also found in Risso’s dolphin and killer and minke whales in 2021 and 2017 [86,87]. A total of 1.85% harp seals, 35.04% hooded seals, 10.2% ringed seals, 11.11% fin whales, 14.28% sei whales and 7.87% mink whales were detected seropositive with isolation of Brucella spp. from a minke whale in North Atlantic Ocean [88].
Table
Table 2. Brucellosis in European marine wildlife.
Table 2. Brucellosis in European marine wildlife.
No.CountriesRegionHostSerologyMolecular IdentificationCitation
No. TestedNo.
Positive		% Prevalence
1RussiaEastern EuropeSea otters78----B. abortus, B. melitensis and B. pinnipedialis[68]
Caspian seals7145.63 [69]
Baikal seals700
Ringed seals600
Beluga whales4375
2CroatiaSouth-Eastern EuropeBottlenose dolphins4----B. ceti ST27[70]
3GermanyCentral EuropeHarbor seals2105----B. pinnipedialis[72]
Common seals426 B. pinnipedialis[71]
Harbor porpoises298
Grey seals34
Hooded seals3
Common dolphins3
White-beaked dolphin1
Ringed seal1
Pilot whale1
Minke whale1
6FinlandNorthern EuropeGrey seals122----B. pinnipedialis[75]
5NorwayHarp and hooded seals900 [25]
Hooded seals3795915.57B. pinnipedialis[74]
Hooded seals29931.03B. pinnipedialis[73]
Ringed seals2000No isolate was achieved
6SwedenRinged seals12216.67 [25]
Harp seals600
Hooded seals300
7SpainSouthern EuropeStriped dolphins22 B. ceti[77]
Bottlenose dolphin11 B. ceti
Striped dolphins16212.5 [76]
Risso’s dolphins400
Bottlenose dolphins2150
Short-beaked common dolphin100
Fin whale100
8ItalyStriped dolphins8112.5B. ceti[78]
9NetherlandsWestern EuropeWild grey seals1119.09 [80]
Harbor seals401640B. pinnipedialis
Porpoises112----B. ceti ST23[79]
10UKCommon seals14069 Brucella spp.[81]
Harbor porpoise185
Baikal seals450
Grey seals3110
Common dolphin11
Atlantic white-sided dolphin1 Brucella spp.[82]
Striped dolphin2
Hooded seal1
Grey seal1
European otter1
Bottlenose dolphin1 Brucella spp.[89]
Grey seal6269.68 [83]
Common seal1218.33
Harbor porpoise351131.42
Common dolphin29931.03
Striped dolphin4125
White-beaked dolphin400
Atlantic white-sided dolphin200
Bottlenose dolphin11
Pilot whale11
Risso’s dolphin100
Killer whale11
Blainville’s beaked whale100
Long-finned pilot whale1 B. ceti[84]
Sowerby’s beaked whale10 B. ceti
Harbor seals3438725.36Brucella spp.[85]
Risso’s dolphin1----B. ceti[86]
Killer whale1----
Common minke whale1 B. ceti[87]
11North Atlantic OceanHarp seals811151.85 [88]
Hooded seals1374835.04
Ringed seal49510.20
Bearded seal1600
Fin whale1081211.11
Sei whale49714.28
Minke whale216177.87Brucella spp.
(--) = Not performed.

4. Discussion

Wildlife interacts with humans, domestic livestock, and pet animals and, thus, can act as reservoirs and sources for the spillover of several infections and zoonotic diseases to the human interface [90]. The potential role of wildlife as a source of human zoonoses is a significant public health concern [91]. The study of brucellosis in wildlife is neglected and has only recently received increasing attention. [92,93]. The impacts of infected wildlife on public health and domestic animals are spillover and reservoir (sustainability). In addition, human activities that put persons at risk, such as hunting, dressing, meat handling, consumption, wildlife sampling, and management in intensive settings, contribute to the transmission of disease [94]. Thus, the current review provides a comprehensive, evidence-based assessment of existing literature and available data on brucellosis in terrestrial and marine wildlife in Europe.
Striking seroprevalences of brucellosis were found in wild boars (Figure 3), but also in European brown hares, red foxes, and wild deer captured in Belgium, Poland, Croatia, the Iberian Peninsula, Italy, and Latvia. B. suis bv 2 was the main etiological agent of brucellosis in wild boars; however, it was also confirmed in brown hares in Poland in 2013 [43]. Although B suis bv 1 is causing severe infection in humans, infections with B. suis bv 2 results in a very mild course in humans. Biovar 1 may also cause infection in wild boars and hares with severe consequences for hunters and farmers if it is capable of becoming enzootic in free areas [95]. B. suis bv 2 may be transmitted to domesticated animals. It has been isolated from domestic pigs in Egypt [96], but it is rarely described as a cause of human brucellosis among hunters [97]. Nevertheless, the presence of B. suis bv 2 in wild boars and hares is a potential source of spillover and spill-back infection in wildlife and domestic livestock. B. suis bv 3 was confirmed in Croatian wild boars and B. melitensis bv 1 and B. abortus bv 1 were isolated from wild ruminants in the Iberian Peninsula, which pose a direct threat to human health. Wild bison (Bison bison) and elk (Cervus canadensis) in the American Greater Yellowstone Ecosystem [98], African buffalo (Syncerus caffer) in south-east Africa [93], and Alpine ibexes (Capra ibex) in the French Alps [28] are considered self-sustaining reservoirs of B. abortus and B. melitensis. In this scenario, reducing spill-back infection from wildlife to livestock and humans would be of greater importance [99]. For this purpose, vaccination, culling, and treatment of wild animals would be interesting but is highly questionable. Hence, French authorities decided to reduce the number of strictly protected ibex dramatically. The reintroduction of endangered bison in the EU and the use of free-ranging water buffaloes for landscape conservation need special caution and care from the veterinary public health service, therefore.
B. canis has caused canine brucellosis in wild canines, e.g., jackals [30] and pet dogs [21]. It is an emerging threat in Europe in the camel class and a threat to human and animal health; of special concern are large stray dog populations. Infected dogs act as transmitters between humans and domestic and wildlife populations, as confirmed previously in Egypt [100] and Pakistan [101]. To the best of our knowledge, no reports have been found for B. ovis in European terrestrial wildlife [99], except for a report from Germany, in which two B. ovis isolates were identified from marine mammals based on the presence of the “omp2b” gene pattern [71]. In marine wildlife, brucellosis causes abortions as well [102]. Most of the Brucella isolates identified were B. pinnipedialis followed by B. ceti from harbor porpoises, dolphins, and seals, but B. abortus and B. melitensis have been isolated from Russian sea otters. The latter findings indicate a potential zoonotic threat to humans and people consuming raw seafood [68,103].
As in domestic animals, serological tests remain the mainstay in diagnosing wildlife brucellosis, e.g., the Rose Bengal Test (RBT) and enzyme-linked immunosorbent assay (ELISA). The reason might be easy handling, availability, and extensive use in domestic animals. Moreover, the antigens used in wildlife testing are smooth lipopolysaccharides (LPS), which cross-react with antibodies provoked by B. abortus, B. melitensis, and B. suis [104]. Anti-smooth Brucella LPS antibodies indicate either an active infection or exposure to Brucella in the recent past. Unfortunately, these tests must be applied without validation due to missing numbers of positive (and negative) sera for the variety of wildlife species to be tested. Competitive ELISA or fluorescent polarization assays (FPA) may be used as they do not depend upon species-specific reagents [105,106]. However, standardization and validation of these diagnostic tests would still be needed [107].
Serology has many pitfalls. Antibody titers may decrease with time and pretend lower prevalence. Furthermore, the detection of latent infection by serology is hampered. Cross-reaction with the LPS of other Gram-negative pathogens reduces sensitivity. In this scenario, the predictive values of the test would be more favorable than the intrinsic values of the test. On the other hand, canine brucellosis cannot be detected with the smooth LPS antigens used for the diagnosis of livestock brucellosis and needs antigens prepared from the rough LPS of B. canis [101]. Cytoplasmic proteins, however, could be of diagnostic importance in this scenario [108,109].
Furthermore, the quality of the serum obtained can influence the selection of the diagnostic tests applied, e.g., strong anti-complementary activity in wild boar and canine sera due to the presence of hemolysis, or other reasons due to unconducive field conditions, amateur collectors, e.g., hunters, and the time-lapse from collection to the submission of the specimens may interfere with sensitivity and specificity. Hence, establishing a definitive brucellosis diagnostic criterion in wildlife valid for all cases is challenging. Nevertheless, the isolation of brucellae remains the gold standard in wildlife too. Brucellosis has been successfully eradicated in domestic animals in many EU countries by applying a test-and-slaughter policy (after banning vaccination) [20,110]. However, this approach is not acceptable for endangered wildlife. Vaccination can be recommended for reservoir species, but no vaccine is available for brucellosis in wildlife [104]. Additionally, ensuring a representative and achievable sampling frame in the wildlife population for diagnostic/epidemiological purposes always remain a problem.

5. Conclusions

This manuscript is aimed at updating the knowledge of brucellosis in European wildlife. A large number of reports exist for wild boars, followed by brown hares, red foxes, and wild deer. There was no significant public health threat from wildlife brucellosis as most of the infections occurred due to B. suis bv 2, B. ceti, and B. pinnipedialis, which seem to not be of zoonotic importance. However, the presence of B. suis bv 3, B. abortus, B. melitensis, and B. canis pose a significant zoonotic threat. They were identified in terrestrial and marine wildlife. Thus, wildlife poses a spillover and spill-back infection threat, which needs to be controlled. Definitive diagnostic criteria, the collection of viable specimens, and establishing a representative sampling frame would be highly desirable to collect more accurate epidemiological information on the prevalence of wildlife brucellosis and its etiology. Vaccination of wild reservoir hosts could be sensible. For this, developing a safe vaccine would be fruitful. The culling of infected wildlife remains an ethical question to be answered carefully. Protection should be used while handling dead animals and awareness of foodborne infection should be raised among consumers.

Author Contributions

Conceptualization, G.W. and H.N.; methodology, T.J. and G.W.; formal analysis, T.J., E.B., A.P., F.M., G.W. and H.N.; data curation, T.J., K.A., S.E., J.M. and V.S.; writing—original draft preparation, T.J.; writing—review and editing, G.W., F.M. and H.N.; project administration, G.W.; funding acquisition, G.W. All authors have read and agreed to the published version of the manuscript.

Funding

The work belongs to the ICRAD (Bruce-GenoProt), funded by the Federal Agency for Agriculture and Food and the Federal Ministry of Food and Agriculture (BMEL) as part of the provision of funds for international research collaborations on world nutrition and other international research tasks in the field of nutrition, agriculture, and consumer health protection. Reference number: 325-06.01-2821ERA27D.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Dadar, M.; Shahali, Y.; Fakhri, Y.; Godfroid, J. The global epidemiology of Brucella infections in terrestrial wildlife: A meta-analysis. Transbound. Emerg. Dis. 2021, 68, 715–729. [Google Scholar] [CrossRef] [PubMed]
  2. Shi, J.-F.; Gong, Q.-L.; Zhao, B.; Ma, B.-Y.; Chen, Z.-Y.; Yang, Y.; Sun, Y.-H.; Wang, Q.; Leng, X.; Zong, Y.; et al. Seroprevalence of brucellosis in buffalo worldwide and associated risk factors: A systematic review and meta-analysis. Front. Vet. Sci. 2021, 8, 553. [Google Scholar] [CrossRef] [PubMed]
  3. Foster, G.; Osterman, B.; Godfroid, J.; Jacques, I.; Cloeckaert, A. Brucella ceti sp. nov. and Brucella pinnipedialis sp. nov. for Brucella strains with cetaceans and seals as their preferred hosts. Int. J. Syst. Evol. Microbiol. 2007, 57, 2688–2693. [Google Scholar] [CrossRef] [Green Version]
  4. Scholz, H.; Nockler, K.; Gollner, C. Brucella inopinata sp. nov., isolated from a breast implant infection. Int. J. Syst. Evol. Microbiol. 2010, 60, 801–808. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Scholz, H.; Hubalek, Z.; Sedlácek, I.; Vergnaud, G.; Tomaso, H.; Al Dahouk, S.; Melzer, F.; Kämpfer, P.; Neubauer, H.; Cloeckaert, A.; et al. Brucella microti sp. nov. isolated from the common vole Microtus arvalis. Int. J. Syst. Evol. Microbiol. 2008, 58, 375–382. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  6. Whatmore, A.; Davison, N.; Cloeckaert, A.; Al Dahouk, S.; Zygmunt, M.; Brew, S.; Perrett, L.; Koylass, M.; Vergnaud, G.; Quance, C.; et al. Brucella papionis sp. nov. isolated from baboons (Papio spp.). Int. J. Syst. Evol. Microbiol. 2014, 64, 4120–4128. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  7. Scholz, H.C.; Revilla-Fernandez, S.; Al Dahouk, S.; Hammerl, J.A.; Zygmunt, M.S.; Cloeckaert, A.; Koylass, M.; Whatmore, A.M.; Blom, J.; Vergnaud, G.; et al. Brucella vulpis sp. nov., isolated from mandibular lymph nodes of red foxes (Vulpes vulpes). Int. J. Syst. Evol. Microbiol. 2016, 66, 2090–2098. [Google Scholar] [CrossRef]
  8. Li, S.Y.; Huang, Y.E.; Chen, J.Y.; Lai, C.H.; Mao, Y.C.; Huang, Y.T.; Liu, P.Y. Genomics of Ochrobactrum pseudogrignonense (newly named Brucella pseudogrignonensis) reveals a new blaOXA subgroup. Microb. Genom. 2021, 7, 626. [Google Scholar] [CrossRef]
  9. Ryan, M.P.; Pembroke, J.T. The Genus Ochrobactrum as major opportunistic pathogens. Microorganisms 2020, 8, 1797. [Google Scholar] [CrossRef]
  10. Akar, K.; Tatar, F.; Schmoock, G.; Wareth, G.; Neubauer, H.; Erganįs, O. Tracking the diversity and Mediterranean lineage of Brucella melitensis isolates from different animal species in Turkey using MLVA-16 genotyping. Ger. J. Vet. Res. 2022, 2, 25–30. [Google Scholar] [CrossRef]
  11. Khurana, S.K.; Sehrawat, A.; Tiwari, R.; Prasad, M.; Gulati, B.; Shabbir, M.Z.; Chhabra, R.; Karthik, K.; Patel, S.K.; Pathak, M. Bovine brucellosis–a comprehensive review. Vet. Q. 2021, 41, 61–88. [Google Scholar] [CrossRef] [PubMed]
  12. Abdul Ghani, S.R.; Azit, N.A.; Mohd Fadzil, S.; Pang, N.T.P.; Rahim, S.S.S.A.; Hassan, M.R.; Jeffree, M.S. Risk factors and outbreak management of brucellosis in Asia: A meta-analysis. Infektološki Glas. 2021, 41, 41–50. [Google Scholar] [CrossRef]
  13. Wareth, G.; Dadar, M.; Ali, H.; Hamdy, M.E.R.; Al-Talhy, A.M.; Elkharsawi, A.R.; Tawab, A.; Neubauer, H. The perspective of antibiotic therapeutic challenges of brucellosis in the Middle East and North African (MENA) countries: Current situation and therapeutic management. Transbound. Emerg. Dis. 2022, 69, e1253–e1268. [Google Scholar] [CrossRef] [PubMed]
  14. Elrashedy, A.; Gaafer, M.; Mousa, W.; Nayel, M.; Salama, A.; Zaghawa, A.; Elsify, A.; Dawood, A.S. Immune response and recent advances in diagnosis and control of brucellosis. Ger. J. Vet. Res. 2022, 2, 10–24. [Google Scholar] [CrossRef]
  15. Zolzaya, B.; Selenge, T.; Narangarav, T.; Gantsetseg, D.; Erdenechimeg, D.; Zinsstag, J.; Schelling, E. Representative seroprevalences of human and livestock brucellosis in two Mongolian provinces. EcoHealth 2014, 11, 356–371. [Google Scholar] [CrossRef] [Green Version]
  16. Avila-Granados, L.M.; Garcia-Gonzalez, D.G.; Zambrano-Varon, J.L.; Arenas-Gamboa, A.M. Brucellosis in Colombia: Current status and challenges in the control of an endemic disease. Front. Vet. Sci. 2019, 6, 321. [Google Scholar] [CrossRef]
  17. Bagheri Nejad, R.; Krecek, R.C.; Khalaf, O.H.; Hailat, N.; Arenas-Gamboa, A.M. Brucellosis in the Middle East: Current situation and a pathway forward. PLoS Negl. Trop. Dis. 2020, 14, e0008071. [Google Scholar] [CrossRef]
  18. Godfroid, J.; Käsbohrer, A. Brucellosis in the European Union and Norway at the turn of the twenty-first century. Vet. Microbiol. 2002, 90, 135–145. [Google Scholar] [CrossRef]
  19. European Food Safety Authority; European Centre for Disease Prevention and Control. The European Union One Health 2020 Zoonoses Report. EFSA J. 2021, 19, e06971. [Google Scholar]
  20. Wareth, G.; Abdeen, A.; Ali, H.; Bardenstein, S.; Blasco, J.M.; Cardoso, R.; Corrêa De Sá, M.I.; Cvetnić, Ž.; de Massis, F.; El-Diasty, M.; et al. Brucellosis in the Mediterranean Countries: History, Prevalence, Distribution, Current Situation and Attempts at Surveillance and Control; World Organization for Animal Health (OIE): Paris, France, 2019. [Google Scholar]
  21. Buhmann, G.; Paul, F.; Herbst, W.; Melzer, F.; Wolf, G.; Hartmann, K.; Fischer, A. Canine brucellosis: Insights into the epidemiologic situation in Europe. Front. Vet. Sci. 2019, 6, 151. [Google Scholar] [CrossRef] [Green Version]
  22. Eltahir, Y.; Al-Farsi, A.; Al-Marzooqi, W.; Al-Toobi, A.; Gaafar, O.M.; Jay, M.; Corde, Y.; Bose, S.; Al-Hamrashdi, A.; Al-Kharousi, K.; et al. Investigation on Brucella infection in farm animals in Saham, Sultanate of Oman with reference to human brucellosis outbreak. BMC Vet. Res. 2019, 15, 378. [Google Scholar] [CrossRef]
  23. Mick, V.; Le Carrou, G.; Corde, Y.; Game, Y.; Jay, M.; Garin-Bastuji, B. Brucella melitensis in France: Persistence in wildlife and probable spillover from Alpine Ibex to domestic animals. PLoS ONE 2014, 9, e94168. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  24. Winkelmayer, R.; Vodnansky, M.; Paulsen, P.; Gansterer, A.; Treml, F. Explorative study on the seroprevalence of Brucella-, Francisella-and Leptospira antibodies in the European hare (Lepus europaeus Pallas) of the Austrian-Czech border region. Wien. Tierarztl. Mon. 2005, 92, 131. [Google Scholar]
  25. Sonne, C.; Andersen-Ranberg, E.; Rajala, E.L.; Agerholm, J.S.; Bonefeld-Jørgensen, E.; Desforges, J.-P.; Eulaers, I.; Jenssen, B.M.; Koch, A.; Rosing-Asvid, A. Seroprevalence for Brucella spp. in Baltic ringed seals (Phoca hispida) and East Greenland harp (Pagophilus groenlandicus) and hooded (Cystophora cristata) seals. Vet. Immunol. Immunopathol. 2018, 198, 14–18. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Muñoz, P.M.; Boadella, M.; Arnal, M.; de Miguel, M.J.; Revilla, M.; Martínez, D.; Vicente, J.; Acevedo, P.; Oleaga, Á.; Ruiz-Fons, F.; et al. Spatial distribution and risk factors of brucellosis in Iberian wild ungulates. BMC Infect. Dis. 2010, 10, 46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Garin-Bastuji, B.; Hars, J.; Drapeau, A.; Cherfa, M.-A.; Game, Y.; Le Horgne, J.-M.; Rautureau, S.; Maucci, E.; Pasquier, J.-J.; Jay, M. Reemergence of Brucella melitensis infection in wildlife, France. Emerg. Infect. Dis. 2014, 20, 1570. [Google Scholar] [CrossRef] [PubMed]
  28. Lambert, S.; Gilot-Fromont, E.; Freycon, P.; Thébault, A.; Game, Y.; Toïgo, C.; Petit, E.; Barthe, M.-N.; Reynaud, G.; Jaÿ, M. High shedding potential and significant individual heterogeneity in naturally-infected Alpine ibex (Capra ibex) with Brucella melitensis. Front. Microbiol. 2018, 9, 1065. [Google Scholar] [CrossRef] [PubMed]
  29. Cvetnic, Z.; Spicic, S.; Toncic, J.; Majnaric, D.; Benic, M.; Albert, D.; Thiebaud, M.; Garin-Bastuji, B. Brucella suis infection in domestic pigs and wild boar in Croatia. Rev. Sci. Tech. 2009, 28, 1057–1067. [Google Scholar] [CrossRef]
  30. Cirović, D.; Chochlakis, D.; Tomanović, S.; Sukara, R.; Penezić, A.; Tselentis, Y.; Psaroulaki, A. Presence of Leishmania and Brucella species in the golden jackal Canis aureus in Serbia. Biomed. Res. Int. 2014, 2014, 728516. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Pyskun, A.; Polishchuk, O.; Piankivska, I.; Pyskun, O.; Moroz, O.; Pishchanskyi, O.; Aliekseieva, H. Presence of antibodies against Brucella spp. in serum samples from wild boars in Ukraine. Porc. Res. 2019, 9, 26–33. [Google Scholar]
  32. Cvetnic, Z.; Mitak, M.; Ocepek, M.; Lojkic, M.; Terzic, S.; Jemersic, L.; Humski, A.; Habrun, B.; Sostaric, B.; Brstilo, M.; et al. Wild boars (Sus scrofa) as reservoirs of Brucella suis biovar 2 in Croatia. Acta Vet. Hung. 2003, 51, 465–473. [Google Scholar] [CrossRef]
  33. Najdenski, H.; Dimova, T.; Zaharieva, M.M.; Nikolov, B.; Petrova-Dinkova, G.; Dalakchieva, S.; Popov, K.; Hristova-Nikolova, I.; Zehtindjiev, P.; Peev, S.; et al. Migratory birds along the Mediterranean—Black Sea Flyway as carriers of zoonotic pathogens. Can. J. Microbiol. 2018, 64, 915–924. [Google Scholar] [CrossRef] [Green Version]
  34. Vengust, G.; Valencak, Z.; Bidovec, A. A serological survey of selected pathogens in wild boar in Slovenia. J. Vet. Med. B 2006, 53, 24–27. [Google Scholar] [CrossRef]
  35. Wu, N.; Abril, C.; Hinicacute, V.; Brodard, I.; Thür, B.; Fattebert, J.; Hüssy, D.; Ryser-Degiorgis, M.-P. Free-ranging wild boar: A disease threat to domestic pigs in Switzerland? J. Wildl. Dis. 2011, 47, 868–879, 812. [Google Scholar] [CrossRef] [PubMed]
  36. Köppel, C.; Knopf, L.; Ryser, M.P.; Miserez, R.; Thür, B.; Stärk, K.D.C. Serosurveillance for selected infectious disease agents in wild boars (Sus scrofa) and outdoor pigs in Switzerland. Eur. J. Wildl. Res. 2007, 53, 212–220. [Google Scholar] [CrossRef]
  37. Leuenberger, R.; Boujon, P.; Thür, B.; Miserez, R.; Garin-Bastuji, B.; Rüfenacht, J.; Stärk, K.D.C. Prevalence of classical swine fever, Aujeszky’s disease and brucellosis in a population of wild boar in Switzerland. Vet. Rec. 2007, 160, 362–368. [Google Scholar] [CrossRef]
  38. Szulowski, K.; Iwaniak, W.; Zlotnicka, J.; Da, M.S.; Weiner, M.; Lipowski, A.; Jablonski, A. Survey of the anti-Brucella antibody status determined by ELISA testing in wild boars in Poland. Med. Weter 2015, 71, 215–218. [Google Scholar]
  39. Al Dahouk, S.; Nöckler, K.; Tomaso, H.; Splettstoesser, W.D.; Jungersen, G.; Riber, U.; Petry, T.; Hoffmann, D.; Scholz, H.C.; Hensel, A.; et al. Seroprevalence of brucellosis, tularemia, and yersiniosis in wild boars (Sus scrofa) from north-eastern Germany. J. Vet. Med. B Infect. Dis. Vet. Public Health 2005, 52, 444–455. [Google Scholar] [CrossRef] [PubMed]
  40. Melzer, F.; Lohse, R.; Nieper, H.; Liebert, M.; Sachse, K. A serological study on brucellosis in wild boars in Germany. Eur. J. Wildl. Res. 2006, 53, 153. [Google Scholar] [CrossRef]
  41. Hubálek, Z.; Juticová, Z.; Svobodová, Š.; Halouzka, J. A Serologic survey for some bacterial and viral zoonoses in game animals in the Czech Republic. J. Wildl. Dis. 1993, 29, 604–607. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  42. Hubálek, Z.; Treml, F.; Juricova, Z.; Hunady, M.; Halouzka, J.; Janik, V.; Bill, D. Serological survey of the wild boar (Sus scrofa) for tularaemia and brucellosis in South Moravia, Czech Republic. Vet. Med. Praha 2002, 47, 60–66. [Google Scholar] [CrossRef] [Green Version]
  43. Szulowski, K.; Iwaniak, W.; Weiner, M.; Zlotnicka, J. Characteristics of Brucella strains isolated from animals in Poland. Pol. J. Vet. Sci. 2013, 16, 757–758. [Google Scholar] [CrossRef] [PubMed]
  44. Treml, F.; Pikula, J.; Bandouchova, H.; Horakova, J. European brown hare as a potential source of zoonotic agents. Vet. Med. Praha 2007, 52, 451. [Google Scholar] [CrossRef] [Green Version]
  45. Frandölich, K.; Wisser, J.; Schmüser, H.; Fehlberg, U.; Neubauer, H.; Grunow, R.; Nikolaou, K.; Priemer, J.; Thiede, S.; Streich, W.J.; et al. Epizootiologic and ecologic investigations of European Brown Hares (Lepus europaeus) in selected populations from Schleswig-Holstein, Germany. J. Wildl. Dis. 2003, 39, 751–761. [Google Scholar] [CrossRef] [PubMed]
  46. Hammerl, J.A.; Ulrich, R.G.; Imholt, C.; Scholz, H.C.; Jacob, J.; Kratzmann, N.; Nöckler, K.; Al Dahouk, S. Molecular survey on brucellosis in rodents and shrews—natural reservoirs of novel Brucella species in Germany? Transbound. Emerg. Dis. 2017, 64, 663–671. [Google Scholar] [CrossRef] [PubMed]
  47. Hubálek, Z.; Scholz, H.; Sedláček, I.; Melzer, F.; Sanogo, Y.; Nesvadbová, J. Brucellosis of the common vole (Microtus arvalis). Vector-Borne Zoonotic Dis. 2007, 7, 679–688. [Google Scholar] [CrossRef]
  48. Kita, J.; Anusz, K. Serologic survey for bovine pathogens in free-ranging European bison from Poland. J. Wildl. Dis. 1991, 27, 16–20. [Google Scholar] [CrossRef] [Green Version]
  49. Salwa, A.; Anusz, K.; Arent, Z.; Paprocka, G.; Kita, J. Seroprevalence of selected viral and bacterial pathogens in free-ranging European bison. Pol. J. Vet. Sci. 2007, 10, 19–23. [Google Scholar]
  50. Weiner, M.; Iwaniak, W.; Szulowski, K. Identification of Brucella DNA in lymph tissue from deer (Cervus elaphus) and wild boars (Sus scrofa) by the use of BCSP31 PCR and AMOS-PCR. Bull. Vet. Inst. Pulawy 2009, 53, 609–612. [Google Scholar]
  51. Krzysiak, M.K.; Jabłoński, A.; Iwaniak, W.; Krajewska, M.; Kęsik-Maliszewska, J.; Larska, M. Seroprevalence and risk factors for selected respiratory and reproductive tract pathogen exposure in European bison (Bison bonasus) in Poland. Vet. Microbiol. 2018, 215, 57–65. [Google Scholar] [CrossRef]
  52. Scholz, H.C.; Hofer, E.; Vergnaud, G.; Le Fleche, P.; Whatmore, A.M.; Al Dahouk, S.; Pfeffer, M.; Krüger, M.; Cloeckaert, A.; Tomaso, H. Isolation of Brucella microti from mandibular lymph nodes of red foxes, Vulpes vulpes, in lower Austria. Vector Borne Zoonotic Dis. 2009, 9, 153–156. [Google Scholar] [CrossRef]
  53. Grantina-Ievina, L.; Avsejenko, J.; Cvetkova, S.; Krastina, D.; Streikisa, M.; Steingolde, Z.; Vevere, I.; Rodze, I. Seroprevalence of Brucella suis in eastern Latvian wild boars (Sus scrofa). Acta Vet. Scand. 2018, 60, 19. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  54. Malmsten, A.; Magnusson, U.; Ruiz-Fons, F.; González-Barrio, D.; Dalin, A.-M. A Serologic survey of pathogens in wild boar (Sus scrofa) in Sweden. J. Wildl. Dis. 2018, 54, 229–237, 229. [Google Scholar] [CrossRef]
  55. Petersen, H.H.; Takeuchi-Storm, N.; Enemark, H.L.; Nielsen, S.T.; Larsen, G.; Chriél, M. Surveillance of important bacterial and parasitic infections in Danish wild boars (Sus scrofa). Acta Vet. Scand. 2020, 62, 41. [Google Scholar] [CrossRef] [PubMed]
  56. Åsbakk, K.; Stuen, S.; Hansen, H.; Forbes, L. A serological survey for brucellosis in reindeer in Finnmark county, northern Norway. Rangifer 1999, 19, 19–24. [Google Scholar] [CrossRef] [Green Version]
  57. Bergagna, S.; Zoppi, S.; Ferroglio, E.; Gobetto, M.; Dondo, A.; Giannatale, E.D.; Gennero, M.S.; Grattarola, C. Epidemiologic survey for Brucella suis biovar 2 in a wild boar (Sus scrofa) population in northwest Italy. J. Wildl. Dis. 2009, 45, 1178–1181. [Google Scholar] [CrossRef]
  58. Pilo, C.; Addis, G.; Deidda, M.; Tedde, M.T.; Liciardi, M. A serosurvey for brucellosis in wild boar (Sus scrofa) in Sardinia, Italy. J. Wildl. Dis. 2015, 51, 885–888. [Google Scholar] [CrossRef]
  59. Di Sabatino, D.; Garofolo, G.; Di Provvido, A.; Zilli, K.; Foschi, G.; Di Giannatale, E.; Ciuffetelli, M.; De Massis, F. Brucella suis biovar 2 Multi Locus Sequence Type ST16 in wild boars (Sus scrofa) from Abruzzi region, Italy. Introduction from Central-Eastern Europe? Infect. Genet. Evol. 2017, 55, 63–67. [Google Scholar] [CrossRef]
  60. Montagnaro, S.; D’Ambrosi, F.; Petruccelli, A.; Ferrara, G.; D’Alessio, N.; Iovane, V.; Veneziano, V.; Fioretti, A.; Pagnini, U. A serological survey of brucellosis in Eurasian wild boar (Sus scrofa) in Campania Region, Italy. J. Wildl. Dis. 2020, 56, 424–428. [Google Scholar] [CrossRef]
  61. Cilia, G.; Fratini, F.; Turchi, B.; Angelini, M.; Cerri, D.; Bertelloni, F. Genital Brucella suis biovar 2 infection of wild boar (Sus scrofa) hunted in Tuscany (Italy). Microorganisms 2021, 9, 582. [Google Scholar] [CrossRef] [PubMed]
  62. Di Francesco, C.E.; Gentile, L.; Di Pirro, V.; Ladiana, L.; Tagliabue, S.; Marsilio, F. Serologic evidence for selected infectious diseases in Marsican brown bears (Ursus arctos marsicanus) in Italy (2004–09). J. Wildl. Dis. 2015, 51, 209–213. [Google Scholar] [CrossRef] [PubMed]
  63. Ebani, V.V.; Guardone, L.; Bertelloni, F.; Perrucci, S.; Poli, A.; Mancianti, F. Survey on the Presence of bacterial and parasitic zoonotic agents in the feces of wild birds. Vet. Sci. 2021, 8, 171. [Google Scholar] [CrossRef] [PubMed]
  64. Gaffuri, A.; Giacometti, M.; Tranquillo, V.M.; Magnino, S.; Cordioli, P.; Lanfranchi, P. Serosurvey of roe deer, chamois and domestic sheep in the central Italian Alps. J. Wildl. Dis. 2006, 42, 685–690. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Grégoire, F.; Mousset, B.; Hanrez, D.; Michaux, C.; Walravens, K.; Linden, A. A serological and bacteriological survey of brucellosis in wild boar (Sus scrofa) in Belgium. BMC Vet. Res. 2012, 8, 80. [Google Scholar] [CrossRef] [Green Version]
  66. van Tulden, P.; Gonzales, J.L.; Kroese, M.; Engelsma, M.; de Zwart, F.; Szot, D.; Bisselink, Y.; van Setten, M.; Koene, M.; Willemsen, P. Monitoring results of wild boar (Sus scrofa) in The Netherlands: Analyses of serological results and the first identification of Brucella suis biovar 2. Infect. Ecol. Epidemiol. 2020, 10, 1794668. [Google Scholar] [CrossRef]
  67. Sonne, C.; Andersen-Ranberg, E.; Rajala, E.L.; Agerholm, J.S.; Bonefeld-Jørgensen, E.; Desforges, J.-P.; Eulaers, I.; Gustavson, K.; Jenssen, B.M.; Koch, A. Prevalence of antibodies against Brucella spp. in West Greenland polar bears (Ursus maritimus) and East Greenland muskoxen (Ovibos moschatus). Polar Biol. 2018, 41, 1671–1680. [Google Scholar] [CrossRef]
  68. Burgess, T.L.; Johnson, C.K.; Burdin, A.; Gill, V.A.; Doroff, A.M.; Tuomi, P.; Smith, W.A.; Goldstein, T. Brucella infection in Asian Sea Otters (Enhydra lutris lutris) on Bering Island, Russia. J. Wildl. Dis. 2017, 53, 864–868. [Google Scholar] [CrossRef]
  69. Ohishi, K.; Abe, E.; Amano, M.; Miyazaki, N.; Boltunov, A.; Katsumata, E.; Maruyama, T. Detection of serum antibodies to Brucella in Russian aquatic mammals. J. Vet. Med. Sci. 2018, 80, 1696–1701. [Google Scholar] [CrossRef] [Green Version]
  70. Cvetnić, Ž.; Duvnjak, S.; Đuras, M.; Gomerčić, T.; Reil, I.; Zdelar-Tuk, M.; Špičić, S. Evidence of Brucella strain ST27 in bottlenose dolphin (Tursiops truncatus) in Europe. Vet. Microbiol. 2016, 196, 93–97. [Google Scholar] [CrossRef]
  71. Prenger-Berninghoff, E.; Siebert, U.; Stede, M.; König, A.; Weiss, R.; Baljer, G. Incidence of Brucella species in marine mammals of the German North Sea. Dis. Aquat. Org. 2008, 81, 65–71. [Google Scholar] [CrossRef]
  72. Siebert, U.; Rademaker, M.; Ulrich, S.A.; Wohlsein, P.; Ronnenberg, K.; Prenger-Berninghoff, E. Bacterial microbiota in Harbor Seals (Phoca vitulina) from the North Sea of Schleswig-Holstein, Germany, around the time of Morbillivirus and Influenza epidemics. J. Wildl. Dis. 2017, 53, 201–214. [Google Scholar] [CrossRef] [PubMed]
  73. Tryland, M.; Sørensen, K.K.; Godfroid, J. Prevalence of Brucella pinnipediae in healthy hooded seals (Cystophora cristata) from the North Atlantic Ocean and ringed seals (Phoca hispida) from Svalbard. Vet. Microbiol. 2005, 105, 103–111. [Google Scholar] [CrossRef] [PubMed]
  74. Nymo, I.H.; Tryland, M.; Frie, A.K.; Haug, T.; Foster, G.; Rødven, R.; Godfroid, J. Age-dependent prevalence of anti-Brucella antibodies in hooded seals Cystophora cristata. Dis. Aquat. Org. 2013, 106, 187–196. [Google Scholar] [CrossRef] [Green Version]
  75. Hirvelä-Koski, V.; Nylund, M.; Skrzypczak, T.; Heikkinen, P.; Kauhala, K.; Jay, M.; Isomursu, M. Isolation of Brucella pinnipedialis from grey seals (Halichoerus grypus) in the Baltic Sea. J. Wildl. Dis. 2017, 53, 850–853. [Google Scholar] [CrossRef] [PubMed]
  76. Van Bressem, M.-F.; Van Waerebeek, K.; Raga, J.A.; Godfroid, J.; Brew, S.D.; MacMillan, A.P. Serological evidence of Brucella species infection in odontocetes from the south Pacific and the Mediterranean. Vet. Rec. 2001, 148, 657–661. [Google Scholar] [CrossRef]
  77. Isidoro-Ayza, M.; Ruiz-Villalobos, N.; Pérez, L.; Guzmán-Verri, C.; Muñoz, P.M.; Alegre, F.; Barberán, M.; Chacón-Díaz, C.; Chaves-Olarte, E.; González-Barrientos, R.; et al. Brucella ceti infection in dolphins from the Western Mediterranean Sea. BMC Vet. Res. 2014, 10, 206. [Google Scholar] [CrossRef] [PubMed]
  78. Garofolo, G.; Petrella, A.; Lucifora, G.; Di Francesco, G.; Di Guardo, G.; Pautasso, A.; Iulini, B.; Varello, K.; Giorda, F.; Goria, M.; et al. Occurrence of Brucella ceti in striped dolphins from Italian Seas. PLoS ONE 2020, 15, e0240178. [Google Scholar] [CrossRef] [PubMed]
  79. Maio, E.; Begeman, L.; Bisselink, Y.; van Tulden, P.; Wiersma, L.; Hiemstra, S.; Ruuls, R.; Gröne, A.; Roest, H.-I.-J.; Willemsen, P.; et al. Identification and typing of Brucella spp. in stranded harbour porpoises (Phocoena phocoena) on the Dutch coast. Vet. Microbiol. 2014, 173, 118–124. [Google Scholar] [CrossRef] [PubMed]
  80. Kroese, M.V.; Beckers, L.; Bisselink, Y.J.W.M.; Brasseur, S.; van Tulden, P.W.; Koene, M.G.J.; Roest, H.I.J.; Ruuls, R.C.; Backer, J.A.; IJzer, J.; et al. Brucella pinnipedialis in Grey Seals (Halichoerus grypus) and Harbor Seals (Phoca vitulina) in The Netherlands. J. Wildl. Dis. 2018, 54, 439–449. [Google Scholar] [CrossRef] [Green Version]
  81. Ross, H.; Jahans, K.; MacMillan, A.; Reid, R.; Thompson, P.; Foster, G. Brucella species infection in North Sea seal and cetacean populations. Vet. Rec. 1996, 138, 647–648. [Google Scholar] [CrossRef]
  82. Foster, G.; Jahans, K.; Reid, R.; Ross, H. Isolation of Brucella species from cetaceans, seals and an otter. Vet. Rec. 1996, 138, 583–586. [Google Scholar] [CrossRef]
  83. Jepson, P.D.; Brew, S.; MacMillan, A.P.; Baker, J.R.; Barnett, J.; Kirkwood, J.K.; Kuiken, T.; Robinson, I.R.; Simpson, V.R. Antibodies to Brucella in marine mammals around the coast of England and Wales. Vet. Rec. 1997, 141, 513–515. [Google Scholar] [CrossRef] [PubMed]
  84. Foster, G.; Whatmore, A.M.; Dagleish, M.P.; Baily, J.L.; Deaville, R.; Davison, N.J.; Koylass, M.S.; Perrett, L.L.; Stubberfield, E.J.; Reid, R.J.; et al. Isolation of Brucella ceti from a long-finned Pilot Whale (Globicephala melas) and a Sowerby’s Beaked Whale (Mesoploden bidens). J. Wildl. Dis. 2015, 51, 868–871. [Google Scholar] [CrossRef] [PubMed]
  85. Kershaw, J.L.; Stubberfield, E.J.; Foster, G.; Brownlow, A.; Hall, A.J.; Perrett, L.L. Exposure of harbour seals Phoca vitulina to Brucella in declining populations across Scotland. Dis. Aquat. Org. 2017, 126, 13–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  86. Davison, N.J.; Dagleish, M.P.; Dale, E.-J.; Ten Doeschate, M.; Muchowski, J.; Perrett, L.L.; Rocchi, M.; Whatmore, A.M.; Brownlow, A.C. First confirmed reports of the isolation of Brucella ceti from a Risso’s dolphin Grampus griseus and a killer whale Orcinus orca. Dis. Aquat. Org. 2021, 145, 191–195. [Google Scholar] [CrossRef] [PubMed]
  87. Davison, N.J.; Perrett, L.L.; Dawson, C.; Dagleish, M.P.; Haskins, G.; Muchowski, J.; Whatmore, A.M. Brucella ceti infection in a common minke whale (Balaenoptera acutorostrata) with associated pathology. J. Wildl. Dis. 2017, 53, 572–576. [Google Scholar] [CrossRef] [PubMed]
  88. Tryland, M.; Kleivane, L.; Alfredsson, A.; Kjeld, M.; Arnason, A.; Stuen, S.; Godfroid, J. Evidence of Brucella infection in marine mammals in the North Atlantic Ocean. Vet. Rec. 1999, 144, 588–592. [Google Scholar] [CrossRef] [PubMed]
  89. Dawson, C.; Perrett, L.; Young, E.; Davison, N.; Monies, R. Isolation of Brucella species from a bottlenosed dolphin (Tursiops truncatus). Vet. Rec. 2006, 158, 831. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  90. Kruse, H.; Kirkemo, A.M.; Handeland, K. Wildlife as source of zoonotic infections. Emerg. Infect. Dis. 2004, 10, 2067–2072. [Google Scholar] [CrossRef] [PubMed]
  91. González-Barrio, D. Zoonoses and Wildlife: One Health Approach. Animals 2022, 12, 480. [Google Scholar] [CrossRef] [PubMed]
  92. Lambert, S.; Thébault, A.; Rossi, S.; Marchand, P.; Petit, E.; Toïgo, C.; Gilot-Fromont, E. Targeted strategies for the management of wildlife diseases: The case of brucellosis in Alpine ibex. Vet. Res. 2021, 52, 116. [Google Scholar] [CrossRef] [PubMed]
  93. Simpson, G.; Thompson, P.N.; Saegerman, C.; Marcotty, T.; Letesson, J.J.; de Bolle, X.; Godfroid, J. Brucellosis in wildlife in Africa: A systematic review and meta-analysis. Sci. Rep. 2021, 11, 5960. [Google Scholar] [CrossRef]
  94. Kneipp, C.C.; Sawford, K.; Wingett, K.; Malik, R.; Stevenson, M.A.; Mor, S.M.; Wiethoelter, A.K. Brucella suis Seroprevalence and associated risk factors in dogs in Eastern Australia, 2016 to 2019. Front. Vet. Sci. 2021, 8, 727641. [Google Scholar] [CrossRef]
  95. Giurgiutiu, D.; Banis, C.; Hunt, E.; Mincer, J.; Nicolardi, C.; Weltman, A.; Stanek, D.; Matthews, S.; Siegenthaler, C.; Blackmore, C.; et al. Brucella suis infection associated with feral swine hunting—Three states, 2007–2008. Morb. Mortal. Wkly. Rep. 2009, 58, 618–621. [Google Scholar]
  96. Elmonir, W.; Abdel-Hamid, N.H.; Hamdy, M.E.R.; Beleta, E.I.M.; El-Diasty, M.; Melzer, F.; Wareth, G.; Neubauer, H. Isolation and molecular confirmation of Brucella suis biovar 2 from slaughtered pigs: An unanticipated biovar from domestic pigs in Egypt. BMC Vet. Res. 2022, 18, 224. [Google Scholar] [CrossRef] [PubMed]
  97. Mailles, A.; Ogielska, M.; Kemiche, F.; Garin-Bastuji, B.; Brieu, N.; Burnusus, Z.; Creuwels, A.; Danjean, M.P.; Guiet, P.; Nasser, V.; et al. Brucella suis biovar 2 infection in humans in France: Emerging infection or better recognition? Epidemiol. Infect. 2017, 145, 2711–2716. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. Schumaker, B.A. Detection and Transmission Dynamics of Brucella Abortus in the Greater Yellowstone Area; University of California: Davis, CA, USA, 2010. [Google Scholar]
  99. Godfroid, J.; Garin-Bastuji, B.; Saegerman, C.; Blasco, J. Brucellosis in terrestrial wildlife. Rev. Sci. Tech. 2013, 32, 27–42. [Google Scholar] [CrossRef] [PubMed]
  100. Wareth, G.; Melzer, F.; El-Diasty, M.; Schmoock, G.; Elbauomy, E.; Abdel-Hamid, N.; Sayour, A.; Neubauer, H. Isolation of Brucella abortus from a dog and a cat confirms their biological role in re-emergence and dissemination of bovine brucellosis on dairy farms. Transbound. Emerg. Dis. 2017, 64, e27–e30. [Google Scholar] [CrossRef]
  101. Jamil, T.; Melzer, F.; Khan, I.; Iqbal, M.; Saqib, M.; Hammad Hussain, M.; Schwarz, S.; Neubauer, H. Serological and molecular investigation of Brucella species in dogs in Pakistan. Pathogens 2019, 8, 294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  102. Miller, W.G.; Adams, L.G.; Ficht, T.A.; Cheville, N.F.; Payeur, J.P.; Harley, D.R.; House, C.; Ridgway, S.H. Brucella-induced abortions and infection in bottlenose dolphins (Tursiops truncatus). J. Zoo Wildl. Med. 1999, 30, 100–110. [Google Scholar] [PubMed]
  103. Nymo, I.H.; Tryland, M.; Godfroid, J. A review of Brucella infection in marine mammals, with special emphasis on Brucella pinnipedialis in the hooded seal (Cystophora cristata). Vet. Res. 2011, 42, 93. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  104. Godfroid, J.; Nielsen, K.; Saegerman, C. Diagnosis of brucellosis in livestock and wildlife. Croat. Med. J. 2010, 51, 296–305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  105. Dong, S.-B.; Xiao, D.; Liu, J.-Y.; Bi, H.-M.; Zheng, Z.-R.; Wang, L.-D.; Yang, X.-W.; Tian, G.-Z.; Zhao, H.-Y.; Piao, D.-R.; et al. Fluorescence polarization assay improves the rapid detection of human brucellosis in China. Infect. Dis. Poverty 2021, 10, 46. [Google Scholar] [CrossRef] [PubMed]
  106. McGiven, J.A.; Tucker, J.D.; Perrett, L.L.; Stack, J.A.; Brew, S.D.; MacMillan, A.P. Validation of FPA and cELISA for the detection of antibodies to Brucella abortus in cattle sera and comparison to SAT, CFT, and iELISA. J. Immunol. Methods 2003, 278, 171–178. [Google Scholar] [CrossRef]
  107. Godfroid, J. Brucellosis in livestock and wildlife: Zoonotic diseases without pandemic potential in need of innovative one health approaches. Arch. Public Health 2017, 75, 34. [Google Scholar] [CrossRef] [PubMed]
  108. Wareth, G.; Pletz, M.W.; Neubauer, H.; Murugaiyan, J. Proteomics of Brucella: Technologies and their applications for basic research and medical microbiology. Microorganisms 2020, 8, 766. [Google Scholar] [CrossRef]
  109. Di Bonaventura, G.; Angeletti, S.; Ianni, A.; Petitti, T.; Gherardi, G. Microbiological laboratory diagnosis of human brucellosis: An overview. Pathogens 2021, 10, 1623. [Google Scholar] [CrossRef]
  110. Henaux, V.; JaŸ, M.; Siebeke, C.; Calavas, D.; Ponsart, C. Review of bovine brucellosis surveillance in Europe in 2015. Rev. Sci. Tech. 2018, 37, 805–821. [Google Scholar] [CrossRef]
Microorganisms 10 01970 g001 550
Figure 1. Flow diagram of the literature source and search strategy.
Figure 1. Flow diagram of the literature source and search strategy.
Microorganisms 10 01970 g001
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Jamil, T.; Akar, K.; Erdenlig, S.; Murugaiyan, J.; Sandalakis, V.; Boukouvala, E.; Psaroulaki, A.; Melzer, F.; Neubauer, H.; Wareth, G. Spatio-Temporal Distribution of Brucellosis in European Terrestrial and Marine Wildlife Species and Its Regional Implications. Microorganisms 2022, 10, 1970. https://doi.org/10.3390/microorganisms10101970

AMA Style

Jamil T, Akar K, Erdenlig S, Murugaiyan J, Sandalakis V, Boukouvala E, Psaroulaki A, Melzer F, Neubauer H, Wareth G. Spatio-Temporal Distribution of Brucellosis in European Terrestrial and Marine Wildlife Species and Its Regional Implications. Microorganisms. 2022; 10(10):1970. https://doi.org/10.3390/microorganisms10101970

Chicago/Turabian Style

Jamil, Tariq, Kadir Akar, Sevil Erdenlig, Jayaseelan Murugaiyan, Vassilios Sandalakis, Evridiki Boukouvala, Anna Psaroulaki, Falk Melzer, Heinrich Neubauer, and Gamal Wareth. 2022. "Spatio-Temporal Distribution of Brucellosis in European Terrestrial and Marine Wildlife Species and Its Regional Implications" Microorganisms 10, no. 10: 1970. https://doi.org/10.3390/microorganisms10101970

APA Style

Jamil, T., Akar, K., Erdenlig, S., Murugaiyan, J., Sandalakis, V., Boukouvala, E., Psaroulaki, A., Melzer, F., Neubauer, H., & Wareth, G. (2022). Spatio-Temporal Distribution of Brucellosis in European Terrestrial and Marine Wildlife Species and Its Regional Implications. Microorganisms, 10(10), 1970. https://doi.org/10.3390/microorganisms10101970

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop