Next Article in Journal
Effects of Sources and Forms of Vitamin K3 on Its Storage Stability in Vitamin Premixes or Vitamin Trace Mineral Premixes
Next Article in Special Issue
Antimicrobial Resistance and Genetic Lineages of Staphylococcus aureus from Wild Rodents: First Report of mecC-Positive Methicillin-Resistant S. aureus (MRSA) in Portugal
Previous Article in Journal
Assessment of Response to Moderate and High Dose Supplementation of Astaxanthin in Laying Hens
Previous Article in Special Issue
Molecular Typing of Pathogenic Leptospira Species Isolated from Wild Mammal Reservoirs in Sardinia
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Animals
Volume 11
Issue 4
10.3390/ani11041139
animals-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:
Article

Presence and Characterization of Zoonotic Bacterial Pathogens in Wild Boar Hunting Dogs (Canis lupus familiaris) in Tuscany (Italy)

by
Giovanni Cilia
1,
Filippo Fratini
1,
Barbara Turchi
1,*,
Valentina Virginia Ebani
1,
Luca Turini
1,
Stefano Bilei
2,
Teresa Bossù
2,
Maria Laura De Marchis
2,
Domenico Cerri
1 and
Fabrizio Bertelloni
1
1
Department of Veterinary Sciences, University of Pisa, Viale delle Piagge 2, 56124 Pisa, Italy
2
Istituto Zooprofilattico Sperimentale del Lazio e della Toscana M. Aleandri, 00178 Rome, Italy
*
Author to whom correspondence should be addressed.
Animals 2021, 11(4), 1139; https://doi.org/10.3390/ani11041139
Submission received: 29 January 2021 / Revised: 8 April 2021 / Accepted: 14 April 2021 / Published: 16 April 2021
(This article belongs to the Special Issue Zoonoses: Wild and Domestic Animal Interaction)
Versions Notes

Abstract

:

Simple Summary

Wildlife is an important reservoir for several zoonotic pathogens, and wild animals can contribute to disease transmission to humans or domestic animals via direct or indirect contact. In the One Health approach, the role of wildlife and the wild environment in the maintenance and spread of zoonoses has great importance. Domestic dogs (Canis lupus familiaris) employed in wild boar hunts may be a good indicator to evaluate this. This investigation reports the presence of Leptospira spp. and antimicrobial-resistant Salmonella spp. and Yersinia enterocolitica in wild boar hunting dogs in the Tuscany region (Italy). The results obtained suggest that wildlife may be the source of pathogens detected in dogs; indeed, all pathogens may be carried by wild animals, in particular wild boar. This investigation highlights the possible risk for dogs connected to work activities. Furthermore, considering that humans could be exposed to the same pathogens during outdoor activities, constant monitoring seems necessary to evaluate the transmission risk.

Abstract

Domestic dogs (Canis lupus familiaris) used for wild boar (Sus scrofa) hunting may represent incidental hosts for several zoonotic pathogens. This investigation aimed to evaluate the presence of anti-Leptospira antibodies and the occurrence, antimicrobial resistance, and virulence of Salmonella spp., Yersinia enterocolitica, and Listeria monocytogenes in sera and rectal swabs collected from 42 domestic hunting dogs in the Tuscany region (Italy). Regarding Leptospira, 31 out of 42 serum samples (73.8%) were positive and serogroup Pomona was the most detected (71.4%) at titers between 1:100 and 1:400. Four Salmonella isolates (9.52%) were obtained, all belonging to serotype Infantis; two of them showed antimicrobial resistance to streptomycin, while pipB and sopE presence was assessed in all but one isolate. Concerning Yersinia enterocolitica, seven isolates (16.7%) were obtained, six belonging to biotype 1 and one to biotype 4. Resistance to amoxicillin–clavulanic acid, cephalothin, and ampicillin was detected. Biotype 4 presented three of the virulence genes searched (ystA, ystB, inv), while isolates of biotype 1 showed only one gene. No Listeria monocytogenes was isolated from dog rectal swabs. The results suggest that hunting dogs are exposed to different bacterial zoonotic agents, potentially linked to their work activity, and highlight the possible health risks for humans.

1. Introduction

The coexistence between domestic dogs (Canis lupus familiaris) and humans has lasted for about 40,000 years. By this relationship, dogs have evolved thanks to several domestication events [1,2]. During these multiple events, dogs did not modify their complex body language, and humans used their sophisticated forms of social cognition and communication to train them [1,2]. The training led to dividing dogs into working-class categories and employing them in jobs that help humans in several areas, including hunting.
Traditionally in Italy, domestic hunting dogs have been employed by hunters to track wildlife, as well as wild boar (Sus scrofa), during the activity known as a “drive hunt”, in in which several dogs are used [3].
Due to contact with some wild animals species and the sharing of environmental areas, domestic hunting dogs can be affected by a large variety of pathogens [4,5,6,7,8,9,10,11]. Moreover, wild boar hunting dogs during game activities or at the end of slaughtering are usually fed raw wild boar meat and/or slaughter waste, such as liver, lung, spleen, heart, kidney, and sometimes testicles; this practice can increase the risk of disease transmission [9].
Wildlife acts as a reservoir for pathogens that contribute to maintaining and/or disseminating important infectious diseases [12,13,14,15,16,17]. Regarding Tuscany (Italy), among bacterial zoonoses, different etiological agents have been detected in wild animals, in particular Leptospira, Salmonella, Yersinia, and Listeria [18,19,20,21,22,23,24,25,26,27].
Leptospirosis is a neglected and re-emerging zoonosis caused by Gram-negative bacteria belonging to the Leptospira genus [28]. Leptospira infection, which is widespread worldwide, is maintained by a large variety of domestic and wild animal species, which act as asymptomatic maintenance hosts [29,30]. The localization of renal reservoirs contributes to maintaining the infection in the environment through constant shedding of Leptospira in urine. In this way, accidental contact with Leptospira-infected urine causes an incidental infection that could lead to clinical disease, as reported in dogs [30,31].
Salmonellosis is the second most diffused zoonosis in Europe [32]. It is caused by a Gram-negative rod-shaped, flagellated, and facultative anaerobic bacteria belonging to the Salmonella enterica species, which includes more than 2600 serovars [33]. Salmonella enterica strains can cause illnesses in both humans and animals [33,34].
Yersinia enterocolitica is the etiological agent of yersiniosis, another important zoonosis [32]. Bacteria belonging to this species can survive in the environment for a long time. Yersinia enterocolitica has been divided into more than 70 serotypes, based on differences in the structure of the somatic antigen, and into 6 biotypes based on its biochemical characteristics [35].
Listeriosis is a zoonosis caused by Listeria monocytogenes, a Gram-positive and facultative intracellular bacterium [36]. Listeria infection occurs as an epidemic or sporadically, and more than 90% of human cases worldwide have generally been caused by strains belonging to serovars 1/2a, 1/2b, and 4b of 13 possible serovars [37].
All of these foodborne zoonoses are spread worldwide and diffused in several environments, such as soil, water, feces, and meat [38]. Moreover, one of the main forms of Salmonella spp. and Yersinia enterocolitica transmission is the consumption of domestic and wild swine meat [39,40].
This investigation was aimed at evaluating infection by Leptospira spp., Salmonella spp., Yersinia enterocolitica, and Listeria monocytogenes in domestic hunting dogs employed for wild boar hunting. Leptospira prevalence was analyzed using serological assay, while Salmonella spp., Yersinia enterocolitica, and Listeria monocytogenes were investigated through isolation methods. The presence of virulence genes and antimicrobial resistance of the obtained isolates was evaluated.

2. Materials and Methods

2.1. Sampling

In January 2020, at the end of the hunting season that started in November 2019, we collected radial vein blood samples and rectal swabs from domestic hunting dogs (Canis lupus familiaris) employed in wild boar hunting in the provinces of Pisa and Lucca (Tuscany, Italy). All specimens were sampled from hunting dogs belonging to hunters who collaborated with the authors during sample collection for previous research [18,22,23,41,42].
Samples were collected after authorization by the Organismo Preposto al Benessere degli Animali (OPBA) of the University of Pisa with protocol no. 21/2020. During the sampling phase, which took place where the dogs were housed by their owners, information about vaccination programs and vaccines used for leptospirosis was recorded. In addition, the occurrence of previous gastrointestinal disorders was taken into consideration, and subjects with recent or previous intestinal diseases were not included in the study.
Blood samples were centrifuged at 10,000 rpm for 10 min to obtain serum. The sera were kept at −20 °C until use for the serological test. Rectal swabs were processed right away to obtain isolates.

2.2. Microscopic Agglutination Test (MAT)

To provide evidence of the vaccine’s effectiveness and to investigate the possible native response against Leptospira serogroups not covered by vaccines, a serological analysis was carried out. In particular, to detect Leptospira antibodies, sera were tested by the microscopic agglutination test (MAT) [43]. A titer of 1:100 was considered positive. The following live Leptospira antigens were used for the MAT: Leptospira interrogans serovar Icterohaemorrhagiae (serogroup Icterohaemorrhagiae, strain RGA), L. interrogans serovar Canicola (serogroup Canicola, strain Alarik), L. interrogans serovar Pomona (serogroup Pomona, strain Mezzano), L. kirschneri serovar Grippotyphosa (serogroup Grippotyphosa, strain Moskva V), L. borgpetersenii serovar Tarassovi (serogroup Tarassovi, strain Mitis Johnson), L. interrogans serovar Bratislava (serogroup Australis, strain Riccio 2), L. interrogans serovar Hardjo (serogroup Sejroe, serovar Hardjoprajitno), and L. borgpetersenii serovar Ballum (serogroup Ballum, strain Mus 127).

2.3. Bacterial Isolation and Characterization

From rectal swabs, Salmonella spp., Yersinia enterocolitica, and Listeria monocytogenes isolation was performed as previously described [22,44]. Salmonella spp. isolates were serotyped by slide agglutination test with commercial antisera (Statens Serum Institut, Copenhagen, Denmark), according to the Kauffmann–White scheme. Yersinia enterocolitica isolates were characterized based on biochemical tests to distinguish the biotype [45].

2.4. Antimicrobial Resistance

The antimicrobial susceptibility of all obtained isolates was evaluated using the disc diffusion test on Mueller Hinton Agar (Oxoid, Ltd., Basingstoke, UK) [46]. The following antibiotics (Oxoid) were employed: amoxicillin–clavulanic acid (AMC; 30 µg), ampicillin (AMP; 10 µg), aztreonam (ATM; 30 µg), cephalothin (KF; 30 µg), cefotaxime (CTX; 30 µg), cefoxitin (FOX; 30 µg), chloramphenicol (C; 30 µg), enrofloxacin (ENR; 5 µg), gentamycin (CN; 10 µg), imipenem (IPM; 10 µg), nalidixic acid (NA; 2 µg), nitrofurantoin (F; 300 µg), streptomycin (S; 10 µg), sulfamethoxazole–trimethoprim (STX; 25 µg), and tetracycline (TE; 30 µg). CLSI (Clinical and Laboratory Standards Institute) zone diameter interpretive criteria were used [47].

2.5. Virulence Genes

DNA was extracted from overnight bacterial cultures of each isolate using Quick-DNA Plus Kits (Zymo Research, Irvine, CA, USA) following the manufacturer’s guidelines.
In Salmonella spp. isolates, the presence of mgtC, pipB, sopB, spvR, spvC, gipA, sodCI, and sopE genes, linked to virulence, was evaluated using primers and protocols as previously reported [48,49,50,51,52].
In Yersinia enterocolitica isolates, the presence of the following virulence genes was evaluated using previously published primers and protocols: ail, virF, ystA, ystB, and inv [53,54,55].
Each polymerase chain reaction (PCR) was carried out in a total volume of 50 μL, including 25 μL of EconoTaq PLUS 2× Master Mix (Lucigen Corporation, Middleton, WI, USA), 0.5 μM of each primer, 3 μL of DNA, and distilled water to reach the final volume. An automated thermal cycler Gene-Amp PCR System 2700 (PerkinElmer, Norwalk, CT, USA) was employed to perform the amplifications, consisting of initial denaturation at 95 °C for 10 min, 35 cycles of denaturation at 95 °C for 1 min, annealing for 2 min, extension at 72 °C for 1 min, and a final extension at 72 °C for 10 min. Annealing temperatures were set based on the specific primers employed. PCR products were analyzed by electrophoresis on 1.5% agarose gel at 100 V for 45 min. PCR Sizer 100 bp DNA Ladder (Norgen Biotek, Thorold, ON, Canada) was used as a DNA marker.

2.6. Statistical Analysis

Data were reported on Excel (Microsoft, Albuquerque, NM, USA) and analyzed with the chi-square (X2) test. The statistical test was used to evaluate the infection rate of each pathogen in relation to sex (male or female) and hunting province (Pisa or Lucca). The statistical significance threshold was set at p ≤ 0.05 [56], and a 95% confidence interval was calculated.

3. Results

Blood and rectal swabs were collected from 42 hunting dogs, 30 from a hunting company in Pisa and 12 from Lucca; in particular, samples were collected from dogs belonging to 10 different owners (Table 1). All dogs were housed in a single box, except during work activities or training. The box appeared clean and in good condition; owners noted that rats and mice were not present, but they did not have a regular rat-control program. All animals were fed only with commercial feed. All dogs (22 males, 20 females) were healthy and did not show clinical signs of leptospirosis or gastrointestinal disorder at sampling time. The vaccines given to the investigated dogs were Eurican L-multi® (including serovars Canicola, Icterohaemorrhagiae, and Grippotyphosa), Nobivac L-4® (including serovars Canicola, Icterohaemorrhagiae, Bratislava, and Grippotyphosa), and Canigen DHPPi/L® (including serovars Canicola and Icterohaemorrhagiae), as reported in Table 1.

3.1. Leptospira spp.

Overall, all sera but one were positive by MAT (Table 1). Some of the positive reactions against Icterohaemorrhagiae, Canicola, Australis, and Grippotyphosa serogroups, 31 out of 42 serum samples (73.8%; 95% confidence interval (CI): 60.5–87.1%), probably linked to vaccination, were positive to serological analysis (shown in bold in Table 1).
Pomona was the most-recorded serogroup (71.4%; 95% CI: 57.7–85.0%), serologically detected in most of the positive sera (30/31). Among them, 8 (26.7%; 95% CI: 10.8–42.5%) showed a titer of 1:400, 17 (56.7%; 95% CI: 38.9–74.4%) a titer of 1:200, and 5 (16.7%; 95% CI: 3.3–30.0%) a titer of 1:100. One serum was also positive to serogroup Australis at a titer of 1:100. Finally, two sera (6.7%; 95% CI: 0.0–15.6%) were positive to serogroup Grippotyphosa, one at a titer of 1:100 and one at 1:200.
No statistical differences (p > 0.05) were reported for serological positivity considering hunting company, province, and dog sex.

3.2. Salmonella spp.

Four Salmonella strains (9.52%; 95% CI: 0.6–18.3%) were isolated from hunting dog rectal swabs. All isolates belonged to Salmonella enterica subspecies enterica serotype Infantis. Only two of them showed resistance to streptomycin (50.0%). All but one isolate harbored some virulence genes. Two isolates scored positive only to the pipB gene, and one to pipB and sopE (Table 2).
No statistical differences (p > 0.05) were reported for the number of obtained Salmonella spp. isolates considering hunting company, province, and dog sex.

3.3. Yersinia enterocolitica

In total, seven strains of Yersinia enterocolitica (16.7%; 95% CI: 5.4–27.9%) were isolated, six of which were biochemically confirmed as biotype 1, and one as biotype 4 (Table 3).
All strains were resistant to at least two antimicrobials. In particularly, all strains (100%) were resistant to ampicillin and cephalothin. Moreover, ampicillin resistance was reported in six isolates (85.7%), cefoxitin resistance in two isolates (28.6%), and streptomycin, nalidixic acid, and chloramphenicol resistance in one isolate (14.3%).
All but one isolate presented at least one virulence gene; only one isolate, biotype 4, scored positive for more than one gene. The most detected genes were ystA, ystB, and ail in two out of the seven isolates (28.6%), followed by inv and virF, detected in one isolate (14.3%).
No statistical differences (p > 0.05) were reported for the number of obtained Yersinia enterocolitica isolates considering hunting company, province, and dog sex.

3.4. Listeria monocytogenes

No Listeria monocytogenes isolates were obtained from hunting dog rectal swabs.

4. Discussion

This investigation reports infection by Leptospira spp., Salmonella ser. Infantis, and Yersinia enterocolitica in a sample of hunting dogs employed in wild boar hunting in two provinces of Tuscany. To the best of the authors’ knowledge, no other investigations have been performed to research these zoonotic bacterial pathogens in Italian hunting dogs.
Concerning Leptospira serological results, all dogs but one were positive, at least for one serogroup. Some positive reactions could be related to immune response induced by vaccine administration, as previously reported [57,58,59]. Indeed, in all serum samples, titers of 1:100 and 1:200 were reported in vaccinated dogs for serovars included in the vaccine. In detail, antibodies for serogroup Icterohaemorrhagiae, Canicola, Grippotyphosa, and Australis were found in dogs regularly vaccinated with Nobivac L-4® (MSD Animal Health); for serogroup Icterohaemorrhagiae, Canicola, and Grippotyphosa in dogs vaccinated with Eurican L-multi® (Boehringer Ingelheim Animal Health); and for serogroup Icterohaemorrhagiae and Canicola in dogs vaccinated with Canigen DHPPi/L® (Virbac S.r.l.). Serogroup Pomona was found in 71.4% of sampled hunting dogs, at titers from 1:100 to 1:400. The serological titers suggested chronic or very recent infection, probably mediated by vaccine status.
Pomona is a serogroup strictly connected to pigs. Indeed, Leptospira, which belongs to this serogroup, has been widely detected in the Tuscany region in domestic and wild swine [19,60,61], particularly in wild boar sampled in the same area and the same period [23]. Pomona was recently isolated in Tuscany from a crested porcupine [21]; even if the role of this animal as maintenance or accidental host is not still clear, this suggests a link to animals other than wild boar. Due to the rare Pomona infection reported in dogs, this serovar is not included in dog vaccines [57], even though infection causes severe disease with lethargy, fever, inappetence, diffuse hemorrhage, and renal and liver failure [62,63]. In recent years in Italy, Pomona incidence in dogs has increased [64,65,66,67], probably due to contact with wild boar, which play a role in spreading the disease as a reservoir.
Two serum samples showed a positive reaction to Grippotyphosa live antigen, at titers of 1:100 and 1:200. In Europe, this is an emerging serogroup in dogs [65,67,68,69,70] and is included in the dog leptospirosis vaccine [57]. In two serum samples, Leptospira co-infection was reported: one was positive to Grippotyphosa and Pomona at titers of 1:200 and 1:100, respectively, and the other to Pomona and Australis at titers of 1:200 and 1:100, respectively. It cannot be excluded that the co-infection could be related to an unspecific reaction between the serum antibody and Leptospira antigens [28]. Grippotyphosa and Australis infection could be related to direct or indirect contact with small rodents, lagomorphs, and hedgehogs, which act as reservoirs for these serovars and are particularly abundant among the wildlife population in this area [65]. Finally, although serology has high diagnostic value for leptospirosis and MAT is considered the gold standard test, with high sensitivity and specificity, in order to better understand the real risk for hunting dogs, it will be necessary to perform isolation or molecular investigation on urine and blood samples in the future.
Regarding rectal swabs, 9.52% were positive to Salmonella spp. Although no studies have been performed on hunting dogs, the prevalence found in this investigation is low, as previously reported in studies on domestic dogs [5,71,72]. All of them belonged to Salmonella enterica subspecies enterica serotype Infantis. This serotype is usually associated with swine [73,74] and has been isolated in free-ranging wild boar in the same investigated area [22] and in the north of Italy [75]. However, other sources of infection exist other than wild swine; indeed, S. ser Infantis was also detected in wild carnivores, ruminants, and birds in Italy [76]. Although no statistical differences emerged regarding Salmonella positivity, all infected dogs were from the same owner. For this reason, we cannot exclude that infection was not linked to work activities, but to the environment where the animals live or the management of these dogs. Only two Salmonella isolates were resistant to antimicrobials, and particularly only to streptomycin. Streptomycin resistance is well documented in Salmonella, particularly in strains isolated from dogs [77,78] and swine [76,79,80]. Concerning virulence genes, pipB and sopE were the only two detected, found only in wild boar sampled in Tuscany [22]. Both genes were found in the S395 isolates, while only pipB was found in in S397 and S398. The sopE gene is transmitted by phage and is involved in the invasion of intestinal epithelial cells. It also stimulates the inflammatory response in the host [44]. The pipB gene is associated with Salmonella pathogenicity island 5 (SPI-5) and plays a role in the survival of Salmonella in the intracellular environment [81].
During this investigation, Yersinia enterocolitica was isolated from 16.7% of rectal swabs from hunting dogs. As for Salmonella, no studies have been carried out on Yersinia enterocolitica infection in hunting dogs. A very close prevalence was previously detected in domestic dogs [82,83,84] and in wild boar hunted in the same Italian region [22]. The most diffuse is biotype 1, while only one isolate belongs to biotype 4. These data are in accordance with the prevalence of yersiniosis and biotypes distribution in wild boar [22,85,86]. As for Salmonella, other sources of infection cannot be definitively excluded; although Y. enterocolitica has been isolated from resident and migratory wild fauna in Italy [87,88], no recent data on the investigated area are available to allow a robust hypothesis. Among isolates belonging to biotype 1, only one virulence gene (within ail, ystA, ystB, and virF) was detected, while in biotype 4 the ystA, ystB, and inv genes were detected. As previously reported in swine [85,89] and wild boar [22], high resistance to amoxicillin–clavulanic acid and cephalothin was also detected in isolates from investigated dogs, but this result could be linked to intrinsic resistance, as previously reported [90]. The rates of resistance to nalidixic acid, chloramphenicol, and streptomycin found in Yersinia enterocolitica isolates from dogs seem to be similar to the antimicrobial resistance associated with wild boar strains [22].
The high prevalence of Leptospira interrogans serogroup Pomona detected serologically seems to be connected to the infection circulating in free-ranging wild boar in the Tuscany region [19,23,65]. The same association could be hypothesized for Salmonella spp. and Yersinia enterocolitica, comparing the results of this investigation with the infection of wild boar sampled in the same investigated area, although other sources of infection cannot be excluded. All dogs were healthy at the time of sampling, and the owners did not report previous disease linked to the investigated pathogens; hunting dogs could potentially become asymptomatic reservoirs and shedders of these bacteria, contributing to their diffusion and representing a possible danger for the owners. This investigation highlights some of the risks hunting dogs are exposed to, presumably linked to their work activities, and the potential hazard for humans sharing the same environment for work or recreational activities.

5. Conclusions

In conclusion, the results of this investigation suggest that hunting dogs could be exposed to different pathogens, potentially during their work activities. Indeed, some of these pathogens are often associated with wildlife, in particular wild boar. To provide strong evidence on the sources of these pathogens, the number of hunting companies and dogs should be increased and a deep investigation into wildlife and the wild environment should be carried out to obtain an important number of isolates to be compared with phenotypic and molecular methods.

Author Contributions

Conceptualization, G.C., F.F. and F.B.; investigation, G.C., B.T., L.T., S.B., T.B., M.L.D.M. and F.B.; data curation, G.C., F.F., B.T., V.V.E., L.T., S.B., T.B., M.L.D.M., D.C. and F.B.; writing—original draft preparation, G.C., B.T. and F.B.; writing—review and editing, G.C., F.F., V.V.E., L.T., S.B., T.B., M.L.D.M., D.C. and F.B.; supervision, F.F. and D.C.; funding acquisition, F.F. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the University of Pisa, grant number PRA_2018_56.

Institutional Review Board Statement

The study was conducted according to the guidelines of the Declaration of Helsinki, and approved by the Ethics Committee (Organismo Preposto al Benessere degli Animali—OPBA) of University of Pisa (protocol code 21/2020).

Data Availability Statement

The data presented in this study are available within the article.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Wayne, R.K.; Vonholdt, B.M. Evolutionary genomics of dog domestication. Mamm. Genome 2012, 23, 3–18. [Google Scholar] [CrossRef] [PubMed]
  2. Larson, G.; Karlsson, E.K.; Perri, A.; Webster, M.T.; Ho, S.Y.W.; Peters, J.; Stahl, P.W.; Piper, P.J.; Lingaas, F.; Fredholm, M.; et al. Rethinking dog domestication by integrating genetics, archeology, and biogeography. Proc. Natl. Acad. Sci. USA 2012, 109, 8878–8883. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  3. Scillitani, L.; Monaco, A.; Toso, S. Do intensive drive hunts affect wild boar (Sus scrofa) spatial behaviour in Italy? Some evidences and management implications. Eur. J. Wildl. Res. 2010, 56, 307–318. [Google Scholar] [CrossRef]
  4. Fiorello, C.V.; Straub, M.H.; Schwartz, L.M.; Liu, J.; Campbell, A.; Kownacki, A.K.; Foley, J.E. Multiple-host pathogens in domestic hunting dogs in Nicaragua’s Bosawás Biosphere Reserve. Acta Trop. 2017, 167, 183–190. [Google Scholar] [CrossRef]
  5. Lowden, P.; Wallis, C.; Gee, N.; Hilton, A. Investigating the prevalence of Salmonella in dogs within the Midlands region of the United Kingdom. BMC Vet. Res. 2015, 11. [Google Scholar] [CrossRef] [Green Version]
  6. Lim, S.; Irwin, P.J.; Lee, S.; Oh, M.; Ahn, K.; Myung, B.; Shin, S. Comparison of selected canine vector-borne diseases between urban animal shelter and rural hunting dogs in Korea. Parasites Vectors 2010, 3, 1–5. [Google Scholar] [CrossRef] [Green Version]
  7. Piantedosi, D.; Neola, B.; D’Alessio, N.; Di Prisco, F.; Santoro, M.; Pacifico, L.; Sgroi, G.; Auletta, L.; Buch, J.; Chandrashekar, R.; et al. Seroprevalence and risk factors associated with Ehrlichia canis, Anaplasma spp., Borrelia burgdorferi sensu lato, and D. immitis in hunting dogs from southern Italy. Parasitol. Res. 2017, 116, 2651–2660. [Google Scholar] [CrossRef]
  8. Cay, A.B.; Letellier, C. Isolation of Aujeszky’s disease virus from two hunting dogs in Belgium after hunting wild boars. Vlaams Diergeneeskd. Tijdschr. 2009, 78, 194–195. [Google Scholar]
  9. Cano-Terriza, D.; Martínez, R.; Moreno, A.; Pérez-Marín, J.E.; Jiménez-Ruiz, S.; Paniagua, J.; Borge, C.; García-Bocanegra, I. Survey of Aujeszky’s Disease Virus in Hunting Dogs from Spain. Ecohealth 2019, 16, 351–355. [Google Scholar] [CrossRef]
  10. Ortuño, A.; Scorza, V.; Castellà, J.; Lappin, M. Prevalence of intestinal parasites in shelter and hunting dogs in Catalonia, Northeastern Spain. Vet. J. 2014, 199, 465–467. [Google Scholar] [CrossRef]
  11. Gómez-Morales, M.A.; Selmi, M.; Ludovisi, A.; Amati, M.; Fiorentino, E.; Breviglieri, L.; Poglayen, G.; Pozio, E. Hunting dogs as sentinel animals for monitoring infections with Trichinella spp. in wildlife. Parasites Vectors 2016, 9, 1–11. [Google Scholar] [CrossRef] [Green Version]
  12. Meng, X.J.; Lindsay, D.S.; Sriranganathan, N. Wild boars as sources for infectious diseases in livestock and humans. Philos. Trans. R. Soc. B Biol. Sci. 2009, 364, 2697–2707. [Google Scholar] [CrossRef] [Green Version]
  13. Pacini, M.I.; Forzan, M.; Cilia, G.; Bertelloni, F.; Fratini, F.; Mazzei, M. Detection and Characterization of Viral Pathogens Associated with Reproductive Failure in Wild Boars in Central Italy. Animals 2021, 11, 304. [Google Scholar] [CrossRef]
  14. Pacini, M.I.; Forzan, M.; Cilia, G.; Bernardini, L.; Marzoli, F.; Pedonese, F.; Bandecchi, P.; Fratini, F.; Mazzei, M. Detection of Pseudorabies Virus in Wild Boar Foetus. Animals 2020, 10, 366. [Google Scholar] [CrossRef] [Green Version]
  15. Mazzei, M.; Nardini, R.; Verin, R.; Forzan, M.; Poli, A.; Tolari, F. Serologic and molecular survey for hepatitis E virus in wild boar (Sus scrofa) in Central Italy. New Microbes New Infect. 2015, 7, 41–47. [Google Scholar] [CrossRef]
  16. Cilia, G.; Bertelloni, F. Leptospira Infection in Wild Boar (Sus scrofa). In Leptospira Infection in Wild Animals; Fratini, F., Bertelloni, F., Cilia, G., Eds.; Nova Science Publisher: Hauppauge, NY, USA, 2020; pp. 53–77. [Google Scholar]
  17. Fratini, F.; Bertelloni, F.; Cilia, G. Leptospira Infection in Wild Animals; Nova Science Publisher: Hauppauge, NY, USA, 2020; ISBN 978-1-53618-222-4. [Google Scholar]
  18. Cilia, G.; Bertelloni, F.; Piredda, I.; Ponti, M.N.; Turchi, B.; Cantinle, C.; Parisi, F.; Pinzauti, P.; Armani, A.; Palmas, B.; et al. Presence of pathogenic Leptospira spp. in the reproductive system and fetuses of wild boars (Sus scrofa) in Italy. PLoS Negl. Trop. Dis. 2020, 14, e0008982. [Google Scholar] [CrossRef]
  19. Bertelloni, F.; Mazzei, M.; Cilia, G.; Forzan, M.; Felicioli, A.; Sagona, S.; Bandecchi, P.; Turchi, B.; Cerri, D.; Fratini, F. Serological Survey on Bacterial and Viral Pathogens in Wild Boars Hunted in Tuscany. Ecohealth 2020, 17, 85–93. [Google Scholar] [CrossRef]
  20. Coppola, F.; Cilia, G.; Bertelloni, F.; Casini, L.; D’Addio, E.; Fratini, F.; Cerri, D.; Felicioli, A. Crested porcupine (Hystrix cristata L.): A new potential host for pathogenic Leptospira among semi-fossorial mammals. Comp. Immunol. Microbiol. Infect. Dis. 2020, 70, 101472. [Google Scholar] [CrossRef]
  21. Cilia, G.; Bertelloni, F.; Coppola, F.; Turchi, B.; Biliotti, C.; Poli, A.; Parisi, F.; Felicioli, A.; Cerri, D.; Fratini, F. Isolation of Leptospira serovar Pomona from a crested porcupine (Hystrix cristata, L., 1758). Vet. Med. Sci. 2020, vms3.308. [Google Scholar] [CrossRef]
  22. Cilia, G.; Turchi, B.; Fratini, F.; Bilei, S.; Bossù, T.; De Marchis, M.L.; Cerri, D.; Pacini, M.I.; Bertelloni, F. Prevalence, Virulence and Antimicrobial Susceptibility of Salmonella spp., Yersinia enterocolitica and Listeria monocytogenes in European Wild Boar (Sus scrofa) Hunted in Tuscany (Central Italy). Pathogens 2021, 10, 93. [Google Scholar] [CrossRef]
  23. Cilia, G.; Bertelloni, F.; Angelini, M.; Cerri, D.; Fratini, F. Leptospira Survey in Wild Boar (Sus scrofa) Hunted in Tuscany, Central Italy. Pathogens 2020, 9, 377. [Google Scholar] [CrossRef]
  24. Magistrali, C.F.; Cucco, L.; Pezzotti, G.; Farneti, S.; Cambiotti, V.; Catania, S.; Prati, P.; Fabbi, M.; Lollai, S.; Mangili, P.; et al. Characterisation of Yersinia pseudotuberculosis isolated from animals with yersiniosis during 1996–2013 indicates the presence of pathogenic and Far Eastern strains in Italy. Vet. Microbiol. 2015, 180, 161–166. [Google Scholar] [CrossRef] [PubMed]
  25. Martini, A.; Marconi, P.; Ponzetta, M.P.; Giorgetti, A.; Viliani, M. Sanitary monitoring models for wild ungulate stock farms in Tuscany. Vet. Res. Commun. 2005, 29, 77–82. [Google Scholar] [CrossRef] [PubMed]
  26. Andreoli, E.; Radaelli, E.; Bertoletti, I.; Bianchi, A.; Scanziani, E.; Tagliabue, S.; Mattiello, S. Leptospira spp. infection in wild ruminants: A survey in Central Italian Alps. Vet. Ital. 2014, 50, 285–291. [Google Scholar] [CrossRef]
  27. Fratini, F.; Turchi, B.; Ebani, V.V.; Bertelloni, F.; Galiero, A.; Cerri, D. The presence of Leptospira in coypus (Myocastor coypus) and rats (Rattus norvegicus) living in a protected wetland in Tuscany (Italy). Vet. Arh. 2015, 85, 407–414. [Google Scholar]
  28. Adler, B.; de la Peña Moctezuma, A. Leptospira and leptospirosis. Vet. Microbiol. 2010, 140, 287–296. [Google Scholar] [CrossRef] [PubMed]
  29. Ruiz-Fons, F. A Review of the Current Status of Relevant Zoonotic Pathogens in Wild Swine (Sus scrofa) Populations: Changes Modulating the Risk of Transmission to Humans. Transbound. Emerg. Dis. 2017, 64, 68–88. [Google Scholar] [CrossRef]
  30. Ellis, W.A. Animal Leptospirosis. In Current Topics in Microbiology and Immunology; Springer: Berlin/Heidelberg, Germany, 2015; Volume 387, pp. 99–137. [Google Scholar]
  31. Adler, B. Leptospira and Leptospirosis. In Current Topics in Microbiology and Immunology; Springer: Berlin/Heidelberg, Germany, 2015; ISBN 978-3-662-45059-8. [Google Scholar]
  32. EFSA. The European Union One Health 2018 Zoonoses Report. EFSA J. 2019, 17. [Google Scholar] [CrossRef] [Green Version]
  33. Jajere, S.M. A review of Salmonella enterica with particular focus on the pathogenicity and virulence factors, host specificity and adaptation and antimicrobial resistance including multidrug resistance. Vet. World 2019, 12, 504–521. [Google Scholar] [CrossRef] [Green Version]
  34. Mezal, E.H.; Sabol, A.; Khan, M.A.; Ali, N.; Stefanova, R.; Khan, A.A. Isolation and molecular characterization of Salmonella enterica serovar Enteritidis from poultry house and clinical samples during 2010. Food Microbiol. 2014, 38, 67–74. [Google Scholar] [CrossRef]
  35. Tirziu, E.; Cumpanasoiu, C.; Gros, R.V.; Seres, M. Yersinia enterocolitica Monographic Study. J. Anim. Sci. Biotechnol. 2011, 44, 144–149. [Google Scholar]
  36. Vázquez-Boland, J.A.; Kuhn, M.; Berche, P.; Chakraborty, T.; Domínguez-Bernal, G.; Goebel, W.; González-Zorn, B.; Wehland, J.; Kreft, J. Listeria pathogenesis and molecular virulence determinants. Clin. Microbiol. Rev. 2001, 14, 584–640. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  37. Shamloo, E.; Hosseini, H.; Moghadam, A.Z.; Larsen, H.M.; Haslberger, A.; Alebouyeh, M. Importance of Listeria monocytogenes in food safety: A review of its prevalence, detection, and antibiotic resistance. Iran. J. Vet. Res. 2019, 20, 241–254. [Google Scholar] [PubMed]
  38. EFSA, (European Food Safety Authority); ECDC, (European Centre for Disease Prevention and Control) The European Union summary report on trends and sources of zoonoses, zoonotic agents and food-borne outbreaks in 2017. EFSA J. 2018, 16. [CrossRef]
  39. Nesbakken, T.; Eckner, K.; Høidal, H.K.; Røtterud, O.J. Occurrence of Yersinia enterocolitica and Campylobacter spp. in slaughter pigs and consequences for meat inspection, slaughtering, and dressing procedures. Int. J. Food Microbiol. 2003, 80, 231–240. [Google Scholar] [CrossRef]
  40. Hoelzer, K.; Switt, A.I.M.; Wiedmann, M. Animal contact as a source of human non-typhoidal salmonellosis. Vet. Res. 2011, 42, 1–28. [Google Scholar] [CrossRef] [Green Version]
  41. Bertelloni, F.; Cilia, G.; Bogi, S.; Ebani, V.V.; Turini, L.; Nuvoloni, R.; Cerri, D.; Fratini, F.; Turchi, B. Pathotypes and Antimicrobial Susceptibility of Escherichia Coli Isolated from Wild Boar (Sus scrofa) in Tuscany. Animals 2020, 10, 744. [Google Scholar] [CrossRef]
  42. 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]
  43. OIE. Leptospirosis. Man. Diagnostic Tests Vaccines Terr. Anim. 2018. Available online: https://www.oie.int/fileadmin/Home/eng/Health_standards/tahm/3.01.12_LEPTO.pdf (accessed on 16 April 2021).
  44. Bertelloni, F.; Tosi, G.; Massi, P.; Fiorentini, L.; Parigi, M.; Cerri, D.; Ebani, V.V.V.V. Some pathogenic characters of paratyphoid Salmonella enterica strains isolated from poultry. Asian Pac. J. Trop. Med. 2017, 10, 1161–1166. [Google Scholar] [CrossRef]
  45. Bottone, E.J. Yersinia enterocolitica: The charisma continues. Clin. Microbiol. Rev. 1997, 10, 257–276. [Google Scholar] [CrossRef]
  46. Clinical and Laboratory Standards Institute. M02-A12 Performance Standards for Antimicrobial Disk Susceptibility Tests; Approved Standard-Twelfth Edition; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2015; Volume 35. [Google Scholar]
  47. Clinical and Laboratory Standard Institute. M31-A3 Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated From Animals; Approved Standard-Third Edition; Clinical and Laboratory Standard Institute: Wayne, PA, USA, 2008; Volume 28, p. 8. [Google Scholar]
  48. Skyberg, J.A.; Logue, C.M.; Nolan, L.K. Virulence Genotyping of Salmonella spp. with Multiplex PCR. Avian Dis. 2006, 50, 77–81. [Google Scholar] [CrossRef] [Green Version]
  49. Karasova, D.; Havlickova, H.; Sisak, F.; Rychlik, I. Deletion of sodCI and spvBC in Salmonella enterica serovar Enteritidis reduced its virulence to the natural virulence of serovars Agona, Hadar and Infantis for mice but not for chickens early after infection. Vet. Microbiol. 2009, 139, 304–309. [Google Scholar] [CrossRef]
  50. Huehn, S.; La Ragione, R.M.; Anjum, M.; Saunders, M.; Woodward, M.J.; Bunge, C.; Helmuth, R.; Hauser, E.; Guerra, B.; Beutlich, J.; et al. Virulotyping and antimicrobial resistance typing of Salmonella enterica serovars relevant to human health in Europe. Foodborne Pathog. Dis. 2010, 7, 523–535. [Google Scholar] [CrossRef]
  51. Bhowmick, P.P.; Devegowda, D.; Karunasagar, I. Virulotyping of seafood associated Salmonella enterica subsp. enterica isolated from Southwest coast of India. Biotechnol. Bioinforma. Bioeng. 2011, 1, 63–69. [Google Scholar]
  52. Parvathi, A.; Vijayan, J.; Murali, G.; Chandran, P. Comparative virulence genotyping and antimicrobial susceptibility profiling of environmental and clinical Salmonella enterica from Cochin, India. Curr. Microbiol. 2011, 62, 21–26. [Google Scholar] [CrossRef]
  53. Thoerner, P.; Kingombe, C.I.B.; Bögli-Stuber, K.; Bissig-Choisat, B.; Wassenaar, T.M.; Frey, J.; Jemmi, T. PCR detection of virulence genes in Yersinia enterocolitica and Yersinia pseudotuberculosis and investigation of virulence gene distribution. Appl. Environ. Microbiol. 2003, 69, 1810–1816. [Google Scholar] [CrossRef] [Green Version]
  54. Thisted Lambertz, S.; Danielsson-Tham, M.L. Identification and characterization of pathogenic Yersinia enterocolitica isolates by PCR and pulsed-field gel electrophoresis. Appl. Environ. Microbiol. 2005, 71, 3674–3681. [Google Scholar] [CrossRef] [Green Version]
  55. Falcão, J.P.; Falcão, D.P.; Pitondo-Silva, A.; Malaspina, A.C.; Brocchi, M. Molecular typing and virulence markers of Yersinia enterocolitica strains from human, animal and food origins isolated between 1968 and 2000 in Brazil. J. Med. Microbiol. 2006, 55, 1539–1548. [Google Scholar] [CrossRef] [Green Version]
  56. R Core Team, R. A Language and Environment for Statistical Computing; R Found. Stat. Comput: Vienna, Austria, 2015. [Google Scholar]
  57. Klaasen, H.L.B.M.; van der Veen, M.; Sutton, D.; Molkenboer, M.J.C.H. A new tetravalent canine leptospirosis vaccine provides at least 12 months immunity against infection. Vet. Immunol. Immunopathol. 2014, 158, 26–29. [Google Scholar] [CrossRef] [Green Version]
  58. Martin, L.E.R.; Wiggans, K.T.; Wennogle, S.A.; Curtis, K.; Chandrashekar, R.; Lappin, M.R. Vaccine-Associated Leptospira Antibodies in Client-Owned Dogs. J. Vet. Intern. Med. 2014, 28, 789–792. [Google Scholar] [CrossRef] [Green Version]
  59. Miller, M.D.; Annis, K.M.; Lappin, M.R.; Lunn, K.F. Variability in Results of the Microscopic Agglutination Test in Dogs with Clinical Leptospirosis and Dogs Vaccinated against Leptospirosis. J. Vet. Intern. Med. 2011, 25, 426–432. [Google Scholar] [CrossRef]
  60. Bertelloni, F.; Turchi, B.; Vattiata, E.; Viola, P.; Pardini, S.; Cerri, D.; Fratini, F. Serological survey on Leptospira infection in slaughtered swine in North-Central Italy. Epidemiol. Infect. 2018, 1–6. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  61. Ebani, V.V.; Cerri, D.; Poli, A.; Andreani, E. Prevalence of Leptospira and Brucella Antibodies in Wild Boars (Sus scrofa) in Tuscany, Italy. J. Wildl. Dis. 2003, 39, 718–722. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  62. Greenlee, J.J.; Alt, D.P.; Bolin, C.A.; Zuerner, R.L.; Andreasen, C.B. Experimental canine leptospirosis caused by Leptospira interrogans serovars pomona and bratislava. Am. J. Vet. Res. 2005, 66, 1816–1822. [Google Scholar] [CrossRef] [Green Version]
  63. Goldstein, R.E.; Lin, R.C.; Langston, C.E.; Scrivani, P.V.; Erb, H.N.; Barr, S.C. Influence of infecting serogroup on clinical features of leptospirosis in dogs. J. Vet. Intern. Med. 2006, 20, 489–494. [Google Scholar] [CrossRef] [PubMed]
  64. Cerri, D.; Ebani, V.V.; Fratini, F.; Pinzauti, P.; Andreani, E. Epidemiology of leptospirosis: Observations on serological data obtained by a “diagnostic laboratory for leptospirosis” from 1995 to 2001. New Microbiol. 2003, 26, 383–389. [Google Scholar] [PubMed]
  65. Bertelloni, F.; Cilia, G.; Turchi, B.; Pinzauti, P.; Cerri, D.; Fratini, F. Epidemiology of leptospirosis in North-Central Italy: Fifteen years of serological data (2002–2016). Comp. Immunol. Microbiol. Infect. Dis. 2019, 65, 14–22. [Google Scholar] [CrossRef]
  66. Tagliabue, S.; Figarolli, B.M.; D’Incau, M.; Foschi, G.; Gennero, M.S.; Giordani, R.; Giordani, R.; Natale, A.; Papa, P.; Ponti, N.; et al. Serological surveillance of Leptospirosis in Italy: Two-year national data (2010–2011). Vet. Ital. 2016, 52, 129–138. [Google Scholar] [CrossRef]
  67. Scanziani, E.; Origgi, F.; Giusti, A.M.; Iacchia, G.; Vasino, A.; Pirovano, G.; Scarpa, P.; Tagliabue, S. Serological survey of leptospiral infection in kennelled dogs in Italy. J. Small Anim. Pract. 2002, 43, 154–157. [Google Scholar] [CrossRef]
  68. Ayral, F.C.; Bicout, D.J.; Pereira, H.; Artois, M.; Kodjo, A. Distribution of Leptospira serogroups in cattle herds and dogs in France. Am. J. Trop. Med. Hyg. 2014, 91, 756–759. [Google Scholar] [CrossRef] [Green Version]
  69. Renaud, C.; Andrews, S.; Djelouadji, Z.; Lecheval, S.; Corrao-Revol, N.; Buff, S.; Demont, P.; Kodjo, A. Prevalence of the Leptospira serovars bratislava, grippotyphosa, mozdok and pomona in French dogs. Vet. J. 2013, 196, 126–127. [Google Scholar] [CrossRef]
  70. Geisen, V.; Stengel, C.; Brem, S.; Müller, W.; Greene, C.; Hartmann, K. Canine leptospirosis infections? clinical signs and outcome with different suspected Leptospira serogroups (42 cases). J. Small Anim. Pract. 2007, 48, 324–328. [Google Scholar] [CrossRef]
  71. Tsai, H.J.; Huang, H.C.; Lin, C.M.; Lien, Y.Y.; Chou, C.H. Salmonellae and campylobacters in household and stray dogs in Northern Taiwan. Vet. Res. Commun. 2007, 31, 931–939. [Google Scholar] [CrossRef]
  72. Procter, T.D.; Pearl, D.L.; Finley, R.L.; Leonard, E.K.; Janecko, N.; Reid-Smith, R.J.; Weese, J.S.; Peregrine, A.S.; Sargeant, J.M. A Cross-Sectional Study Examining Campylobacter and Other Zoonotic Enteric Pathogens in Dogs that Frequent Dog Parks in Three Cities in South-Western Ontario and Risk Factors for Shedding of Campylobacter spp. Zoonoses Public Health 2014, 61, 208–218. [Google Scholar] [CrossRef]
  73. Noda, T.; Murakami, K.; Ishiguro, Y.; Asai, T. Chicken Meat Is an Infection Source of Salmonella Serovar Infantis for Humans in Japan. Foodborne Pathog. Dis. 2010, 7, 727–735. [Google Scholar] [CrossRef]
  74. Borowiak, M.; Szabo, I.; Baumann, B.; Junker, E.; Hammerl, J.A.; Kaesbohrer, A.; Malorny, B.; Fischer, J. VIM-1-producing Salmonella Infantis isolated from swine and minced pork meat in Germany. J. Antimicrob. Chemother. 2017, 72, 2131–2133. [Google Scholar] [CrossRef] [Green Version]
  75. Chiari, M.; Zanoni, M.; Tagliabue, S.; Lavazza, A.; Alborali, L.G. Salmonella serotypes in wild boars (Sus scrofa) hunted in northern Italy. Acta Vet. Scand. 2013, 55, 42. [Google Scholar] [CrossRef] [Green Version]
  76. Botti, V.; Valérie Navillod, F.; Domenis, L.; Orusa, R.; Pepe, E.; Robetto, S.; Guidetti, C. Salmonella spp. and antibiotic-resistant strains in wild mammals and birds in north-western Italy from 2002 to 2010. Vet. Ital. 2013, 49, 195–202. [Google Scholar] [CrossRef]
  77. Philbey, A.W.; Mather, H.A.; Gibbons, J.F.; Thompson, H.; Taylor, D.J.; Coia, J.E. Serovars, bacteriophage types and antimicrobial sensitivities associated with salmonellosis in dogs in the UK (1954–2012). Vet. Rec. 2014, 174, 94. [Google Scholar] [CrossRef]
  78. Seepersadsingh, N.; Adesiyun, A.A.; Seebaransingh, R. Prevalence and antimicrobial resistance of Salmonella spp. in non-diarrhoeic dogs in Trinidad. J. Vet. Med. Ser. B Infect. Dis. Vet. Public Health 2004, 51, 337–342. [Google Scholar] [CrossRef]
  79. Caleja, C.; de Toro, M.; Gonçalves, A.; Themudo, P.; Vieira-Pinto, M.; Monteiro, D.; Rodrigues, J.; Sáenz, Y.; Carvalho, C.; Igrejas, G.; et al. Antimicrobial resistance and class I integrons in Salmonella enterica isolates from wild boars and Bísaro pigs. Int. Microbiol. 2011, 14, 19–24. [Google Scholar] [CrossRef] [PubMed]
  80. Zottola, T.; Montagnaro, S.; Magnapera, C.; Sasso, S.; De Martino, L.; Bragagnolo, A.; D’Amici, L.; Condoleo, R.; Pisanelli, G.; Iovane, G.; et al. Prevalence and antimicrobial susceptibility of Salmonella in European wild boar (Sus scrofa); Latium Region –Italy. Comp. Immunol. Microbiol. Infect. Dis. 2013, 36, 161–168. [Google Scholar] [CrossRef] [PubMed]
  81. Knodler, L.A.; Vallance, B.A.; Hensel, M.; Jäckel, D.; Finlay, B.B.; Steele-Mortimer, O. Salmonella type III effectors PipB and PipB2 are targeted to detergent-resistant microdomains on internal host cell membranes. Mol. Microbiol. 2003, 49, 685–704. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  82. Wang, X.; Cui, Z.; Wang, H.; Tang, L.; Yang, J.; Gu, L.; Jin, D.; Luo, L.; Qiu, H.; Xiao, Y.; et al. Pathogenic strains of Yersinia enterocolitica isolated from domestic dogs (Canis familiaris) belonging to farmers are of the same subtype as pathogenic Y. enterocolitica strains isolated from humans and may be a source of human infection in Jiangsu Province, China. J. Clin. Microbiol. 2010, 48, 1604–1610. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  83. Stamm, I.; Hailer, M.; Depner, B.; Kopp, P.A.; Rau, J. Yersinia enterocolitica in diagnostic fecal samples from European dogs and cats: Identification by Fourier transform infrared spectroscopy and matrix-Assisted laser desorption ionization-time of flight mass spectrometry. J. Clin. Microbiol. 2013, 51, 887–893. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  84. Fredriksson-Ahomaa, M.; Korte, T.; Korkeala, H. Transmission of Yersinia enterocolitica 4/O:3 to pets via contaminated pork. Lett. Appl. Microbiol. 2001, 32, 375–378. [Google Scholar] [CrossRef] [PubMed]
  85. Takahashi, T.; Kabeya, H.; Sato, S.; Yamazaki, A.; Kamata, Y.; Taira, K.; Asakura, H.; Sugiyama, H.; Takai, S.; Maruyama, S. Prevalence of yersinia among wild sika deer (Cervus nippon) and boars (sus scrofa) in Japan. J. Wildl. Dis. 2020, 56, 270–277. [Google Scholar] [CrossRef]
  86. Syczyło, K.; Platt-Samoraj, A.; Bancerz-Kisiel, A.; Szczerba-Turek, A.; Pajdak-Czaus, J.; Łabuć, S.; Procajło, Z.; Socha, P.; Chuzhebayeva, G.; Szweda, W. The prevalence of Yersinia enterocolitica in game animals in Poland. PLoS ONE 2018, 13, e0195136. [Google Scholar] [CrossRef]
  87. Foti, M.; Rinaldo, D.; Guercio, A.; Giacopello, C.; Aleo, A.; De Leo, F.; Fisichella, V.; Mammina, C. Pathogenic microorganisms carried by migratory birds passing through the territory of the island of Ustica, Sicily (Italy). Avian Pathol. 2011, 40, 405–409. [Google Scholar] [CrossRef] [Green Version]
  88. Foti, M.; Siclari, A.; Mascetti, A.; Fisichella, V. Study of the spread of antimicrobial-resistant Enterobacteriaceae from wild mammals in the National Park of Aspromonte (Calabria, Italy). Environ. Toxicol. Pharmacol. 2018, 63, 69–73. [Google Scholar] [CrossRef]
  89. von Altrock, A.; Seinige, D.; Kehrenberg, C. Yersinia enterocolitica isolates from wild boars hunted in Lower Saxony, Germany. Appl. Environ. Microbiol. 2015, 81, 4835–4840. [Google Scholar] [CrossRef] [Green Version]
  90. Clinical and Laboratory Standards Institute (CLSI). M100 Performance Standards for Antimicrobial Susceptibility Testing A CLSI Supplement for Global Application, 28th ed.; CLSI Supplement M100; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2018. [Google Scholar]
Table
Table 1. Serological reactions detected in hunting dog sera in relation to Leptospira serogroups, their vaccination state, and hunting company.
Table 1. Serological reactions detected in hunting dog sera in relation to Leptospira serogroups, their vaccination state, and hunting company.
DogSexYearBreedHunting CompanyLeptospira SerogroupVaccine
IcCaPoGrTaAuSeBa
D1 *M2SMPisa1:1001:1001:4001:100 E
D2 *F6SMPisa1:1001:100 1:100 E
D3 *F2SMPisa1:1001:1001:2001:100 E
D4 *M2SMPisa1:1001:100 1:200 E
D5 *M2SMPisa1:1001:1001:1001:100 E
D6 *F9ESPisa1:1001:1001:1001:100 E
D7 *M6ESPisa1:1001:1001:1001:100 E
D8 *F6SMPisa1:1001:1001:2001:100 E
D9 *F4SMPisa1:1001:1001:4001:200 E
D10 *M4SMPisa1:2001:1001:4001:100 E
D11 *F10SMPisa1:1001:100 1:100 E
D12 *F2SMPisa1:1001:100 1:200 E
D13 *F1SMPisa1:1001:1001:4001:100 E
D14 *F1SMPisa1:1001:1001:2001:100 E
D15 *F2SMPisa1:1001:100 1:100 E
D16 *F3SMPisa1:1001:2001:4001:100 E
D17 +M2ESSPisa1:1001:1001:2001:200 E
D18 +F7ESSPisa1:2001:1001:2001:100 E
D19 ¤M4SMPisa1:1001:2001:2001:100 1:100 N
D20 ¤F3SMPisa 1:200
D21 ¤M2SMPisa 1:200
D22 °M9BSPisa1:1001:1001:4001:100 1:100 N
D23 °F3ESSPisa1:1001:1001:2001:100 E
D24 #M6BSPisa1:1001:100 C
D25 #M3SMPisa 1:200
D26 #M3SMPisa 1:200
D27 #M3SMPisa 1:400
D28 #M2SMPisa 1:200
D29 #F3SMPisa 1:200
D30 #F8SMPisa 1:200
D31M1SMLucca1:1001:1001:2001:200 1:100 N
D32 •M2SMLucca1:1001:1001:4001:100 1:100 N
D33 •M11GFLucca1:1001:100 1:100 1:100 N
D34 •F2GFLucca1:1001:100 1:100 1:100 N
D35 •M3SMLucca1:1001:1001:1001:200 1:100 N
D36 •M3SMLucca1:1001:100 1:100 1:100 N
D37 •F7SMLucca1:1001:100 1:100 1:100 N
D38 ◊M7HBLucca 1:200
D39 ◊F4SMLucca 1:200 1:100
D40 ◊F4SMLucca 1:1001:200
D41 □M6SMLucca
D42 □M5SMLucca 1:200
Dog IDs with same symbols from same owners. SM, Segugio Maremmano; ES, English Setter; ESS, English Springer Spaniel; BS, Brittany Spaniel; GF, Griffon Bleu de Gascogne; HB, half-breed; Ic, Icterohaemorrhagiae; Ca, Canicola; Po, Pomona; Gr, Grippotyphosa; Ta, Tarassovi; Au, Australis; Se, Sejroe; Ba, Ballum; E, Eurican L-multi®, covering for serovars Canicola, Icterohaemorrhagiae, and Grippotyphosa; N, Nobivac L-4®, covering for serovars Canicola, Icterohaemorrhagiae, Bratislava, and Grippotyphosa; C, Canigen DHPPi/L®, covering for serovars Canicola and Icterohaemorrhagiae.
Table
Table 2. Virulence genes and antimicrobial resistance profiles of analyzed and characterized Salmonella spp. strains.
Table 2. Virulence genes and antimicrobial resistance profiles of analyzed and characterized Salmonella spp. strains.
IsolateSerotypeDogVirulence Gene ProfileAntimicrobial Resistance Profile
S395InfantisD2pipB, sopEStreptomycin
S396InfantisD9--
S397InfantisD13pipB-
S398InfantisD16pipBStreptomycin
Table
Table 3. Virulence genes and antimicrobial resistance profiles of analyzed Yersinia enterocolitica isolates.
Table 3. Virulence genes and antimicrobial resistance profiles of analyzed Yersinia enterocolitica isolates.
IsolateBiotypeDogVirulence Gene ProfileAntimicrobial Resistance Profile
YD11D6ailAMP, KF
YD21D7ystAAMP, AMC, KF, FOX
YD31D10 AMP, AMC, KF
YD44D13ystA, ystB, invAMP, AMC, KF, FOX, C, S, NA
YD51D15ailAMP, AMC, KF
YD61D16ystBAMP, AMC, KF
YD71D17virFAMP, AMC, KF
AMC, amoxicillin–clavulanic acid; AMP, ampicillin; KF, cephalothin; FOX, cefoxitin; S, streptomycin; NA, nalidixic acid; C, chloramphenicol.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Cilia, G.; Fratini, F.; Turchi, B.; Ebani, V.V.; Turini, L.; Bilei, S.; Bossù, T.; De Marchis, M.L.; Cerri, D.; Bertelloni, F. Presence and Characterization of Zoonotic Bacterial Pathogens in Wild Boar Hunting Dogs (Canis lupus familiaris) in Tuscany (Italy). Animals 2021, 11, 1139. https://doi.org/10.3390/ani11041139

AMA Style

Cilia G, Fratini F, Turchi B, Ebani VV, Turini L, Bilei S, Bossù T, De Marchis ML, Cerri D, Bertelloni F. Presence and Characterization of Zoonotic Bacterial Pathogens in Wild Boar Hunting Dogs (Canis lupus familiaris) in Tuscany (Italy). Animals. 2021; 11(4):1139. https://doi.org/10.3390/ani11041139

Chicago/Turabian Style

Cilia, Giovanni, Filippo Fratini, Barbara Turchi, Valentina Virginia Ebani, Luca Turini, Stefano Bilei, Teresa Bossù, Maria Laura De Marchis, Domenico Cerri, and Fabrizio Bertelloni. 2021. "Presence and Characterization of Zoonotic Bacterial Pathogens in Wild Boar Hunting Dogs (Canis lupus familiaris) in Tuscany (Italy)" Animals 11, no. 4: 1139. https://doi.org/10.3390/ani11041139

APA Style

Cilia, G., Fratini, F., Turchi, B., Ebani, V. V., Turini, L., Bilei, S., Bossù, T., De Marchis, M. L., Cerri, D., & Bertelloni, F. (2021). Presence and Characterization of Zoonotic Bacterial Pathogens in Wild Boar Hunting Dogs (Canis lupus familiaris) in Tuscany (Italy). Animals, 11(4), 1139. https://doi.org/10.3390/ani11041139

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