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. 2025 Oct 31;21:101263. doi: 10.1016/j.onehlt.2025.101263

Estimated prevalence and genetic diversity of Bartonella species in small mammals in Europe: Systematic review and meta-analysis

Aya AK Zarea a,b,⁎, Younes Laidoudi c,d, Amienwanlen E Odigie e, Daniela Mrenoshki e, Maria Francesca Iulietto a, Grazia Greco e, Roberto Condoleo a
PMCID: PMC12666148  PMID: 41333645

Abstract

Bartonellosis is a neglected vector-borne zoonotic disease caused by Bartonella species that infect a wide array of mammals. The adaptation of Bartonella to various animal hosts, including small mammal populations, has been reported, indicating their potential as a significant reservoir harboring a high genetic diversity of these pathogens, thereby posing a risk for zoonotic transmission to humans through close ecological or physical contact. Thus, this study aimed to give an overview of the prevalence and the genetic diversity of Bartonella spp in small mammals throughout Europe. Consequently, a systematic review was undertaken by retrieving all relevant articles indexed in PubMed, Scopus and Web of Science. Subsequently, a meta-analysis was performed to compute the pooled prevalence of Bartonella spp. Moreover, subgroup moderator analyses were then performed, examining the impact of sub-European region, sample type, gender, and small mammal species on the observed prevalence estimates. A total of 76 studies were included in this study. The estimated pooled prevalence of Bartonella spp across small mammal populations in Europe was 30%. Notably, regional analysis revealed significant variations, with the highest prevalence observed in the Eastern region (43%). At the country level, Russia had the highest pooled prevalence of 65%, while Austria had the lowest estimated prevalence (5.7%). Although variations were observed in Bartonella spp prevalence among subgroups, this difference was not statistically significant (p-value > 0.05). A high diversity of Bartonella spp was observed in European small mammals with twenty-one Bartonella species detected, and nine of them being pathogenic to humans. The present study offers a comprehensive understanding of the eco-epidemiology of Bartonella spp in small mammal in Europe, providing insight into their role as reservoirs and potential vectors in the maintenance and transmission of Bartonella species.

Keywords: Bartonella species, Europe, Systematic review, Small mammals, Meta-analysis

1. Introduction

Bartonella is a fastidious, Gram-negative, facultative intracellular alpha-proteobacteria that infects a wide diversity of mammalian reservoirs including canids, felids, birds, ruminant, rodents, bats, and wild animals through the infection of erythrocytes and endothelial cells [[1], [2], [3], [4], [5]]. Infection with Bartonella spp results in persistent bacteremia by evading the host immune response [6]. Among mammalian populations, blood-feeding arthropod vectors such as fleas, ticks, lice, sand flies, and bed bugs considered the main route of Bartonella spp transmission [7]. Notably, some Bartonella species remain viable in arthropod faeces and can infect superficial wounds through scratches [8].

Currently, more than 45 species and 3 subspecies of Bartonella have been detected (https://lpsn.dsmz.de/family/bartonellaceae); of these, at least 15 species known to be zoonotic [3,8]. As a result of the improvement and implementation of more efficient molecular techniques for Bartonella characterization, the number of Bartonella species is rapidly increasing, including novel ones [3,9]. However, due to the high diversity of Bartonella spp and their wide range of mammalian hosts and arthropod vectors, the ecology of these bacteria is complex and not well completely understood [10,11].

According to the European Centre for Disease Prevention and Control (ECDC) data, more than 60% of human pathogens are of animal origin, with most of them being vector-borne disease [12]. Among these zoonotic diseases, cat scratch disease (CSD), caused by B. henselae, where cats serve as the primary reservoir and transmission to humans primarily occurs through infected cat fleas (Ctenocephalides felis) [8,[13], [14], [15]]. Additionally, B. bacilliformis and B. quintana are the causative agents of human bartonellosis known as Carrion’s disease and trench fever [3]. Moreover, in the last decade, other Bartonella species, such as B. clarridgeiae, B. koehlerae, B. grahamii, B. vinsonii, B. tribocorum, B. alsatica, B. ancashensis, B. doshiae, B. elizabethae, B. kosoy, B. rattimassiliensis, and B. rochalimae have been associated with human bartonellosis particularly among immunocompromised individuals, exhibiting symptoms ranging from mild to fever, lymphadenitis, encephalitis, bacillary, angiomatosis, neuroretinitis and endocarditis [[16], [17], [18], [19], [20]].

Rodents are the largest and most diverse group of living mammals, constituting approximately 43% of the total number of mammalian species worldwide [21,22]. In Europe, a wide diversity of rodent species are inhabitants, including bank voles (Myodes glareolus), wood mice (Apodemus sylvaticus), house mice (Mus musculus), and brown rats (Rattus norvegicus) [23]. These species are integral to European ecosystems, serving as prey for a range of predators and facilitating essential seed dispersal mechanisms. Besides their ecological roles, these small mammals are also significant in public health, acting as reservoirs for numerous pathogens, including those with zoonotic potential [24]. Moreover, they consider an important host for numerous vectors, including fleas and young ticks, leading to risk for pathogen spillover, especially those transmitted by vectors [[24], [25], [26], [27]]. For example, the diverse Bartonella genus which has over 22 known species is associated with approximately 90 rodent species including ten documented as human pathogens [28,29].

This study aims to assess the prevalence and genetic diversity of Bartonella spp in small mammals in Europe and the risk factors that contribute to the spread of these pathogens. An overview of the characteristics of Bartonella spp would be insightful into the role of small mammals as reservoirs and potential vectors in the maintenance and transmission of a diverse array of Bartonella species and could guide public health strategies in the control of zoonotic species among animal populations and humans.

2. Methods

The current study was conducted following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) standards [30]. This protocol was registered in the International Prospective Register of Systematic Reviews (PROSPERO) under the registration number CRD42024526863.

2.1. Data sources and search strategy

On February 29, 2024, three databases, including PubMed (https://pubmed.ncbi.nlm.nih.gov), Web of Sciences (https://apps.webofknowledge.com/), and Scopus (https://www.scopus.com), were screened in the title, abstract, and full text, depending on the database capabilities to retrieve relevant articles using a combination of specific strings as follows: (molecular" OR "survey" OR "occurrence" OR "prevalence" OR “incidence” OR “epidemiology” OR “detection” OR “surveillance” OR “genetic”) AND ("Bartonella*" OR "bartonellosis")) AND (“rodent*" OR “mammal*” OR "small mammals" OR "rat*" OR "mice" OR "mouse" OR “hedgehog*” OR “shrew”). Moreover, a systematic snowballing approach was applied to identify further relevant studies. This included both backward snowballing (examining the reference lists of included articles) and forward snowballing (checking all the references that cited the selected article). Initial pool of articles was then subjected to a rigorous screening process, restricting the final selection to studies conducted in Europe according to the European Union country classification (https://eur-lex.europa.eu/browse/eurovoc.html?params=72#arrow_72).

2.2. Inclusion and exclusion criteria

According to the PRISMA guidelines, the article title and abstract were first assessed for their relevancy to the topic. Two investigators independently evaluated the full texts to determine whether the content aligned with the current review's approach. A third independent author decision was reached after adjudication in cases of disagreement. Studies were included if they met with the inclusion criteria (PECOTS Element): (1) full texts published in English and studies conducted in Europe countries, (2) cross-sectional studies, observational research, letters to the Editor or short reports that studied the prevalence of Bartonella spp by molecular methods in small mammals (except bats). While serological studies, clinical trials, case reports, and workshop presentations were excluded.

2.3. Data extraction

Data were extracted using a standardized Excel sheet (Microsoft Excel®, Version 2016). The following main data were extracted:

  • 1)

    Study publication details: title, authors, year, and country where the study was conducted.

  • 2)

    Methodology: (a) full description of the enrolled animals, including species; (b) sampling period in year and month; (c) molecular methods and the gene (s) targeted for species identification and characterization; (d) sample size and type; (e) prevalence estimates; (e) Bartonella species detected; (f) possible moderators for the Bartonella occurrence (e.g., sub-European region, small mammal’s family, age and gender).

The classification of animal species was conducted at the family level, as referenced by the Animal Diversity Web (ADW). https://animaldiversity.org. and Musser, G. (2024) [31].

2.4. Quality assessment and risk of publication bias

The Joanna Briggs Institute (JBI) Critical Appraisal tools for Prevalence Studies were initially used to evaluate the methodological quality of the included studies [32]. Seven domains were assessed individually using the ratings "Yes", "Unclear" and "No", with ratings of two, one and zero respectively. The total scores ranged from 0 to 14, with scores ≥11 considered high quality, scores between 7 to 10 considered moderate quality, and less than 7 considered low-quality studies and will be excluded. Two investigators rigorously evaluated each article, and any disagreement were resolved through consensus. The risk of publication bias among studies was evaluated using funnel plots and verified using Egger's regression test.

2.5. Statistical analysis

Descriptive analysis was initially performed on the studies included in the systematic review. In cases where multiple prevalence data for different countries were reported within a single record, each study was treated as a separate entity. The estimated pooled prevalence of Bartonella spp in small mammals was calculated using the restricted maximum likelihood (REML) method, with a random effects model was used to pool the individuals. The Freeman-Tukey double arcsine approach was applied to stabilize the inherent variability caused in the prevalence studies [[33], [34], [35]]. The degree of heterogeneity among studies was evaluated using the Higgins inverse variance index (I2) statistic and the Q value. The subsequent thresholds for the degree of heterogeneity were employed; I2 = 0- 25%, 30 - 60% and over 75% may indicate low, moderate and high heterogeneity respectively [36]. The Baujat plot and leave-one-out diagnostics tests were built to investigate the presence of outliers. Meta-regression analysis was performed to evaluate the potential effect of the year of publication on the pooled prevalence reported across studies. Moreover, subgroup moderator analysis was performed to explain the observed heterogeneity and investigate the impact on the observed prevalence estimates of geographical region (sub-Europe region), small mammals' family, sample type (i.e., Blood, tissue and faeces), and gender (male, female).

3. Results

3.1. Search results and quality of eligible studies

The selection of eligible records is outlined in a PRISMA flow diagram (Figure 1). In total, 63 records were included based on the predefined inclusion and exclusion criteria, out of 1,037 records initially identified from PubMed (n = 398), Scopus (n = 427), and Web of Science (n = 212). Considering the prevalence data of different countries in the same record, 76 studies were included in the meta-analysis. The included records received a quality assessment score ranging from 8 to 14 based on JBI's critical evaluation. Of these, 64 studies (84.2%) were rated as high quality, 12 studies (15.8%) as moderate quality, and no study was excluded based on its quality (Supplementary Table S1).

Fig. 1.

Fig. 1

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Flow chart of the search strategies and selection of studies included in the systematic review and meta-analysis of Bartonella spp. in small mammals in Europe.

3.2. Risk of publication bias

The funnel plot appeared symmetric, suggesting that there was no publication bias among the studies (Figure 2). This finding was corroborated by Egger’s regression test (P > 0.2), which also indicated no significant publication bias (Supplementary Material, Fig. 1, Fig. 2).

Fig. 2.

Fig. 2

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Funnel plot for the publication bias test.

3.3. Characteristic of the studies

The review encompassed studies from 2001 to 2023, ranging from one to 16 studies, with the highest number in 2019 (n = 16), followed by 2023 (n = 7) with no study retrieved in 2006 (Figure 3 (Panel A)). The included studies were carried out in 25 European countries and ranged from 1 to 8 studies for each country, with the highest number of studies in Poland (n = 8) and Spain (n = 7) (Figure 3 (Panel B)), Supplementary material, Table S2). At the sub-Europe region level, a high number of studies were retrieved from the central (n = 25) and western (n = 24), followed by the southern (n = 14), northern (n = 7), and eastern (n = 5) region of Europe.

Fig. 3.

Fig. 3

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Distribution of publications and studies number (Panel A. Distribution of publications number per year and Panel B : Distribution of studies number per country)

3.4. Small mammal’s species and their Bartonella prevalence

The included studies (n=76) screened a total of 20,271 samples for Bartonella spp, of which 16,603 samples came from identified small mammal species and were investigated in 64 studies. A total of 35 small mammal species were identified, and belonging to 8 mammalian families within 3 orders (Rodentia, Eulipotyphla and Erinaceomorpha). Rodentia is considered the most abundant order, with Cricetidae being the most common family (n = 8418, 50.7%), followed by Muridae (n = 6509, 39.2%) and Soricidae (n = 663, 4%). Bartonella spp prevalence rate was varied according to the small mammals species with the highest rat was detected in European snow vole (2/2, 100%), Edible dormouse (23/31, 74.2%), Mediterranean water shrew (9/15, 60%), Birch mouse (9/15, 60%), Red squirrel (69/115, 60%) and Social vole (28/48, 58.3%), while the lowest was detected on Lesser white-toothed shrew (24/467, 5.1.5 %), House mouse (28/438, 6.4%), Montane water vole (18/172, 10.5%) and Domestic mouse (22/218, 10.2%). Moreover, no Bartonella spp was detected in all of Mediterranean pine vole, East European vole, Pygmy shrew and Rattus sp. (Figure 4).

Fig. 4.

Fig. 4

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Bubble plot showing the prevalence of Bartonella species in small mammals in Europe with the size of the circle represent the total animal sampled.

3.5. Bartonella species

A total of 7387 samples were positive for Bartonella spp, with 3099 (42%) samples were sent for sequencing to identify the species using different loci such as ITS, gltA, rpoB, virB5, 16S rRNA, nuoG, and ftsZ. In detail, B. taylorii was the highly dominant species (39.1%) cross the European countries (n= 18), followed by B. grahamii (18.1%, no. of countries = 21), B. tribocorum (9.7%,10 countries), B. birtlesii (5.2%, 11 countries), and B. doshiae (4%, 10 countries). Furthermore, species related to companion animals, such as B. rochalimae (2.9%, 5 countries), B. henselae (1.2%, 5 countries), and B. clarridgeiae (0.1%, 3 countries) (Fig. 5, Fig. 6, Supplementary material, Table S3). Furthermore, novel Bartonella species were reported in studies in Slovakia, Spain, Sweden, France, and Slovenia with a percentage of 0.8% of the total detections. In Slovakia, the novel species identified showed 92.5% similarity to B. clarridgeiae and 94.5% to B. rochalimae. In Spain and France, novel species with less than 90% similarity to any known Bartonella species were also detected. Additionally, in France, 41 strains of Bartonella strains (FJ946856) were similar to a species previously identified in a dog in Thailand, suggesting the presence of a new species (Bai et al., 2009).

Fig. 5.

Fig. 5

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Heat map showing the number of Bartonella species identified from sequenced positive small mammals per each country.

Fig. 6.

Fig. 6

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Prevalence of Bartonella species with their 95%CI in small mammals in Europe

A few cases of B. rudakovii (0.86%), B. elizabethae (0.7%), B. coopersplainsensis (0.3%), B. queenslandensis (0.1%), B. mastomydis (0.06%), B. melophagi (0.03%), and B. kosoy (0.03%) were detected. Finally, unidentified Bartonella spp showed a prevalence of 1.5% and the co-occurrence of multiple infections (co-infection) was observed at a prevalence rate of 2.8% (Figure 6).

3.6. Meta-analysis of Bartonella species in small mammals

The overall prevalence of Bartonella spp in small mammal population in Europe, was 30% (95%CI: 24-36), with observed high heterogeneity (I2 = 98%, Q-statistics = 3304.86, P-value < 0.0001) indicating substantial variance between the studies (Figure 7). The estimated pooled prevalence was not statistically significant associated with the year of publication (regression slope = -0.005, P-value < 0.34) (Figure 8).

Fig. 7.

Fig. 7

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Forest plot displaying the pooled prevalence estimates of Bartonella spp. in small mammals. The “Proportion” column shows the prevalence of Bartonella spp. in each study, while the 95% CI represents the corresponding confidence interval (CI). The dashed line represents the global pooled prevalence estimate based on the random effects model. The length of the horizontal lines represents the 95% CIs. The estimated global prevalence is the red diamond at the bottom of the plot.

Fig. 8.

Fig. 8

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A meta-regression graph representing the global prevalence of Bartonella spp. in small mammals based on year of publication. The pink line is the regression line, which was plotted based on the intercept and the slope of the regression model. The different color bubbles represent the countries under study and their sizes indicate the effect size of each study Year of publication (slope = -0.005, P-value < 0.34).

3.7. Pooled prevalence based on sub-Europe region and country

Among sub-European regions, the highest pooled prevalence was estimated in the Eastern region 43% (95%CI: 23–65), followed by the Southern and West regions which had the same value (31%, 95%CI: South 19-44, and West: 22-42). Central Europe prevalence was 26% (95%CI: 15-38) and was similar to the Northern region (25%, 95%CI: 13- 39) (Table 1). Regarding the country level, the estimated prevalence was ranged between 5.7 to 65%, with Russia showing the highest pooled prevalence of 65% (95%CI: 57.2–72.4), followed by the Czech Republic 54.4% (95%CI: 18.6–87.8), Turkey 47.1% (95%CI: 22.1–72.9), France 43.1% (95%CI: 29.7-57.0), Italy 41.6% (95%CI: 0-100) and Georgia 41.2% (95%CI: 29.7-53.1). While the lower estimated prevalence was observed in Austria 5.7% (95%CI: 0.00- 18.6) and Hungary 7.5% (95%CI: 0.00 - 37.5) (Figure 9). It is important to note that the study of Inoue et al. (2010) collected samples from the Netherlands and Czech Republic, thereby classifying it as a non-identified (NA) country.

Table 1.

Meta-regression and subgroup analysis of Bartonella spp prevalence in small mammals in Europe based on sub-Europe region, small mammals spp, sample type and gender.

Variables
 Study nu.
 total
 cases
 ES
 95% CI
 wt of ES
 Heterogeneity
 Subgroup analysis
tau2 tau Q I2 p-value R2 QM df I2 p-value
Region 0.0 1.9442 4 98.7 0.7
 North 7 1437 506 25 13 - 39 9.1 0.0348 0.19 186.19 96.8 <0.01
 Central 25 9135 3112 26 13 - 39 32.5 0.1030 0.32 1239.00 98.1 <0.01
 East 5 500 171 43 23 - 65 6.6 0.0572 0.23 130.96 97 <0.01
 West 24 7056 2788 31 22 - 44 33.4 0.0698 0.26 1364.81 98.3 <0.01
 South 14 2035 741 31 19 - 44 18.4 0.0617 0.25 304.3 95.7 <0.01
 NA 1 50 0 0 0 - 5.8 1.3
Small mammals species 0.54 10.0751 7 96.3 0.29
 Muridae 45 7111 2881 28.1 21.5 - 35.1 48.2 0.09 0.31 2291.1 95.9
 Cricetidae 33 8418 3100 28.4 21.3 - 36 36.1 0.06 0.25 1412.7 95.4
 Soricidae 8 663 88 23.2 10.8 - 37.9 9 0.05 0.23 181.3 90
 Talpidae 5 207 88 59.2 29.3 - 86.7 2.1 0.02 0.16 11.04 63.8
 sciuridae 5 135 73 46.2 19.6 - 73.8 2.7 0.05 0.23 26.8 85.1
 Gliridae 1 31 23 74.2 57.1 - 88.3 0.6
 Erinaceidae 1 23 3 13 1.8 - 30.4 0.6
 Sminthidae 1 15 9 60 33.8 - 83.7 0.6
Gender 0.0 0.3286 2 96.31 0.56
 Male 6 826 453 48.6 26.9 - 70.7 50.6 0.07 0.26 47.44 89.5
 Female 6 789 299 38.5 15.8 - 64 49.4 0.08 0.30 103.45 95.2
 Sample type 1.37 3.1146 2 98.7 0.21
 Tissue 54 11418 3946 27 20 - 34 70.9 0.08 0.29 2576.6 97.9 <0.001
 Blood 21 8838 3441 38 30 - 47 28 0.04 0.19 615.5 96.9 <0.01
 Feaces 1 16 1 6 0.0 - 25 1.2
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Fig. 9.

Fig. 9

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Spatial distribution of Bartonella spp. prevalence in small mammals in Europe.

3.8. Meta-regression and subgroup analysis

A subgroup analysis was conducted to evaluate the potential influence of different determinants including sampling types, sub-European regions, small mammal species and gender on the prevalence of Bartonella spp in small mammals across Europe. No significant differences were observed between sub-European regions (P-value = 0.7). Regarding sample type, a higher prevalence of Bartonella spp was observed in blood samples (38%) compared to tissue samples (27%); however, there were fewer studies on blood samples (20 vs. 54). Moreover, only one study analyzed faeces with a prevalence of 6%. When considering small mammal’s family, Gliridae had a high Bartonella spp prevalence of 74.2%, followed by Sminthidae 60%, Talpidae 59.2%, Sciuridae 46.2%, Cricetidae 28.4%, Soricidae 23.2%, Erinaceidae 13%, and Muridae 28.1% (Table 1). Moreover, a higher Bartonella spp prevalence was seen in male gender (48.6%) than females (38.5%). Although the differences of Bartonella prevalence among subgroup categories were observed, none of the comparisons were statistically significant (P-value > 0.05) (Table 1).

4. Discussion

Emerging and re-emerging infectious pathogens are a threat to human health. Within them, Bartonella is considered an emerging vector-borne pathogen often zoonotic, reported worldwide. Since 1993, when the Bartonella genus was first reported, research efforts have focused on small mammals, recognized as an important reservoir for Bartonella [37]. Initially, reports of Bartonella occurrence on small mammals were conducted in North America and then expanded to Europe, Asia, Latin America, and Africa [4]; hence, this is the first study that mapped the distribution and species diversity of Bartonella spp in small mammals in Europe.

While Bartonella species have been reported in at least half of the European countries (n=25), the result of this study indicates that the occurrence of Bartonella spp was first investigated in the UK’s wild population of woodland rodents and squirrels [38,39], followed by another study from Sweden in 2003 [40]. Since then, the awareness of bartonellosis in small mammals has increased in Europe. Thus, highlighting the awareness of these countries of the threat of small mammals to spillover Bartonella spp to other animal species and humans.

The prevalence of Bartonella species ranged from 2% to 100% in rodents worldwide [4,41]. In the present study, the estimated pooled prevalence of Bartonella spp was 30% in European small mammal populations, with high heterogeneity was observed between the included studies. This finding was slightly in agreement with a study conducted in 67 countries, which reported a combined prevalence of 34.4% among rodent populations [5]. While, it was higher than those reported in rodents from the Mediterranean region (23%) [42] and South Africa 16.9% [43].

Moreover, our finding revealed geographical variation in Bartonella spp prevalence across sub- Europe region and countries. The highest prevalence was observed in Eastern Europe (43%), although this was based on few studies (n = 5) [[44], [45], [46], [47], [48]]. Other regions showed similar rates: Southern (31%), Western (31%), Central (26%), and Northern Europe (25%). At the country level, Bartonella spp prevalence in the present study ranged from 5.7% in Austria [[49], [50], [51]] to 65% in Russia [46,48], with all of included countries reporting presence of Bartonella spp. in small mammals, highlighting the role of small mammals as reservoirs capable of spreading Bartonella spp. across Europe [24]. The observed variability in Bartonella spp prevalence in different geographical regions could be returned to the vector species, local vector control measure, seasonal timing of sample collection, sample size, geographic focus (rural vs. urban), animal species, habitat environmental condition and the number of included studies [52,53].

Interestingly, in the study of Zarea et al. (2023) [2], a high combined prevalence of Bartonella spp in companion animals was observed in regions located at latitudes 57°N–29°S and 32°N–38°S. This aligns with the countries showing high prevalence in our meta-analysis. These findings highlight the need for further investigation into environmental and risk factors, such as temperature, season, rainfall, humidity, vector density and movement patterns of small mammal populations to better understand the reasons of this variability and allow us to have proper control and prevention methods.

In general, collecting blood samples from small mammals is more challenging during sampling, but it is considered the standard sample for Bartonella detection and culture, as Bartonella are known to target endothelial cells and causing bacteremia. For example, B. henselae has been found in blood vessel walls [54], and B. quintana is discovered within and in clusters surrounding endothelial cells [55]. Furthermore, spleen tissue is preferred to use in case of lacking blood samples [56]. In the present study, Bartonella was more prevalent in blood samples (38%) than in spleen tissues (27%), with no significant difference observed between sample types (P-value = 0.21, R2 = 1.37). Interestingly, a study by Mass et al. (2020) [57] has detected Bartonella spp in the feces of Eurasian beavers (1/16) in The Netherlands, while the spleen tissue from the same animals was negative. These findings raise questions about the distribution of Bartonella across different animal tissues in relation to the sample matrices collected for surveys, as well as the role of faecal shedding in the epidemiology of these pathogens.

Worldwide, approximately six orders of small mammal have been known, with the Rodentia order being the most common one in Europe [58]. The same finding was observed in our result, where the Rodentia order was the most abundant (n= 15710) and in the meantime had the highest prevalence of Bartonella infection in Europe (38.7%), compared to the Eulipotyphla (n=870, 20.2%) and Erinaceomorpha (n=23, 13.4%) order. The high detection rate of Bartonella in Rodentia order could be related to a high host density or abundance that significantly influences the infection rate [59,60]. Previous studies have shown that the higher prevalence of Bartonella spp was positively correlated with the most abundant small mammal of the micromammal community in the Mediterranean peri-urban environment [61,62]. Moreover, a higher host density can increase vector transmission and contact rate between hosts, leading to increase the likelihood of Bartonella occurrence [4,61]. This abundance-driven pattern was also observed at the family and species level in our study. However, no statistical differences were observed (P-value = 0.29) within different small mammal’s families suggesting that more studies are required to determine whether the infection rate is correlated with high density or larger populations. In particular, factors such as rodent behavior (i.e., physical contact, grooming, mobility, spatial behavior), climatic conditions, vector presence (i.e., flea parasitism), and rodent seasonality (e.g., for reproductive purposes) can influence the risk of Bartonella infection in small mammals [63].

Some Bartonella species show low specificity, enabling them to adapt to a wide range of different hosts, while others are highly host-specific (i.e., B. henselae for the cat and B. bovis for ruminant). However, the host association of many species is still unclear, especially in small mammals [64]. Globally, more than 30 species and subspecies of Bartonella are found in small mammals, with 13 of which recognized having zoonotic potential [3,4,65]. Moreover, recombination of Bartonella spp within the small mammals exists and may serve for the new species [26,66,67].

In our study, 21 Bartonella species were detected, highlighting the genetic diversity of Bartonella spp circulating in European small mammals. The most dominant species was B. taylorii (39.1%) followed by B. grahemiii (18.1%), B. tribocorum (9.7%) and B. birtlesii (5.2%) in almost all Europe [5,40,44,[68], [69], [70], [71]]. These species were also detected throughout the world such as in Africa [72,73], Asia [65,74], America [[75], [76], [77]].

However, the most frequently detected Bartonella species may be a distortion and reflect historical detection biases. For instance, B. grahamii was first found in the blood of moles and later isolated from Myodes glareolus in the UK [78]. Subsequently, B. elizabethae was detected in rodents in 1993, followed by the identification of B. taylorii in wood mice in 1995 [79] and Bartonella tribocorum from wild rats in 1998 [80]. More recently, novel Bartonella species, such as B. kosoyi, have been described, particularly from rodents, and not being identified until 2018 [9]. It is important to note that not all published sequences exhibit 100% homology, and different methodologies have been used across studies, which may influence the reported diversity of Bartonella species. In our study, novel Bartonella species were reported in different countries throughout Europe, including Greece [81], Croatia [45], Spain [82], the Czech Republic [83], Slovakia [69,84], Sweden [40], Slovenia [85], and France [86], highlighting the necessity for persistent surveys in the field.

While this study focused on small mammals, these species are recognized as important reservoirs for Bartonella spp, posing potential risks to humans and domestic animals. In Europe, Bartonella infections have been reported in cats and dogs, with pooled prevalence of 15.6% and 0.6%, respectively [2], suggesting possible cross-species transmission. Frequent interactions between rodents and companion animals in shared environments may facilitate the spread of rodent-associated Bartonella spp. to humans. Moreover, the risk of rodent-associated Bartonella infections in humans, particularly among individuals with specific vulnerabilities such as alcoholism, homelessness, and intravenous drug use was reported [79,80]. Although the IV transmission route remains uncertain, it was suggested to increase the risk of Bartonella infection [81]. Poor hygiene and infestation with ectoparasites, such as lice and fleas, also increase the risk of bartonellosis, especially among homeless populations [87]. In this study, nine Bartonella species are known human pathogens, including B. henselae, B. clarridgeiae, B. quintana, B. elizabethae, B. vinsonii subsp. berkhoffii, B. vinsonii subsp. Arupensis, B. tribocorum, B. melophagi, B. rochalimae, and B. washoensis were detected. These species are responsible for a range of clinical signs, including CSD, bacteremia, trench fever, endocarditis, splenomegaly, neuroretinitis, and even death in immunocompromised people [19,20]. Human infections involving rodent-associated Bartonella spp. have been reported across Europe and other regions. B. henselae, B. tribocorum, B. doshiae, B. schoenbuchensis and B. alsatica have been reported in French patients ([88,89]; B. elizabethae was detected in a Mexican patient with bacillary angiomatosis [20]; B. tribocorum and B. elizabethae were isolated from a woman in Tbilisi, Georgia, presenting with lymphadenopathy and fever [29]; B. grahamii was associated with bilateral neuroretinitis in a Dutch patient [90]; and B. vinsonii subsp. arupensis was identified in an Italian child with hepatic granulomatous lesions [85]. These findings highlight the zoonotic potential of Bartonella spp circulating among small mammals and reinforce the need for enhanced surveillance and a One Health approach to understanding their transmission dynamics.

5. Conclusion

This systematic review and meta-analysis provide a comprehensive overview of the prevalence and genetic diversity of Bartonella spp in small mammals across Europe. The estimated pooled prevalence of Bartonella infection was 30%, with notable regional variations. This suggests that multiple ecological and epidemiological factors such as vector distribution, host density, and environmental conditions—collectively influence Bartonella transmission dynamics. Furthermore, a high diversity of Bartonella species was detected, with 21 identified species, nine of which are confirmed human pathogens. This finding highlights the potential public health risk posed by small mammals, particularly in regions with high Bartonella prevalence and frequent human-animal- vector interactions. Our results reinforce the importance of ongoing surveillance of Bartonella spp in small mammal populations. Enhanced diagnostic efforts, including molecular characterization of emerging strains, will be crucial for assessing spillover risks and implementing effective One Health strategies to mitigate zoonotic transmission. Future studies should investigate the drivers of Bartonella prevalence, including climatic factors, vector ecology, and host behavior, to better predict and prevent potential outbreaks in both animal and human populations.

CRediT authorship contribution statement

Aya A.K. Zarea: Writing – review & editing, Writing – original draft, Visualization, Validation, Software, Methodology, Formal analysis, Data curation, Conceptualization. Younes Laidoudi: Writing – review & editing, Investigation. Amienwanlen E. Odigie: Writing – review & editing, Data curation. Daniela Mrenoshki: Writing – review & editing, Data curation. Maria Francesca Iulietto: Writing – review & editing, Investigation. Grazia Greco: Writing – review & editing, Investigation. Roberto Condoleo: Writing – review & editing, Supervision, Methodology, Investigation, Conceptualization.

Declaration of competing interest

All authors declare that they have no conflicts of interest.

Acknowledgments

This study has been carried out within the framework of the COST Action CA21170 ‘Prevention, anticipation and mitigation of tick-borne disease risk applying the DAMA protocol’ (PRAGMATICK).

Footnotes

Appendix A

Supplementary data to this article can be found online at https://doi.org/10.1016/j.onehlt.2025.101263.

Appendix A. Supplementary data

Supplementary material

mmc1.docx (78.6KB, docx)

Data availability

Data will be made available on request.

References

  • 1.Greco G., Zarea A.A.K., Sgroi G., Tempesta M., D’Alessio N., Lanave G., Bezerra-Santos M.A., Iatta R., Veneziano V., Otranto D., Chomel B. Zoonotic Bartonella species in Eurasian wolves and other free-ranging wild mammals from Italy. Zoonoses Public Health. 2021;68:316–326. doi: 10.1111/zph.12827. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 2.Zarea A.A.K., Tempesta M., Odigie A.E., Mrenoshki D., Fanelli A., Martella V., Decaro N., Greco G. Cats and Dogs: A Systematic Review and Meta-Analysis, Transboundary and Emerging Diseases. Vol. 2023. 2023. The Global Molecular Prevalence of Bartonella spp; pp. 1–19. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Okaro U., Addisu A., Casanas B., Anderson B. Bartonella Species, an Emerging Cause of Blood-Culture-Negative Endocarditis. Clin. Microbiol. Rev. 2017;30:709–746. doi: 10.1128/CMR.00013-17. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 4.Gutiérrez R., Krasnov B., Morick D., Gottlieb Y., Khokhlova I.S., Harrus S. Bartonella Infection in Rodents and Their Flea Ectoparasites: An Overview. Vector-Borne and Zoonotic Diseases. 2015;15:27–39. doi: 10.1089/vbz.2014.1606. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 5.Krügel M., Król N., Kempf V.A.J., Pfeffer M., Obiegala A. Emerging rodent-associated Bartonella: a threat for human health? Parasit. Vectors. 2022;15:113. doi: 10.1186/s13071-022-05162-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Jacomo V., Kelly P.J., Raoult D. Natural History of Bartonella Infections (an Exception to Koch’s Postulate) Clin. Vaccine Immunol. 2002;9:8–18. doi: 10.1128/CDLI.9.1.8-18.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 7.Buffet J.-P., Kosoy M., Vayssier-Taussat M. Natural History of Bartonella -Infecting Rodents in Light of New Knowledge on Genomics, Diversity and Evolution. Future Microbiol. 2013;8:1117–1128. doi: 10.2217/fmb.13.77. [DOI] [PubMed] [Google Scholar]
  • 8.Chomel B.B., Boulouis H.-J., Maruyama S., Breitschwerdt E.B. Bartonella Spp. in Pets and Effect on Human Health. Emerg. Infect. Dis. 2006;12:389–394. doi: 10.3201/eid1203.050931. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 9.Gutiérrez R., Shalit T., Markus B., Yuan C., Nachum-Biala Y., Elad D., Harrus S. Bartonella kosoyi sp. nov. and Bartonella krasnovii sp. nov., two novel species closely related to the zoonotic Bartonella elizabethae, isolated from black rats and wild desert rodent-fleas. Int. J. Syst. Evol. Microbiol. 2020;70:1656–1665. doi: 10.1099/ijsem.0.003952. [DOI] [PubMed] [Google Scholar]
  • 10.Lei B.R., Olival K.J. Contrasting Patterns in Mammal–Bacteria Coevolution: Bartonella and Leptospira in Bats and Rodents. PLoS Negl. Trop. Dis. 2014;8 doi: 10.1371/journal.pntd.0002738. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Kosoy M., Mckee C., Albayrak L., Fofanov Y. Genotyping of Bartonella bacteria and their animal hosts: current status and perspectives. Parasitology. 2018;145:543–562. doi: 10.1017/S0031182017001263. [DOI] [PubMed] [Google Scholar]
  • 12.European Centre for Disease Prevention and Control . European Centre for Disease Prevention and Control; Stockholm: 2023. Zoonotic diseases and foodborne outbreaks on the rise, but still below pre-pandemic levels.https://www.ecdc.europa.eu/en/news-events/zoonotic-diseases-and-foodborne-outbreaks-rise-still-below-pre-pandemic-levels (accessed November 16, 2023) [Google Scholar]
  • 13.Chomel B.B., Boulouis H.-J., Breitschwerdt E.B., Kasten R.W., Vayssier-Taussat M., Birtles R.J., Koehler J.E., Dehio C. Ecological fitness and strategies of adaptation of Bartonella species to their hosts and vectors. Vet. Res. 2009;40:29. doi: 10.1051/vetres/2009011. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Zarea A.A.K., Bezerra-Santos M.A., Nguyen V., Colella V., Dantas-Torres F., Halos L., Beugnet F., Tempesta M., Otranto D., Greco G. Occurrence and bacterial loads of Bartonella and haemotropic Mycoplasma species in privately owned cats and dogs and their fleas from East and Southeast Asia. Zoonoses Public Health. 2022;69:704–720. doi: 10.1111/zph.12959. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Zarea A.A.K., Tempesta M., Fouad E.A., Ndiana L.A., Mahmoud M.S., Mrenoshki D., Martella V., Decaro N., Chomel B., Greco G. Prevalence of Bartonella spp., haemotropic Mycoplasma spp. and others vector-borne pathogens in private-owned dogs and cats, Egypt. Acta Trop. 2023;240 doi: 10.1016/j.actatropica.2023.106857. [DOI] [PubMed] [Google Scholar]
  • 16.Majerová K., Gutiérrez R., Fonville M., Hönig V., Papežík P., Hofmannová L., Lesiczka P.M., Nachum-Biala Y., Růžek D., Sprong H., Harrus S., Modrý D., Votýpka J. Hedgehogs and Squirrels as Hosts of Zoonotic Bartonella Species. Pathogens. 2021;10:686. doi: 10.3390/pathogens10060686. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Bai Y., Kosoy M.Y., Diaz M.H., Winchell J., Baggett H., Maloney S.A., Boonmar S., Bhengsri S., Sawatwong P., Peruski L.F. Bartonella vinsonii subsp. arupensis in Humans, Thailand. Emerg. Infect. Dis. 2012;18:989–991. doi: 10.3201/eid1806.111750. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Breitschwerdt E.B., Maggi R.G., Duncan A.W., Nicholson W.L., Hegarty B.C., Woods C.W. Bartonella Species in Blood of Immunocompetent Persons with Animal and Arthropod Contact. Emerg. Infect. Dis. 2007;13:938–941. doi: 10.3201/eid1306.061337. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 19.Breitschwerdt E.B., Maggi R.G., Nicholson W.L., Cherry N.A., Woods C.W. Bartonella sp. Bacteremia in Patients with Neurological and Neurocognitive Dysfunction. J. Clin. Microbiol. 2008;46:2856–2861. doi: 10.1128/JCM.00832-08. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 20.Corral J., Manríquez Robles A., Toussaint Caire S., Hernández-Castro R., Moreno-Coutiño G. First Report of Bacillary Angiomatosis by Bartonella elizabethae in an HIV-Positive Patient. Am. J. Dermatopathol. 2019;41:750–753. doi: 10.1097/DAD.0000000000001439. [DOI] [PubMed] [Google Scholar]
  • 21.Huchon D., Madsen O., Sibbald M.J.J.B., Ament K., Stanhope M.J., Catzeflis F., De Jong W.W., Douzery E.J.P. Rodent Phylogeny and a Timescale for the Evolution of Glires: Evidence from an Extensive Taxon Sampling Using Three Nuclear Genes. Mol. Biol. Evol. 2002;19:1053–1065. doi: 10.1093/oxfordjournals.molbev.a004164. [DOI] [PubMed] [Google Scholar]
  • 22.Wilson D.E., Reeder D.M. 3rd ed. Johns Hopkins University Press; Baltimore: 2005. Mammal Species of the World: A Taxonomic and Geographic Reference. [Google Scholar]
  • 23.Jurišić A., Ćupina A.I., Kavran M., Potkonjak A., Ivanović I., Bjelić-Čabrilo O., Meseldžija M., Dudić M., Poljaković-Pajnik L., Vasić V. Surveillance Strategies of Rodents in Agroecosystems. Forestry and Urban Environments, Sustainability. 2022;14:9233. doi: 10.3390/su14159233. [DOI] [Google Scholar]
  • 24.Meerburg B.G., Singleton G.R., Kijlstra A. Rodent-borne diseases and their risks for public health. Crit. Rev. Microbiol. 2009;35:221–270. doi: 10.1080/10408410902989837. [DOI] [PubMed] [Google Scholar]
  • 25.Han B.A., Schmidt J.P., Bowden S.E., Drake J.M. Rodent reservoirs of future zoonotic diseases. Proc. Natl. Acad. Sci. USA. 2015;112:7039–7044. doi: 10.1073/pnas.1501598112. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Paziewska A., Harris P.D., Zwolińska L., Bajer A., Siński E. Recombination Within and Between Species of the Alpha Proteobacterium Bartonella Infecting Rodents. Microb. Ecol. 2011;61:134–145. doi: 10.1007/s00248-010-9735-1. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Bown K.J., Bennett M., Begon M. Flea-borne Bartonella grahamii and Bartonella taylorii in Bank Voles. Emerg. Infect. Dis. 2004;10:684–687. doi: 10.3201/eid1004.030455. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 28.Kosoy M., Murray M., Gilmore R.D., Bai Y., Gage K.L. Bartonella Strains from Ground Squirrels Are Identical to Bartonella washoensis Isolated from a Human Patient. J. Clin. Microbiol. 2003;41:645–650. doi: 10.1128/JCM.41.2.645-650.2003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Kandelaki G., Malania L., Bai Y., Chakvetadze N., Katsitadze G., Imnadze P., Nelson C., Harrus S., Kosoy M. Human Lymphadenopathy Caused by Ratborne Bartonella, Tbilisi, Georgia. Emerg. Infect. Dis. 2016;22:544–546. doi: 10.3201/eid2203.151823. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 30.Page M.J., Moher D., Bossuyt P.M., Boutron I., Hoffmann T.C., Mulrow C.D., Shamseer L., Tetzlaff J.M., Akl E.A., Brennan S.E., Chou R., Glanville J., Grimshaw J.M., Hróbjartsson A., Lalu M.M., Li T., Loder E.W., Mayo-Wilson E., McDonald S., McGuinness L.A., Stewart L.A., Thomas J., Tricco A.C., Welch V.A., Whiting P., McKenzie J.E. PRISMA 2020 explanation and elaboration: updated guidance and exemplars for reporting systematic reviews. BMJ. 2021 doi: 10.1136/bmj.n160. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 31.Musser G. rodent. Encyclopedia Britannica. 2024 https://www.britannica.com/animal/rodent [Google Scholar]
  • 32.Munn Z., Barker T.H., Moola S., Tufanaru C., Stern C., McArthur A., Stephenson M., Aromataris E. JBI Database of Systematic Reviews and Implementation Reports Publish Ahead of Print. 2019. Methodological quality of case series studies: an introduction to the JBI critical appraisal tool. [DOI] [PubMed] [Google Scholar]
  • 33.Barendregt J.J., Doi S.A., Lee Y.Y., Norman R.E., Vos T. Meta-analysis of prevalence. J. Epidemiol. Community Health. 2013;67:974–978. doi: 10.1136/jech-2013-203104. [DOI] [PubMed] [Google Scholar]
  • 34.Negeri Z.F., Shaikh M., Beyene J. Bivariate random-effects meta-analysis models for diagnostic test accuracy studies using arcsine-based transformations. Biom. J. 2018;60:827–844. doi: 10.1002/bimj.201700101. [DOI] [PubMed] [Google Scholar]
  • 35.Condoleo R., Campagna M.C., Zarea A., Briganti P., D’Amici L., Iulietto M.F. Prevalence of Listeria monocytogenes in mozzarella cheese: A systematic review and meta-analysis. J. Dairy Sci. 2025 doi: 10.3168/jds.2025-26815. S0022030225007817. [DOI] [PubMed] [Google Scholar]
  • 36.Higgins J.P.T., Thompson S.G. Quantifying heterogeneity in a meta-analysis. Stat. Med. 2002;21:1539–1558. doi: 10.1002/sim.1186. [DOI] [PubMed] [Google Scholar]
  • 37.Kosoy M.Y. Ecological Associations between bacteria of the genus Bartonella and mammals. Biol. Bull. 2010;37:716–724. [Google Scholar]
  • 38.Birtles R.J., Hazel S.M., Bennett M., Bown K., Raoult D., Begon M. Longitudinal monitoring of the dynamics of infections due to Bartonella species in UK woodland rodents. Epidemiol. Infect. 2001;126:323–329. doi: 10.1017/S095026880100526X. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 39.Bown K.J., Ellis B.A., Birtles R.J., Durden L.A., Lello J., Begon M., Bennett M. New World origins for haemoparasites infecting United Kingdom grey squirrels (Sciurus carolinensis), as revealed by phylogenetic analysis of bartonella infecting squirrel populations in England and the United States. Epidemiol. Infect. 2002;129:647–653. doi: 10.1017/S0950268802007768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Holmberg M., Mills J.N., Mcgill S., Benjamin G., Ellis B.A. Bartonella infection in sylvatic small mammals of central Sweden. Epidemiol. Infect. 2003;130:149–157. doi: 10.1017/S0950268802008075. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 41.Saengsawang P., Morand S., Desquesnes M., Yangtara S., Inpankaew T. Molecular Detection of Bartonella Species in Rodents Residing in Urban and Suburban Areas of Central Thailand. Microorganisms. 2021;9:2588. doi: 10.3390/microorganisms9122588. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Tahmasebi Ashtiani Z., Bagheri Amiri F., Ahmadinezhad M., Mostafavi E., Esmaeili S. Bartonellosis in World Health Organization Eastern Mediterranean Region, a systematic review and meta-analysis. Eur. J. Pub. Health. 2025;35:i48–i54. doi: 10.1093/eurpub/ckae123. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Mhlanga T.A., Chitanga S., Matthee S., Malatji M.P., Mukaratirwa S. Prevalence and genetic diversity of Bartonella spp. in wild small mammals from South Africa. Appl. Environ. Microbiol. 2024;90 doi: 10.1128/aem.00842-24. e00842-24. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Szewczyk T., Werszko J., Slivinska K., Laskowski Z., Karbowiak G. Rodents in Chernobyl Exclusion Zone, Ukraine, Acta Parasit. Vol. 66. 2021. Molecular Detection of Bartonella spp; pp. 222–227. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Tadin A., Tokarz R., Markotić A., Margaletić J., Turk N., Habuš J., Svoboda P., Vucelja M., Desai A., Jain K., Lipkin W.I. Molecular Survey of Zoonotic Agents in Rodents and Other Small Mammals in Croatia. The American Society of Tropical Medicine and Hygiene. 2016;94:466–473. doi: 10.4269/ajtmh.15-0517. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Mediannikov O., Ivanov L., Zdanovskaya N., Vysochina N., Fournier P., Tarasevich I., Raoult D. Molecular Screening of Bartonella Species in Rodents from the Russian Far East. Ann. N. Y. Acad. Sci. 2005;1063:308–311. doi: 10.1196/annals.1355.049. [DOI] [PubMed] [Google Scholar]
  • 47.Malania L., Bai Y., Osikowicz L.M., Tsertsvadze N., Katsitadze G., Imnadze P., Kosoy M. Prevalence and Diversity of Bartonella Species in Rodents from Georgia (Caucasus) The American Society of Tropical Medicine and Hygiene. 2016;95:466–471. doi: 10.4269/ajtmh.16-0041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 48.Markov A.P., Lopyrev I.V., Irkhin A.I., Khliap L.A., Levitskiĭ S.A., Kirillov M.I., Manuvera V.A., Il’ina T.S., Pokrovskaia M.S., Aleshkin G.I., Bashkirov V.N., Smirnov G.B., Kosoĭ M. Wild small mammals are the reservoir hosts of the Bartonella genus bacteria in the south of Moscow region. Mol. Gen. Mikrobiol. Virusol. 2006:8–13. [PubMed] [Google Scholar]
  • 49.Jeske K., Herzig-Straschil B., Răileanu C., Kunec D., Tauchmann O., Emirhar D., Schmidt S., Trimpert J., Silaghi C., Heckel G., Ulrich R.G., Drewes S. Zoonotic pathogen screening of striped field mice (Apodemus agrarius) from Austria. Transbound. Emerg. Dis. 2022;69:886–890. doi: 10.1111/tbed.14015. [DOI] [PubMed] [Google Scholar]
  • 50.Haring V., Jacob J., Walther B., Trost M., Stubbe M., Mertens-Scholz K., Melzer F., Scuda N., Gentil M., Sixl W., Schäfer T., Stanko M., Wolf R., Pfeffer M., Ulrich R.G., Obiegala A. White-Toothed Shrews (Genus Crocidura): Potential Reservoirs for Zoonotic Leptospira spp. and Arthropod-Borne Pathogens? Pathogens. 2023;12:781. doi: 10.3390/pathogens12060781. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 51.Obiegala A., Heuser E., Ryll R., Imholt C., Fürst J., Prautsch L., Plenge-Bönig A., Ulrich R.G., Pfeffer M. Norway and black rats in Europe: potential reservoirs for zoonotic arthropod-borne pathogens? Pest Manag. Sci. 2019;75:1556–1563. doi: 10.1002/ps.5323. [DOI] [PubMed] [Google Scholar]
  • 52.Greco G., Brianti E., Buonavoglia C., Carelli G., Pollmeier M., Schunack B., Dowgier G., Capelli G., Dantas-Torres F., Otranto D. Effectiveness of a 10% imidacloprid/4.5% flumethrin polymer matrix collar in reducing the risk of Bartonella spp. infection in privately owned cats. Parasit. Vectors. 2019;12:69. doi: 10.1186/s13071-018-3257-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.Bezerra-Santos M.A., Dantas-Torres F., Benelli G., Otranto D. Emerging parasites and vectors in a rapidly changing world: from ecology to management. Acta Trop. 2023;238 doi: 10.1016/j.actatropica.2022.106746. [DOI] [PubMed] [Google Scholar]
  • 54.Guccion J.G., Gibert C.L., Ortega L.G., Hadfield T.L. Cat Scratch Disease and Acquired Immunodeficiency Disease: Diagnosis by Transmission Electron Microscopy. Ultrastruct. Pathol. 1996;20:195–202. doi: 10.3109/01913129609016315. [DOI] [PubMed] [Google Scholar]
  • 55.Arias-Stella J., Lieberman P.H., Erlandson R.A., Arias-Stella J. Histology, Immunohistochemistry, and Ultrastructure of the Verruga in Carrionʼs Disease. Am. J. Surg. Pathol. 1986;10:595–610. doi: 10.1097/00000478-198609000-00002. [DOI] [PubMed] [Google Scholar]
  • 56.Han P.-Y., Xu F.-H., Tian J.-W., Zhao J.-Y., Yang Z., Kong W., Wang B., Guo L.-J., Zhang Y.-Z. Molecular Prevalence, Genetic Diversity, and Tissue Tropism of Bartonella Species in Small Mammals from Yunnan Province, China. Animals. 2024;14:1320. doi: 10.3390/ani14091320. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Maas M., Glorie J., Dam-Deisz C., De Vries A., Franssen F.F.J., Jaarsma R.I., Hengeveld P.D., Dierikx C.M., Van Der Giessen J.W.B., Opsteegh M. Zoonotic Pathogens in Eurasian Beavers (Castor fiber) in the Netherlands. J. Wildl. Dis. 2022;58 doi: 10.7589/JWD-D-21-00097. [DOI] [PubMed] [Google Scholar]
  • 58.Markova A., Puzachenko A. Preliminary Analysis of European Small Mammal Faunas of the Eemian Interglacial: Species Composition and Species Diversity at a Regional Scale. Quaternary. 2018;1:9. doi: 10.3390/quat1020009. [DOI] [Google Scholar]
  • 59.Kosoy M., Mandel E., Green D., Marston E., Childs J. Prospective Studies of Bartonella of Rodents. Part I. Demographic and Temporal Patterns in Population Dynamics. Vector-Borne and Zoonotic Diseases. 2004;4:285–295. doi: 10.1089/vbz.2004.4.285. [DOI] [PubMed] [Google Scholar]
  • 60.Rodríguez-Pastor R., Escudero R., Lambin X., Vidal M.D., Gil H., Jado I., Rodríguez-Vargas M., Luque-Larena J.J., Mougeot F. Zoonotic pathogens in fluctuating common vole (Microtus arvalis) populations: occurrence and dynamics. Parasitology. 2019;146:389–398. doi: 10.1017/S0031182018001543. [DOI] [PubMed] [Google Scholar]
  • 61.Cevidanes A., Altet L., Chirife A.D., Proboste T., Millán J. Drivers of Bartonella infection in micromammals and their fleas in a Mediterranean peri-urban area. Vet. Microbiol. 2017;203:181–188. doi: 10.1016/j.vetmic.2017.03.023. [DOI] [PubMed] [Google Scholar]
  • 62.Telfer S., Clough H.E., Birtles R.J., Bennett M., Carslake D., Helyar S., Begon M. Ecological differences and coexistence in a guild of microparasites: bartonella in wild rodents. Ecology. 2007;88:1841–1849. doi: 10.1890/06-1004.1. [DOI] [PubMed] [Google Scholar]
  • 63.Krasnov B.R., Morand S., Hawlena H., Khokhlova I.S., Shenbrot G.I. Sex-biased parasitism, seasonality and sexual size dimorphism in desert rodents. Oecologia. 2005;146:209–217. doi: 10.1007/s00442-005-0189-y. [DOI] [PubMed] [Google Scholar]
  • 64.Engel P., Salzburger W., Liesch M., Chang C.-C., Maruyama S., Lanz C., Calteau A., Lajus A., Médigue C., Schuster S.C., Dehio C. Parallel Evolution of a Type IV Secretion System in Radiating Lineages of the Host-Restricted Bacterial Pathogen Bartonella. PLoS Genet. 2011;7 doi: 10.1371/journal.pgen.1001296. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 65.Jiyipong T., Jittapalapong S., Morand S., Rolain J.-M. Bartonella species in small mammals and their potential vectors in Asia. Asian Pac. J. Trop. Biomed. 2014;4:757–767. doi: 10.12980/APJTB.4.2014C742. [DOI] [Google Scholar]
  • 66.Berglund E.C., Ellegaard K., Granberg F., Xie Z., Maruyama S., Kosoy M.Y., Birtles R.J., Andersson S.G.E. Rapid diversification by recombination in Bartonella grahamii from wild rodents in Asia contrasts with low levels of genomic divergence in Northern Europe and America: genomic diversity of bartonella grahamii. Mol. Ecol. 2010;19:2241–2255. doi: 10.1111/j.1365-294X.2010.04646.x. [DOI] [PubMed] [Google Scholar]
  • 67.Paziewska A., Siński E., Harris P.D. Recombination, Diversity and Allele Sharing of Infectivity Proteins Between Bartonella Species from Rodents. Microb. Ecol. 2012;64:525–536. doi: 10.1007/s00248-012-0033-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 68.Spitalská E., Boldis V., Kostanová Z., Kocianová E., Stefanidesová K. Incidence of various tick-borne microorganisms in rodents and ticks of central Slovakia. Acta Virol. 2008;52:175–179. [PubMed] [Google Scholar]
  • 69.Kraljik J., Paziewska-Harris A., Miklisová D., Blaňarová L., Mošanský L., Bona M., Stanko M. Genetic diversity of Bartonella genotypes found in the striped field mouse (Apodemus agrarius) in Central Europe. Parasitology. 2016;143:1437–1442. doi: 10.1017/S0031182016000962. [DOI] [PubMed] [Google Scholar]
  • 70.Lipatova I., Paulauskas A., Puraite I., Radzijevskaja J., Balciauskas L., Gedminas V. Bartonella infection in small mammals and their ectoparasites in Lithuania. Microbes Infect. 2015;17:884–888. doi: 10.1016/j.micinf.2015.08.013. [DOI] [PubMed] [Google Scholar]
  • 71.Gil H., García-Esteban C., Barandika J.F., Peig J., Toledo A., Escudero R., Jado I., Rodríguez-Vargas M., García-Amil C., Lobo B., Roales P., Rodríguez-Moreno I., Olmeda A.S., García-Pérez A.L., Anda P. Variability of Bartonella Genotypes among Small Mammals in Spain. Appl. Environ. Microbiol. 2010;76:8062–8070. doi: 10.1128/AEM.01963-10. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 72.Demoncheaux J.-P., Medkour H., Louni M., Laugier L., Pasqualini C., Fenollar F., Davoust B., Mediannikov O. Detection of Potential Zoonotic Bartonella Species in African Giant Rats (Cricetomys gambianus) and Fleas from an Urban Area in Senegal. Microorganisms. 2022;10:489. doi: 10.3390/microorganisms10030489. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 73.Kamani J., Morick D., Mumcuoglu K.Y., Harrus S. Prevalence and Diversity of Bartonella Species in Commensal Rodents and Ectoparasites from Nigeria. West Africa, PLoS Negl Trop Dis. 2013;7 doi: 10.1371/journal.pntd.0002246. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 74.Cui Hong A.N., Bao Bao C.H.E.N., Wen L.Y.U., Shou Min N.I.E., Sheng Zhen L.I., Suo Ping F.A.N., Yang Xin S.U.N., Jin Ren L.I.U., Dong Mei L.I., Ji Ru X.U. Bartonella Species Investigated among Rodents from Shaanxi Province of China. 2020;33 doi: 10.3967/bes2020.028. 201_2015. [DOI] [PubMed] [Google Scholar]
  • 75.Sepúlveda-García P., Rubio A.V., Salgado R., Riquelme M., Bonacic C., Canales N., Müller A. Molecular detection and characterization of Bartonella spp. in rodents from central and southern Chile, with emphasis on introduced rats (Rattus spp.) Comp. Immunol. Microbiol. Infect. Dis. 2023;100 doi: 10.1016/j.cimid.2023.102026. [DOI] [PubMed] [Google Scholar]
  • 76.Müller A., Gutiérrez R., Seguel M., Monti G., Otth C., Bittencourt P., Sepúlveda P., Alabí A., Nachum-Biala Y., Harrus S. Molecular survey of Bartonella spp. in rodents and fleas from Chile. Acta Trop. 2020;212 doi: 10.1016/j.actatropica.2020.105672. [DOI] [PubMed] [Google Scholar]
  • 77.Peterson A.C., Ghersi B.M., Alda F., Firth C., Frye M.J., Bai Y., Osikowicz L.M., Riegel C., Lipkin W.I., Kosoy M.Y., Blum M.J. Rodent-Borne Bartonella Infection Varies According to Host Species Within and Among Cities. EcoHealth. 2017;14:771–782. doi: 10.1007/s10393-017-1291-4. [DOI] [PubMed] [Google Scholar]
  • 78.Graham-Smith G.S. A New Form of Parasite found in the Red Blood Corpuscles of Moles. Epidemiol. Infect. 1905;5:453–459. doi: 10.1017/S0022172400006768. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 79.Birtles R.J., Harrison T.G., Saunders N.A., Molyneux D.H. Proposals To Unify the Genera Grahamella and Bartonella, with Descriptions of Bartonella talpae comb, nov., Bartonella peromysci comb. nov., and Three New Species, Bartonella grahamii sp. nov., Bartonella taylorii sp. nov., and Bartonella doshiae sp. nov. Int. J. Syst. Bacteriol. 1995;45:1–8. doi: 10.1099/00207713-45-1-1. [DOI] [PubMed] [Google Scholar]
  • 80.Heller R., Riegel P., Hansmann Y., Delacour G., Bermond D., Dehio C., Lamarque F., Monteil H., Chomel B., Piemont Y. Bartonella tribocorum sp. nov., a new Bartonella species isolated from the blood of wild rats. Int. J. Syst. Bacteriol. 1998;48:1333–1339. doi: 10.1099/00207713-48-4-1333. [DOI] [PubMed] [Google Scholar]
  • 81.Tea A., Alexiou-Daniel S., Papoutsi A., Papa A., Antoniadis A. Bartonella Species Isolated from Rodents, Greece. Emerg. Infect. Dis. 2004;10:963–964. doi: 10.3201/eid1005.030430. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 82.Márquez F.J., Rodríguez-Liébana J.J., Pachón-Ibáñez M.E., Docobo-Pérez F., Hidalgo-Fontiveros A., Bernabeu-Wittel M., Muniain M.A., Pachón J. Molecular Screening of Bartonella Species in Rodents from South Western Spain. Vector-Borne and Zoonotic Diseases. 2008;8:695–700. doi: 10.1089/vbz.2007.0257. [DOI] [PubMed] [Google Scholar]
  • 83.Bartoš O., Klimešová B., Volfová K., Chmel M., Dresler J., Pajer P., Kabíčková H., Adamík P., Modrý D., Fučíková A.M., Votýpka J. Two novel Bartonella (sub)species isolated from edible dormice (Glis glis): hints of cultivation stress-induced genomic changes. Front. Microbiol. 2023;14:1289671. doi: 10.3389/fmicb.2023.1289671. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 84.Špitalská E., Minichová L., Kocianová E., Škultéty Ľ., Mahríková L., Hamšíková Z., Slovák M., Kazimírová M. Diversity and prevalence of Bartonella species in small mammals from Slovakia, Central Europe. Parasitol. Res. 2017;116:3087–3095. doi: 10.1007/s00436-017-5620-x. [DOI] [PubMed] [Google Scholar]
  • 85.Knap N., Duh D., Birtles R., Trilar T., Petrovec M., AvÅ¡iÄ-Åupanc T. Molecular detection of Bartonella species infecting rodents in Slovenia. FEMS Immunology & Medical Microbiology. 2007;50:45–50. doi: 10.1111/j.1574-695X.2007.00226.x. [DOI] [PubMed] [Google Scholar]
  • 86.Buffet J.-P., Marsot M., Vaumourin E., Gasqui P., Masséglia S., Marcheteau E., Huet D., Chapuis J.-L., Pisanu B., Ferquel E., Halos L., Vourc’h G., Vayssier-Taussat M. Co-infection of Borrelia afzelii and Bartonella spp. in bank voles from a suburban forest. Comp. Immunol. Microbiol. Infect. Dis. 2012;35:583–589. doi: 10.1016/j.cimid.2012.07.002. [DOI] [PubMed] [Google Scholar]
  • 87.Foucault C., Brouqui P., Raoult D. Bartonella quintana Characteristics and Clinical Management. Emerg. Infect. Dis. 2006;12:217–223. doi: 10.3201/eid1202.050874. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 88.Fenollar F., Sire S., Wilhelm N., Raoult D. Bartonella vinsonii subsp. arupensis as an Agent of Blood Culture-Negative Endocarditis in a Human. J. Clin. Microbiol. 2005;43:945–947. doi: 10.1128/JCM.43.9.4923.2005. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 89.Vayssier-Taussat M., Moutailler S., Féménia F., Raymond P., Croce O., La Scola B., Fournier P.-E., Raoult D. Identification of Novel Zoonotic Activity of Bartonella spp., France. Emerg. Infect. Dis. 2016;22:457–462. doi: 10.3201/eid2203.150269. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 90.Kerkhoff F.T., Bergmans A.M.C., Van Der Zee A., Rothova A. Demonstration of Bartonella grahamii DNA in Ocular Fluids of a Patient with Neuroretinitis. J. Clin. Microbiol. 1999;37:4034–4038. doi: 10.1128/JCM.37.12.4034-4038.1999. [DOI] [PMC free article] [PubMed] [Google Scholar]

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