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. 2024 Jul 22;10(15):e35009. doi: 10.1016/j.heliyon.2024.e35009

Prevalence and genetic diversity of rodent-associated Bartonella in Hulunbuir border regions, China

Xuexia Wen a,b,1, Yaoqi Fang a,b,1, Feng Jiang a,b,1, Yixin Wang a,b, Qijun Chen a,b, Zeliang Chen a,b, Yuhan Wu a,b, Qing Xin a,b, Xiaohu Han a,b,⁎, Hua Deng c,⁎⁎
PMCID: PMC11334643  PMID: 39166044

Abstract

Bartonella spp. are globally distributed gram-negative facultative intracellular bacteria that infect a wide range of hosts. Rodents are natural reservoirs of many Bartonella species, some of which are also pathogenic to humans. The rapid development of transportation and tourism has highlighted the risk of Bartonella transmission to humans. Thus, it is essential to maintain surveillance of Bartonella spp. infections in rodents. In China, Bartonella spp. infections have been monitored in various areas; however, these have not included the Hulunbuir border regions. In the present study, we monitored the prevalence and genetics of rodent-associated Bartonella spp. in the Hulunbuir border regions. Eleven rodent species were captured at five ports. Eight species were confirmed as Bartonella-positive using quantitative PCR assay, with an overall positivity rate of 20.05 %. Lasiopodomys brandtii was the predominant rodent species captured for Bartonella detection. Sequencing and phylogenetic analysis (using the maximum likelihood method) revealed the presence of three Bartonella species in these rodents, including two pathogenic to humans, namely, Bartonella alsatica and Bartonella grahamii. B. grahamii was the predominant Bartonella species identified in the rodents. Taken together, these results highlight the prevalence and genetic diversity of Bartonella spp. in rodents in the Hulunbuir border regions, indicating the need for risk assessment of human spillover.

Keywords: Bartonella, Rodents, Epidemiology, Genetic diversity, Hulunbuir border regions

Highlights

  • •

    Eight of the eleven captured rodent species were Bartonella-positive, with an overall positivity rate of 20.05 %.

  • •

    Lasiopodomys brandtii was the predominant rodent species captured for the detection of Bartonella.

  • •

    Three Bartonella species, including two pathogenic to humans, were detected in the captured rodents.

  • •

    Bartonella grahamii was the predominant Bartonella species identified in the captured rodents.

1. Introduction

Bartonella spp. are gram-negative facultative intracellular bacteria, first identified in patients in Peru in 1909 and classified as rickettsia before 1993 [1]. Bartonella spp. belong to the group Alphaproteobacteria of the family Bartonellaceae. The host animals of Bartonella spp., including Rodentia, Chiroptera, Artiodactyla, Lagomorpha, Carnivora, and Insectivora are diverse [2]. Bartonella spp. mainly parasitize red blood cells or vascular endothelial cells and are transmitted by blood-sucking arthropods, including sandflies, fleas, lice, mites, and ticks. Humans can get infected with Bartonella through bites by blood-sucking arthropods, or through traumatic exposure to contaminants [3]. To date, at least 50 recognized and 10 candidate Bartonella species have been identified, of which more than 18 have been identified as zoonotic species [[4], [5], [6]].

Rodents belong to the order Rodentia and are considered natural reservoirs of Bartonella [5,7]. With their vast diversity and robust reproductive capabilities, rodents are ubiquitous and remarkably adaptable to a wide range of natural environments. As carriers of numerous pathogenic microorganisms, and with their close interactions with humans and other animals, rodents have become a focal point in the study and prevention of various environmental diseases [8,9]. In 1940, Bartonella vinsonii subsp. arupensis was first detected in rodents in the United States [10]. Approximately half a century later, Bartonella infection was detected in rodents in the UK, followed by Portugal [7], Canada [11], Japan [12], Thailand [13,14], China [15], Australia [16], Germany [17], Malaysia [18], India [19], and Switzerland [20]. Bartonella-positive rates in Portugal, Thailand, China, Malaysia, India, and other regions were >50 % [7,[13], [14], [15],18,19]. Currently, the members within genus Bartonella have been isolated from more than 98 rodent species in seven families, and approximately 22 rodent-related Bartonella and their subspecies have been identified [21]. Eight species or subspecies of rodent-related Bartonella, namely Bartonella alsatica, Bartonella doshiae, Bartonella elizabethae, Bartonella grahamii, Bartonella rattimassiliensis, Bartonella tribocorun, Bartonella vinsoni subsp.vinsonii, and B. vinsoni subsp.arupensis, have been reported to be pathogenic to humans and can cause myocarditis, endocarditis, lymphadenitis, hepatitis, and other diseases [5]. Therefore, investigating the prevalence of rodent-related Bartonella infection is of great significance for controlling Bartonella infection in humans.

China is located in East Asia along the west coast of the Pacific Ocean, with a vast territory and complex and diverse terrain. Rodents are widely distributed throughout China. Investigations into rodent infection with Bartonella in China began in 1999 when Ying et al. isolated B. elizabathae from rodent blood [15]. Subsequently, studies were carried out in 15 provinces, including Yunnan [22], Heilongjiang [23], Taiwan [24], Zhejiang [25], Fujian [26], Hebei [27], Shanxi [28,29], Guangdong [30], Jiangxi [31], Guizhou [32], and Sichuan [33]. Hulunbuir is situated to the south of Russia and the east of Mongolia. Arihashate Port, Ebudug Port, Arxan Port, Heishantou Port, and Manzhouli Port are important border crossings in this region. Rodents have a strong tendency to move along the border and can freely migrate across it, which poses a significant risk for the introduction and spread of diseases transmitted by rodents [34]. Hulunbuir is one of the most beautiful grasslands in China. With 80,000 square kilometers of natural grassland, it is one of the four major grasslands worldwide and an important part of the eastern Mongolian grassland, creating favorable conditions for the growth and reproduction of rodents [35]. In recent years, with the continuous development of tourism and animal husbandry industries in Hulunbuir, human activities have gradually expanded, giving rise to greater opportunities for direct or indirect contact with rodents, increasing the risk of transmission of bartonellosis [36]. Therefore, in the present study, we explored the prevalence and genetics of rodent-associated Bartonella species in the Hulunbuir border regions to provide basic data for understanding the risk of zoonotic spillover and control of Bartonella infection in humans.

2. Materials and methods

2.1. Ethics statement

The protocols were approved by the Institutional Ethics Committee of Shenyang Agricultural University (No. 2021040701). All animal experiments were conducted in strict accordance with the animal husbandry guidelines of the Shenyang Agricultural University (Liaoning, China).

2.2. Rodent sample collection

The rodents were captured from the Hulunbuir border regions between June 2021 and November 2022. Five sites were selected for rodent trapping; their geographical distributions are shown in Fig. 1. The rat traps with peanuts dipped in sesame oil as bait were arranged every 5 m according to the movement trajectory or feces of the rodents. The traps were placed at 6:30 p.m. and retracted at 6:00 a.m. the next morning. The cages where the rodents were captured were brought to the laboratory and placed in a bucket of water, to which excess ether was subsequently added, and the bucket was then sealed. Each captured rodent was then transferred to a white cloth bag and transported to the Manzhouli International Travel Health Care Center for breed identification. Rodent species were identified and recorded in accordance with the Chinese Manual of Important Medical Animal Identification. The liver, spleen, lung, and kidney tissues of the rodents were collected aseptically and stored at −80 °C for further pathogenic detection.

Fig. 1.

Fig. 1

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Geographic maps of the rodent sampling sites in the Hulunbuir border regions. These maps were plotted using ArcGIS 10.2 (Environmental Systems Research Institute Inc., CA, USA). (A) World map showing the location of China. (B) Map showing the locations of Inner Mongolia Autonomous Region and Hulunbuir City. (C) Enlarged map of Hulunbuir City; the red symbols indicate the sampling regions. Arihashate Port: latitude 48.4439°N, longitude 115.8815°E; Ebudug Port: latitude 50.2424°N, longitude 120.1909°E; Arxan Port: latitude 47.1771°N, longitude 119.9431°E; Heishantou Port: latitude 40.2340°N, longitude 122.0775°E; Manzhouli Port: latitude 49.5800°N, longitude 117.4500°E. (For interpretation of the references to colour in this figure legend, the reader is referred to the Web version of this article.)

2.3. Quantitative PCR-based Bartonella screening

Approximately 200 mg of mixed liver, spleen, lung, and kidney tissues from rodents were placed in a 2 mL RNase-free tube. To this, 5 zirconium beads and 500 μL of PBS were added for grinding. After grinding, the mixture was centrifuged at 6000 rpm for 10 min and 200 μL of the supernatant was used for nucleic acid extraction. A DNA extraction kit (TransGen Biotech Co., LTD, Beijing, China) was used to extract nucleic acids, following the manufacturer's instructions. Bartonella was detected using genus-specific quantitative PCR (qPCR) by amplifying a fragment of 301 bp within the transfer mRNA (ssrA) gene [37]. AceQ Universal U + Probe Master Mix V2 (Nanjing Vazyme Biotech Co., Ltd., Nanjing, China) was used for Bartonella-specific qPCR according to the manufacturer's instructions.

2.4. Molecular characterization of Bartonella spp.

In positive samples detected by qPCR, the citrate synthase (gltA), RNA polymerase subunit (rpoB), and ssrA gene fragments of Bartonella were further amplified by PCR and sequenced using Sanger's method [[37], [38], [39]]. PCR was performed using 2 × Taq Plus Master Mix II (Nanjing Vazyme Biotech Co., Ltd.). The amplification products of gltA, rpoB, and ssrA were 379, 866, and 301 bp in length, respectively, and were identified using 1.2 % agarose gel electrophoresis. The PCR products were purified and transported to Sangon Biotech Co., Ltd. (Shanghai, China) for Sanger sequencing.

2.5. Phylogenetic analysis

The sequences obtained were assembled using DNASTAR Lasergene v7.1 and then deposited in GenBank (Accession Number: OR739188-OR739220). The genotypes of the sequences were initially identified using the Basic Local Alignment Search Tool (BLAST) program of the National Center for Biotechnology (NCBI). For the phylogenetic analysis, reference sequences of different Bartonella genotypes were downloaded from the GenBank database. A phylogenetic tree was constructed using the maximum likelihood (ML) method in MEGA X (https://www.megasoftware.net). A bootstrap test with 1000 bootstrap replicates was conducted to estimate the confidence.

2.6. Statistical analysis

The composition of rodent species in the Hulunbuir border regions and the detection rate of Bartonella infection in different collection areas and species were evaluated using the chi-square test or Fisher's exact test with SPSS 23.0 (SPSS, Inc., Chicago, IL, USA). Differences with a value of p < 0.05 were considered statistically significant.

3. Results

3.1. Rodent species captured in Hulunbuir border regions

A total of 878 rodents were collected from five collection areas in the Hulunbuir border regions between June 2021 and November 2022 (Table 1). Of these, 410 rodents were collected at the Arihashate Port, 162 from the Ebudug Port, 159 from the Arxan Port, 74 from the Heishantou Port, and 73 from the Manzhouli Port (Table 1). The captured rodents belonged to four families, nine genera, and eleven species (Table 1). Lasiopodomys brandtii showed the highest abundance, followed by Apodemus agrarius and Microtus gregalis, accounting for 61.5 % (540/878), 14.69 % (129/878), and 12.19 % (107/878) of the total rodents, respectively (Table 1 and Fig. 2A). Rodent species compositions varied significantly among the five ports (P < 0.001, χ2 = 637.9). The distribution of various rodent species across the five ports is presented in Table 1. The proportions of Lasiopodomys brandtii at Arihashate Port and Ebudug Port were significantly higher than those at the other three ports, at 88.53 % (363/410) and 90.12 % (146/162), respectively. Arxan Port was mainly inhabited by Apodemus agrarius, accounting for 81.13 % (129/159). Heishantou Port was mainly inhabited by Microtus gregalis, accounting for 63.51 % (47/74). Meriones unguiculatus was predominant at the Manzhouli Port, accounting for 60.27 % (44/73). Apodemus agrarius and Apodemus peninsulae captured at Arxan Port were not present at the other ports, whereas Rattus norvegicus was only collected from Heishantou Port, and Cricetulus barabensis was only found at Manzhouli Port (Table 1), suggesting that the compositions of rodent species in these three areas was more diverse than those in the other two ports.

Table 1.

Positivity rates of Bartonella infection in rodents captured in Hulunbuir border regions in this study.

Family Genus Species Arihashate Port Ebudug Port Arxan Port Heishantou Port Manzhouli Port Total
Muridae Apodemus Apodemus agrarius 0 0 14/129 (10.85 %) 0 0 14/129 (10.85 %)
Apodemus peninsulae 0 0 1/7 (14.29 %) 0 0 1/7 (14.29 %)
Rattus Rattus norvegicus 0 0 0 1/14 (7.14 %) 0 1/14 (7.14 %)
Mus Mus musculus 0 0 0 0/1 0/2 0/3
Cricetifae Cricetus Cricetulus barabensis 0 0 0 0 0/1 0/1
Microtus Lasiopodomys brandtii 69/363 (19 %) 59/146 (40.41 %) 9/18 (50 %) 0/3 2/10 (20 %) 139/540 (25.74 %)
Microtus gregalis 7/38 (18.42 %) 3/8 (37.5 %) 1/3 (33.33 %) 0/47 0/11 11/107 (10.28 %)
Phodopus Phodopus sungorus 0 0 0/2 0 0/1 0/3
Meriones Meriones unguiculatus 1/4 (25 %) 0 0 0 2/44 (4.55 %) 3/48 (6.25 %)
Dipodidae Allactaga Allactaga sibirica 1/5 (20 %) 1/1 (100 %) 0 4/9 (44.44 %) 0 6/15 (40 %)
Sciuridae Citellus Spermophilus dauricus 0 1/7 (14.29 %) 0 0 4 1/11 (9.09 %)
Total 78/410 (19.02 %) 64/162 (39.51 %) 25/159 (15.72 %) 5/74 (6.76 %) 4/73 (5.48 %) 176/878 (20.05 %)
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Fig. 2.

Fig. 2

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Composition of small rodent species and positivity rates of Bartonella infection in rodents captured in the Hulunbuir border regions. The graphs were generated using the GraphPad Prism version 8.0 (Graph Pad Software Inc., CA, USA). (A) Composition of small rodent species captured in the Hulunbuir border regions. (B) Positivity rates of Bartonella infection among different rodent species. (C) Positivity rates of Bartonella infection in rodents at different collection sites.

3.2. Bartonella prevalence in captured rodents

qPCR was performed to detect Bartonella infection in tissue samples from the captured rodents. We found that 176 of the 878 samples were positive, with a positivity rate of 20.05 %. Bartonella was detected at all five ports, indicating that its wide distribution in the Hulunbuir border regions. The Bartonella infection rate was the highest in rodents at Ebudug Port, with 39.51 % (64/162), followed by Arihashate Port and Arxan Port, with positivity rates of 19.02 % (78/410) and 15.72 % (25/159), respectively. Bartonella infection rates at Heishantou Port and Manzhouli Port were lower, with 6.76 % (5/74) and 5.48 % (4/73), respectively (Table 1 and Fig. 2C). The difference in positivity rates among the different collection areas was significant (P < 0.001, χ2 = 165.28).

Eight of the 11 captured rodent species were infected with Bartonella (Table 1 and Fig. 2B). The positivity rate of Bartonella infection was the highest in Allactaga sibirica, with a positivity rate of 40 % (6/15), followed by 25.74 % (139/540) in Lasiopodomys brandtii, 14.29 % (1/7) in Apodemus peninsulae, 10.85 % (14/129) in Apodemus agrarius, and 10.28 % (11/107) in Microtus gregalis. Spermophilus dauricus, Rattus norvegicus, and Meriones unguiculatus had positivity rates of <10 %. The positivity rates among the different rodent species were significant (P < 0.001, χ2 = 33.2).

3.3. Molecular characterization of Bartonella species in captured rodents

The qPCR-positive samples were further amplified and sequenced using the gltA, rpoB, and ssrA gene fragments of Bartonella. Phylogenetic trees were created based on sequences obtained by the ML method using MEGA X software. The analysis showed that three Bartonella species were detected at five sites in the Hulunbuir border regions. The gltA, rpoB, and ssrA gene fragments from the three ports (Arihashate Port, Heishantou Port, and Manzhouli Port) clustered with B. grahamii (Fig. 3, Fig. 4, Fig. 5), with 96–99 % identity to gltA, 98–100 % to rpoB, and 96–98 % to ssrA. The samples from Arxan Port grouped with B. Japonica (Fig. 3, Fig. 4, Fig. 5), with 96.8 % identity with gltA, 99.8 % with rpoB, and 98 % with ssrA. The gltA gene fragments of samples from Ebudug Port grouped with B. alsatica and B. heixiaziensis (Fig. 3), sharing 99.39 % identity with B. alsatica and 98.64 % identity with B. heixiaziensis at the nucleotide level. The ssrA and rpoB sequences also shared a high genetic similarity (98.6 % and 99.51 %) with those of B. alsatica (Fig. 4, Fig. 5).

Fig. 3.

Fig. 3

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Phylogenetic analysis of gltA gene fragments of Bartonella. Sequences of Bartonella determined in this study are marked with dark dots. EBDG, AES, HST, ARHST, and MZL correspond to the sampling locations Ebudug Port, Arxan Port, Heishantou Port, Arihashate Port and Manzhouli Port. The scale bar indicates the number of nucleotide substitutions per site.

Fig. 4.

Fig. 4

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Phylogenetic analysis of ropB gene fragments of Bartonella. Sequences of Bartonella determined in this study are marked with dark dots. EBDG, AES, HST, ARHST, and MZL correspond to the sampling locations Ebudug Port, Arxan Port, Heishantou Port, Arihashate Port and Manzhouli Port. The scale bar indicates the number of nucleotide substitutions per site.

Fig. 5.

Fig. 5

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Phylogenetic analysis of ssrA gene fragments of Bartonella. Sequences of Bartonella determined in this study are marked with dark dots. The identification EBDG, AES, HST, ARHST, and MZL correspond to the sampling locations Ebudug Port, Arxan Port, Heishantou Port, Arihashate Port and Manzhouli Port. The scale bar indicates the number of nucleotide substitutions per site.

4. Discussion

Bartonella is a zoonotic pathogen with rodents as its natural host [5]. With the development of transportation, tourism, and the construction of some key projects, there has been an increase in opportunities for human contact with wildlife, particularly disease-carrying vectors, which may lead to the transmission of bartonellosis to humans. Therefore, it is necessary to investigate the prevalence of rodent-associated Bartonella spp.

In this study, 878 rodents were collected from five ports in the Hulunbuir border areas and tested for Bartonella infection. The overall infection rate of Bartonella at the five ports was 20.05 %, which was lower than that in most areas in China. The Bartonella-positivity rate in rodents at the Ebudug Port was the highest at 39.51 %, which is comparable to that found in the Qaidam Basin (38.6 %, 39/101 [40]), Shangdang Basin (37.4 %, [55/147] [29]), Qinghai-Tibetan Plateau (30.1 %, [31/103] [41]), and Zhejiang province (31.4 % [134/427] [25]), of China. The positivity rates at Arihashate Port and Arxan Port were 19.02 % and 15.72 %, respectively, similar to those found in rodents from Hebei (17 %, [38/223] [27]), Guizhou (16.05 % [13/81] [32]), and southeastern China (14.86 %, [169/1137] [42]). The positivity rates of rodent-associated Bartonella at Heishantou Port and Manzhouli Port were low, at 6.76 % and 5.56 %, respectively, which are similar to that in Guangzhou (6.4 % [30]) and eastern China (8.4 % [43]).

A total of 11 rodent species were captured from the Hulunbuir border areas. No Bartonella infection was detected in three rodent species: Mus musculus, Phodopus sungorus, and Cricetulus barabensis. Since only three individuals of each of these three rodent species were collected, the absence of Bartonella infection may not accurately reflect the true infection rate in these species. Among rodents positive for Bartonella infection, Allactaga sibirica had the highest positivity rate (40 %). Bartonella infections in Allactaga sibirica have been reported in the Qaidam Basin (100 %, [3/3] [40]), and Shaanxi Province (20 %, [1/5] [44]), of China. The other seven Bartonella-positive rodent species were Lasiopodomys brandtii (25.74 %), Apodemus peninsulae (14.29 %), Apodemus agrarius (10.85 %), Microtus gregalis (10.28 %), Spermophilus dauricus (9.09 %), Rattus norvegicus (7.14 %), and Meriones unguiculatus (6.25 %). Apodemus peninsulae captured from the Shaanxi Province (17.65 %, [3/17] [44]), Zhejiang Province (29 %, [2/7] [25]), the Qinghai-Tibetan Plateau (37.93 % [22/58] [41]), and Zhongtiao Mountain (100 % [1/1] [28]), were Bartonella-positive. Apodemus agrarius and Rattus norvegicus, which are widely distributed in China, have also been found to be infected with Bartonella in many areas of the country. Bartonella was also detected in Microtus gregalis collected from the Qinghai-Tibetan Plateau [41] and Meriones unguiculatus collected from Inner Mongolia [45]. Lasiopodomys brandtii has not previously been reported to harbor Bartonella.

Three species of Bartonella were identified in rodents from the Hulunbuir border areas. The samples from Arihashate Port, Heishantou Port and Manzhouli Port harbored B. grahamii, those from the Arxan Port harbored B. Japonica, and those from the Ebudug Port harbored B. alsatica. Therefore, the distribution of Bartonella was likely influenced by areas. Among the three Bartonella species, B. alsatica and B. grahamii have been reported to cause lymphadenopathy, endocarditis and neuroretinitis in humans [[46], [47], [48], [49], [50], [51]]. To date, there have been four reported cases of human infections by B. alsatica [[48], [49], [50], [51]]. The first and third patients were rabbit breeders and both presented with endocarditis post-infection [48,51]. The second case involved a rabbit butcher who accidently scratched her finger during work, leading to lymphadenopathy [50]. The fourth patient with a B. alsatica infection had a history of regularly hunting wild rabbits, and his clinical manifestation was acute renal failure due to a membranoproliferative glomerulonephritis [49]. To date, only two cases of B. grahamii infection in humans have been reported, one case of lymphadenitis caused by a cat scratch and one case of neuroretinitis in a dog owner [46,47]. Given that two species of human pathogenic Bartonella have been detected in the Hulunbuir border areas, it is crucial to continue monitoring Bartonella infection in this region. It is also essential to monitor antibody levels in the human population to prevent the transmission of Bartonella to humans.

In conclusion, we investigated the prevalence and genetic diversity of rodent-associated Bartonella in the Hulunbuir border regions in China. Eight of the 11 rodent species captured were Bartonella-positive, with an overall positivity rate of 20.05 %. Three Bartonella species, including two pathogenic to humans, B. alsatica and B. grahamii, were detected in the captured rodents. Lasiopodomys brandtii was the dominant rodent species captured for the detection of Bartonella, whereas B. grahamii was the predominant Bartonella species in the captured rodents. Our results highlight the prevalence and genetic diversity of Bartonella species in rodents in the Hulunbuir border regions, indicating the need for risk assessment of human spillover.

Data availability statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

Funding

This study was supported by the National Key R&D Program of China (2022YFC2303700) and the Science and Technology Partnership Program, Ministry of Science and Technology of China (No. KY201901014).

CRediT authorship contribution statement

Xuexia Wen: Writing – original draft, Investigation. Yaoqi Fang: Investigation. Feng Jiang: Investigation. Yixin Wang: Data curation. Qijun Chen: Writing – review & editing, Funding acquisition. Zeliang Chen: Writing – review & editing. Yuhan Wu: Data curation. Qing Xin: Data curation. Xiaohu Han: Writing – original draft, Conceptualization. Hua Deng: Investigation.

Declaration of competing interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Contributor Information

Xiaohu Han, Email: hxh8849@syau.edu.cn.

Hua Deng, Email: 550275346@qq.com.

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Data Availability Statement

The original contributions presented in the study are included in the article, further inquiries can be directed to the corresponding authors.

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