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Molecular and serological survey of Brucella spp. among rodents in western Iran

BMC Veterinary Research volume 21, Article number: 240 (2025) Cite this article

Abstract

Introduction and purpose

Brucellosis is a prevalent bacterial zoonosis globally, affecting a broad range of hosts. The role of rodents in the survival and transmission of Brucella species to humans remains uncertain. This study aimed to investigate the prevalence of Brucella infection among wild rodents in western Iran, specifically in KabudarAhang County within Hamadan Province.

Materials and methods

Sampling was conducted across various regions of KabudarAhang County in western Iran between April 2014 and September 2017. Serological testing was performed using the standard tube agglutination method while molecular investigation was carried out through real-time PCR analysis. Subsequently, molecularly positive samples underwent species identification via conventional PCR.

Results

Serological testing revealed 7 positive samples (1.76%), including four Meriones persicus, one Mus musculus, one Meriones libycus, and one Spermophilus fulvus. In the molecular survey, three samples (0.68%) tested positive for Brucella; these included one M. musculus and two M. persicus. The molecular species identification test detected B. abortus in M. musculus among those positive for Brucella.

Conclusion

These findings suggest that wild rodents may play an overlooked role in the maintenance of pathogenic Brucella species in natural environments. Furthermore, in situations where standard diagnostic guidelines for brucellosis in wildlife are not well established, employing multiple testing approaches is crucial for accurate detection.

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Introduction

Brucellosis poses a significant dual threat to humans, leading to both economic losses in the dairy industry and serious health concerns. Brucella species are capable of causing infection in a wide range of hosts. Currently, the genus Brucella comprises 13 recognized specie. Brucella melitensis, Brucella abortus, and Brucella suis biovar 1 and 3 are recognized as the most pathogenic species for humans, primarily affecting goats and sheep, cattle, and pigs, respectively [1].

The role of wildlife in Brucella cycle is critically important, yet often overlooked [1]. Countries aiming to eradicate brucellosis from domestic animal populations remain susceptible to setbacks in their control and prevention strategies, primarily due to the risk of transmission from wildlife to domestic species [2]. Rodents, constituting 42% of global mammalian biodiversity, are highly adaptable and can facilitate pathogen transmission across ecosystems [3]. Transmission of rodents-associated Brucella spp. to humans appears to be exceedingly rare. However, the potential zoonotic aspects of B. neotomae, B. microti, and B. suis biovar 5 have been documented [4,5,6,7]. At least 22 rodent species have been documented as susceptible to Brucella infection [8]. Infections have been observed among rodents and lagomorphs in areas where infected livestock are present [9], suggesting that these animals may contribute to in the persistence of Brucella species [10]. In recent decades, the emergence of multidrug resistance (MDR) has become a critical global health issue. Studies have shown that rodents may play a significant role in this phenomenon by acting as reservoirs for pathogenic microorganisms, facilitating the acquisition and dissemination of antibiotic resistance genes and virulence factors [11]. Data on rodent brucellosis in Iran is limited, and the available information from other global regions is both scarce and outdated.

Brucellosis is predominantly reported in the Middle East and Central Asia [1] and is widespread in countries neighboring Iran, including Iraq [12], Pakistan [13], and Turkey [14]. Iran remains one of the countries grappling with high prevalence rates. Recent data from the Ministry of Health and Medical Education of Iran indicate an incidence rate of approximately 22 cases per 100,000 individuals [15]. Iran’s national program for the prevention and control of brucellosis primarily targets livestock through a multifaceted approach, which has resulted in a significant reduction in human clinical cases [16]. The prevalence of human brucellosis in the western and northern regions of Iran is particularly concerning. Hamedan Province stands out for its exceptionally high incidence of clinical cases, with an infection rate approximately three times higher than the national average in 2012 [17]. Between 2009 and 2015, 81% of the 9,318 reported cases in Hamedan Province were among rural residents [18]. The seroprevalence of brucellosis in Hamadan Province has been reported as 4.6% in individual goats and 13.6% at the flock level, while in sheep it is 3% in individuals and 27.9% at the flock level [19]. Additionally, bovine brucellosis has been documented at 1.81% [19, 20]. Brucella species have also been isolated from 4.81% (12/291) of unpasteurized dairy products [21]. KabudarAhang County has the highest incidence of human brucellosis in Hamadan Province, with 143.2 cases per 100,000 people [18]. The current study investigates the infection rate of rodent in KabudarAhang County, Hamedan Province in wester Iran.

Materials and methods

Study area and sample size

Hamadan Province is located at 34°56′ North latitude and 48°56′ East longitude. KabudarAhang County, situated in the northwest of the province, has a population of approximately 160,000 (Fig. 1). To investigate Brucella infection in rodents, this study utilized biobank samples sourced from the National Reference Laboratory of Plague, Tularemia, and Q Fever at Pasteur Institute of Iran. These samples were gathered as part of a multi-phase surveillance program focused on rodent-borne zoonotic diseases. In this research, all archived samples at the center from 2014 to 2017 were analyzed. A total of 6,747 traps were deployed across 33 regions for sample collection. Field investigations were carried out over a three-year period, spanning from April 2014 to September 2017.

Fig. 1
figure 1

Geographic location of Hamadan Province within Iran, with a focus on KabudarAhang County in the northwest (left). The right side of the map highlights the sampling site where rodents were trapped across various habitats, including agricultural fields, livestock pastures, grain storage areas, rural residences, and natural environments such as rivers, streams, and plains.

Full size image

Trapping and sampling

Rodents were captured using wooden live traps and subsequently transported to the Research Centre for Emerging and Reemerging Infectious Diseases at the Pasteur Institute of Iran for further processing. Rodent identification was carried out based on morphological criteria [22]. Following euthanasia via inhaled CO₂ in accordance with the AVMA Guidelines [23], blood was collected via cardiac puncture. The blood samples were centrifuged at 2000 × g for 10 min, and the resulting sera were stored at -20 °C. Subsequently, autopsies were performed, and spleen samples were aseptically collected and stored at -20 °C.

Serological analysis

The serological analysis was conducted using the standard tube agglutination test with the Wright antigen and control sera (Research and Production Complex of Pasteur Institute of Iran, Karaj, Iran). Eight serial dilutions of serum sample were prepared with normal saline solution, each with a volume of 500 µl (1:10, 1:20, 1:40, 1:80, 1:160, 1:320, 1:640, and 1:1280). Subsequently, 500 µl of Wright antigen was added to each tube to achieve final concentration of 1:20, 1:40, 1:80, 1:160, 1:320, 1:640, 1:1280, and 1:2560. All tubes were incubated at 37 °C for 24 h. The dilution of the last tube showing agglutination was recorded. All sample sets were tested alongside control sera.

Additionally, Serological tests for tularemia and plague were conducted on positive samples to assess potential cross-reactivity. The F. tularensis tube agglutination test was performed using a commercial kit (Bioveta, Inc., Ivanovice, Czech Republic) according to the manufacturer’s protocol. An in-house ELISA (developed by the Pasteur Institute of Madagascar) was used to detect IgG against the F1 capsular antigen of Y. pestis [24]. Positive and negative control sera were procured from the kit supplier and manufacturer.

Molecular survey

DNA extraction was performed using the FavorPrep™ Tissue Genomic DNA Extraction Kit (Cat. No. FATGK 001–1, Favorgen Biotech Corp., Taiwan) with 10 mg of spleen tissue, according to manufacturer’s instructions. The output of the DNA extraction process was evaluated using spectrophotometry. Optical absorbance was measured at 260 nm, 280 nm, and 230 nm wavelengths. If the A260/A280 and A260/A230 ratios fell within the acceptable ranges (A260/A280 ratio ~ 1.8 and A260/A230 ratio 2.0–2.2), molecular testing was subsequently performed.

The IS711 gene was amplified for detecting the Brucella genus using a Rotor-Gene™ 6600 in TaqMan real-time PCR system (Corbett Research Ltd., Australia). The qPCR was conducted in a total volume of 20 µl, which included 10 µl of 2x Real Q Plus Master Mix for Probe™ (Cat. No. A313402, Ampliqon Co., Denmark), 900 nmol of forward primer, 900 nmol of reverse primer, 200 nmol of probe, 4 µl of DNA template (containing 1–100 ng), and double-distilled water to reach the final volume. The reaction program comprised an initial cycle at 95 °C for 10 min, followed by 45 cycles of denaturation at 95 °C for 15 s and annealing/extension at 60 °C for 60 s. Each qPCR analysis included positive and negative controls. All analyzed sets in the molecular test were accompanied by internal control templates, dilution controls, and no-template controls (NTCs). The no template control (NTC) consisted of double-distilled water, while DNA from B. abortus was used as the positive control.

Molecularly positive samples for the Brucella genus underwent species determination using a conventional PCR test with Labcycler™ (SensoQuest, Germany), following the protocol recommended by Hinić et al. [25]. Each PCR reaction contained 4 µL of template DNA, 10 µL of Taq DNA Polymerase Master Mix RED (Cat. No.: A180303, Ampliqon, Denmark), and 10 pmol/µl of each primer, in a total volume of 20 µL. The PCR conditions included an initial denaturation at 95 °C for 3 min, followed by 40 cycles of amplification with of denaturation at 95 °C for 30 s, annealing at 60 °C for 35 s, and elongation at 72 °C for 20 s. A final elongation step at 72 °C for 10 min was then performed. PCR products were analyzed by loading onto a 1% agarose gel and electrophoresing for 40 min at 100 volts, with visualization using a Gel Doc instrument. Table 1 summarizes the primers and probes used for molecular investigation.

Table 1 Primers and probe used for molecular investigation
Full size table

Results

A total of 435 rodents were examined molecularly, while 396 rodents underwent serological analysis. Out of the total sample size, 39 rodents (8.96%) were excluded from the serological study due to insufficient serum quantities and qualities. The most prevalent rodent species, listed in descending order, were: 327 Meriones persicus (75.17%), 44 Meriones libycus (10.11%), 24 Meriones vinogradovi (5.52%), 13 Ellobius lutescens (2.99%), 8 Microtus qazvinensis (1.84%), 7 Spermophilus fulvus (1.61%), 7 Meriones tristrami (1.61%), 2 Arvicola persicus (0.46%), 2 Calomyscus elburzensis isatissus (0.46%), and 1 Mus musculus domesticus (0.23%).

Seven samples (1.76%) tested positive in serological analysis. Four samples were from M. persicus (4/299, 1.34%, 95% CI: 0.36 − 3.38%), one from Mus musculus (1/1, 100.00%, 95% CI: 2.50 − 100.00%), one from M. libycus (1/39, 2.56%, 95% CI: 0.06 − 13.45%), and one from Spermophilus fulvus (1/6, 16.67%, 95% CI: 0.42 − 64.12%). Notably, there was no cross-reactivity observed with Francisella tularensis and Yersinia species among the positive samples.

Additionally, 3 out of 435 DNA samples tested positive for Brucella genus. Two samples were from M. persicus (2/327, 0.61%, 95% CI: 0.07 − 2.20%), while one was from M. musculus (1/1, 100.00%, 95% CI: 2.50 − 100.00%), which was also confirmed as the infected species through serological testing. The M. musculus sample exhibited a specific band in the Brucella species determination test and was identified as B. abortus. Table 2 provides details on the positive samples.

Table 2 The number of positive rodents and their respective species
Full size table

Discussion

This study represents the first investigation into the prevalence of Brucella spp. in wild rodent within Iran. The findings revealed seropositivity in seven rodents representing four different species and the presence of Brucella DNA in three rodents across two species. Of the seven seropositive rodents, Brucella DNA was detected in the spleen of only one. Notably, two additional samples that tested positive for Brucella DNA via molecular analysis were serologically negative. All the positive samples identified in this study were found in habitats near rural agricultural fields and livestock pastures. Traditional livestock farming and free-range sheep grazing are common practices in these areas. Natural infections by Brucella have been previously reported in Microtus arvalis [26], Hydrochoerus hydrochaeris [27], Neotoma lepida [28, 29], Spermophilus townsendii [28], Spermophilus citellus [30], Rattus fuscipes assimilis, Melomys cervinipes, Melomys lutillus [31], Rattus norvegicus [32,33,34], Rattus rattus [35], Myodes glareolus, Apodemus spp [36], and Mus musculus [37]. Our results suggest the presence of natural infection in the Meriones species, which has not been previously documented. However, to confirm natural infection, bacterial isolation is necessary.

Experimental inoculation studies indicate that white mice (Mus musculus), guinea pigs (Cavia porcellus), rats (Rattus norvegicus), and bank voles (Clethrionomys glareolus) are susceptible to B. abortus [38, 39]. However, rats show relative resistance when infected orally [38] Rodents may contract Brucella from cattle, deer, goats, or other animals that shed these bacteria through abortion [40]. Evidence of rodent infection has been documented near farms with brucellosis-affected livestock [41] Furthermore, there is significant evidence indicating that rodents can transmit Brucella infections to their offspring or to other animal species. For instance, Brucella microti has been detected in the mandibular lymph nodes of seemingly healthy foxes, suggesting exposure through predation on infected rodents [42]. Vertical transmission in rats and potential latent carrier status in offspring from infected mothers has been reported [43]. Sexual transmission of B. abortus between infected male and uninfected female rats has been also documented [44]. These findings underscore the potential role of rodents in the ecology and transmission of Brucella spp., although the factors driving rodent infection and the role of vectors remain unclear.

The bcsp31 and IS711 genetic markers are reliable for identifying Brucella at the genus level [25, 45]. Targeting multiple genetic markers enhance the molecular diagnostic approach for field animals [46]. This study employed the IS711 sequence, which is considered the most sensitive target due to its high copy number [47]. Given the typically low pathogen load in wildlife specimens, using a marker with a high copy number is crucial. The high cycle threshold values observed in positive qPCR tests in this study suggest a low microbial load. Hinić et al. demonstrated that the IS711 marker did not produce false-positive when tested against 68 organisms closely related to the Brucella [47].

This study focuses on common human-pathogenic Brucella species in rodents. In Iran, B. abortus and B. melitensis are predominant species [48, 49]. A specific conventional PCR targeting the BruAb2_0168 confirmed the presence of B. abortus in Mus musculus. Previously, Brucella isolation from Mus musculus has been reported [37]. Due to the high degree of DNA homology within the genus Brucella, differentiating between infection caused by human-pathogenic species (B. melitensis, B. abortus, and B. suis) and those from rodent-associated species (B. neotomae, and B. microti, and B. suis bv. 5) remains a diagnostic challenge, particularly in field samples. Most species determination methods have been optimized for DNA extracted from pure cultures, and the quality of the DNA is a critical factor in their success [46]. The sensitivity of these methods for wildlife samples has not been thoroughly assessed. Species-level identification is more accurate when performed on isolates derived from pure bacterial cultures. However, a limitation of our study was the reliance on biobank samples collected over a three-year period. This retrospective approach posed significant challenges for bacterial isolation and culture, as fresh samples were not available for processing.

Serosurveys face challenges due to antibody cross-reactivity between Brucella species and other Gram-negative bacteria, latent infections without seroconversion, declining antibody levels, and early-phase of infection. These factors can lead to false-positive or negative serological results, complicating the interpretation [47]. Moreover, routine serological assays do not differentiate between Brucella species, complicating the understanding of transmission dynamics.

Rodents are attracted to farms by the availability of stover, forage, which, are easily accessible, and farm structures that offer secure nesting sites. Consequently, contact between rodents and livestock is common on most farms. A recent study in Iran found that commensal rodents on seropositive sheep and dairy cattle farms harbored Brucella species, suggesting a reservoirs role for these animals [50]. Despite following the established brucellosis control program, these farms continue to report cases of the disease, failing to achieve full eradicate. Dadar et al. isolated the field strains of B. abortus biovar 3, B. melitensis biovar 1, and the B. melitensis vaccine strain Rev1 from seropositive dairy cattle, as well as field strains of B. abortus biovar 3 and B. melitensis biovar 1 form Mus musculus and Rattus norvegicus, respectively. They reported that 68.75% of rodent tissues tested positive for the Omp28 gene, and 62.5% for the IS711 insertion sequence. B. melitensis DNA was identified in rodents from both sheep and dairy cattle farms [50].

In our study area, sheep are primarily raised through free-range grazing on pastures and agricultural lands, habitats that are also conducive to wild rodents. One limitation of our study is the exclusion of livestock from the surveillance. Despite the high incidence of human brucellosis in KabudarAhang county, studies on animal brucellosis in the area remain limited. A 2020 study reported a brucellosis prevalence of 1.88% in domestic animals in Hamadan Province [51]. Additionally, a 2018 serological study in Hamadan found a Brucella infection rate of 3.3% among dogs [52]. Adhering to biosafety standards, implementing rodent control programs, and maintaining hygiene in breeding facilities can mitigate potential transmission risks. While industrial farms rigorously implement pest control programs, rodents remain a common issue in less-developed rural areas. Investigating the seasonal prevalence of brucellosis in rodents, its relation to calving and lambing seasons, and conducting multi-species surveys involving rodents, wild carnivores, and livestock could deepen our understanding of the enzootic cycle of brucellosis.

Conclusion

The prevention of human brucellosis is largely depending on controlling the disease in animals. However, countries face challenges in eradicating brucellosis, including the survival of Brucella spp. in wildlife. Our findings suggest that rodents may serve as hosts for Brucella species associated with livestock. However, the spillback of the pathogen from rodents to livestock remains uncertain. Enhancing biosafety policies on farms to minimize contact between rodents and livestock is advisable. Disease control programs should consider extending surveillance beyond domestic animal populations, although the costs associated with wildlife surveillance are critical factors to consider in the planning of infectious disease control.

Data availability

All data is available upon request from the corresponding author.

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Acknowledgements

We are grateful to our collaborators, including Hamed Hanifi, Dr. Ahmad Ghasemi, Ali Mohammadi, Amir-Hesam Nemati, and Seyyed Adel Hosseini, for their invaluable assistance in rodent sampling.

Funding

This work received financial support from the Pasteur Institute of Iran and the Centre for Infectious Diseases Control of the Ministry of Health and Medical Education (Grant No. 810).

Author information

Authors and Affiliations

  1. Faculty of Veterinary Medicine, Shahid Bahonar University of Kerman, Kerman, Iran

    Majid Hemati

  2. Department of Pathobiology, Faculty of Veterinary Medicine, Shahid Bahonar University, Kerman, Iran

    Mohammad Khalili

  3. National Reference Laboratory for Plague, Tularemia and Q Fever, Research Centre for Emerging and Reemerging Infectious Diseases, Pasteur Institute of Iran, Kabudar Ahang, Iran

    Saber Esmaeili, Hossein Ahangari Cohan & Ehsan Mostafavi

  4. WHO Collaborating Centre for Vector-Borne Diseases, Department of Epidemiology and Biostatistics, Research Centre for Emerging and Reemerging Infectious Diseases, Pasteur Institute of Iran, Tehran, Iran

    Saber Esmaeili, Hossein Ahangari Cohan & Ehsan Mostafavi

  5. Department of Biology, Faculty of Science, Urmia University, Urmia, Iran

    Ahmad Mahmoudi

Authors
  1. Majid Hemati
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  2. Mohammad Khalili
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  3. Saber Esmaeili
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  6. Ehsan Mostafavi
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Contributions

Conceptualization: M.H, M.K, S.E, and E.M; data analysis and curation: M.H and A.M; visualization: M.H; investigation: M.H, M.K, S.E, A.M, and E.M; methodology: M.H, M.K, S.E, and E.M; project administration and supervision: M.K and E.M; figure preparation: M.H and H.C; funding acquisition: E.M; writing original draft: M.H and H.C; writing-review and editing: M.H, M.K, S.E, A.M, H.C, and E.M; All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Ehsan Mostafavi.

Ethics declarations

Ethics approval and consent to participate

All procedures were conducted in accordance with international ethical standards (AVMA guidelines for the euthanasia of animals) and complied with biosafety regulations. The Human and Animal Ethics Committee at the Pasteur Institute of Iran reviewed, approved, and monitored the ethical aspects of this study (IR.PII.REC.1395.9 ID). This study does not involve any human participants.

Consent for publication

This study does not involve human participants, and no individual data is included.

Competing interests

The authors declare no competing interests.

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Hemati, M., Khalili, M., Esmaeili, S. et al. Molecular and serological survey of Brucella spp. among rodents in western Iran. BMC Vet Res 21, 240 (2025). https://doiorg.publicaciones.saludcastillayleon.es/10.1186/s12917-025-04698-9

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BMC Veterinary Research

ISSN: 1746-6148

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