Prevalence of Bartonella spp. infections in Iran: a systematic review and meta-analysis

1. Context

Bartonella are facultative intracellular bacteria ( 1 ), that can infect a wide range of mammalian hosts, including wild and domestic carnivores ( 2 ), with some species also associated with human infections, including B. henselae, B. quintana, B. bacilliformis, B. elizabethae, B. vinsonii, B. koehlerae, B. clarridgieae, B. alsatica, B. doshiae, B. grahamii, B. ratti, B. massiliensis, and B. tribocorum ( 3 ). Bartonella species have also been isolated froma wide variety of invertebrates , including fleas, ticks, body lice, sheep keds, and even spiders ( 4 ).

In humans, Bartonella infections are able to cause relatively mild flu-like symptoms in immunocompetent individuals. However, more severe manifestations have also been cited in immunocompromised patients such as HIV/AIDS patients and organ transplant recipients ( 3 ).

Among bartonella spp., B. henselae is the most prevalent zoonotic species with a global distribution and is the causative agent of Cat-Scratch Disease. Infections with B. henselae in immunocompromised patients, predisposes the patient to bacillary angiomatosis and peliosis hepatis ( 5 , 6 ). Moreover, B. henselae has been considered the most common cause of neuritis often followed by acute loss of vision ( 7 ). In addition to B. henselae, B. quintana, the etiological agent of trench fever, can also cause bacillary angiomatosis and peliosis hepatis in HIV patients, chronic bacteremia, chronic lymphadenopathy, and blood culture negative endocarditis ( 8 ).

The transmission mode of Bartonella spp. to humans is caused by the scratches from an infected reservoir host or via contact with the infectious faeces of arthropod vectors such as fleas ( 9 ). Bartonella spp. are considered neglected zoonotic pathogens ( 10 ). Despite its public health importance, the epidemiology of Bartonella spp. remains under-studied ( 11 ), particularly in Iran, where- despite being isolated from cats, dogs, ticks, fleas, and humans in some studies ( 12 - 14 ), no systematic review and meta-analysis has been carried out. Therefore, the aim of this systematic review was to summarize and estimate the pooled prevalence of Bartonella infections in humans, domestic and wild animals, and invertebrates in Iran.

2. Data Acquisition

This systematic review and meta-analysis study was prepared and reported according to the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses (PRISMA) 2020 guideline ( 15 ).

2.1. Search strategy

PubMed, Scopus, Web of Science, Google Scholar, Scientific Information Database (SID), MagIran, and IranDoc were searched on 03 October, 2023 with “Bartonella” OR “bartonellosis” OR “Cat scratch disease” AND “Iran”. Search was carried out according to the settings of each database with no restrictions on publication date. For PubMed, Scopus, and Web of Science only English keywords were used whilst for Google Scholar, SID, and MagIran both English and the Persian translation of the keywords were used. All results were extracted, except for Google Scholar, where all results found using Persian keywords and the first 100 results found using English keywords were extracted. The results were gathered in an EndNote library. Only one copy of the duplicate results were kept.

2.2. Title and abstract screening

The titles and abstracts of the results were screened by two independent reviewers in order to identify eligible papers based on the inclusion/exclusion criteria. The inclusion criteria were cross-sectional studies investigating the prevalence of Bartonella infections in humans, pets, farm animals, and parasites in Iran. Conflicts arising over the eligibility of the papers were solved by discussion.

2.3. Data extraction

The last name of the first author, year of publication, sampling period, genus of Bartonella isolates, type of utilized diagnostic test, number of positive infections, sample size, species of the host, and sampling location were extracted into an Excel file.

2.4. Statistical analysis

For meta-analysis, a random-effects model was used and Freeman-Tukey Double Arcsine transformation was applied to stabilize the variance. If a study had pooled biological samples, the pooled point estimate was used. Initially, it was planned to perform the meta-analysis for each detection method separately. However, the meta-analyses of the seroprevalence and culture-based prevalence were not carried out due to the low number of studies using the mentioned detection methods. Instead, the findings of these detection tests were summarized narratively. Subgroup analysis was performed for the species of the hosts. All of the statistical analysis were performed using Stata version 17.

3. Results

A total number of 220 results were identified. 93 results were deleted as duplicates. The titles and abstracts of 127 results were screened, and initially, 22 papers were deemed eligible, full-texts were subsequently sought for these. However, the study by Saydam et al. ( 16 ) was excluded because when the corresponding author was contacted, it was revealed that the study only enrolled confirmed cases of bartonellosis and prevalence could not be determined. A conference paper by Sazmand et al. ( 17 ) was deemed duplicate and excluded due to the similarity of the authors, the location of sampling, and sample size with another study that was already included. A conference paper by Greco ( 18 ) was excluded because the corresponding author did not provide the full-text. Finally, 19 papers were included (Figure 1). The characteristics of the included studies are presented in Table 1.

Figure 1. Flow chart of the studies.

3.1. Detection tests

Polymerase Chain Reaction (PCR) was the most frequently-used detection test (n=18), while Indirect Immunofluorescent Antibody Assay (IFA) and culture were each applied in two studies.

3.2. Host range

The DNA of Bartonella spp. has been isolated from Norway rats (1 study), camels (1 study), cats (5 studies), dogs (3 studies), Ctenocephalides canis and Pulex Irritans fleas (1 study), and Rhipicephalus sanguineus ticks (1 study). Also, the sero-positivity for Bartonella spp. has been detected in humans (1 study).

3.3. Molecular prevalence of Bartonella spp.

Based on PCR methods, the pooled prevalence estimate of Bartonella spp. infection was 4% (95% CI: 2-8%), withan I2 value of 93.89%. In subgroup analysis, the highest prevalence of Bartonella infections was observed in dogs (10%, 95% CI: 1-25%) and cats (10%, 95% CI: 7-13%). For the subgroups of dogs and cats, the I2 value was 92.93% and 0%, respectively. The pooled estimate of Bartonella spp. infection prevalence in rats, camels, ticks, fleas, and humans were 17%, 3%, 0%, 0%, and 0%, respectively (Figure 2).

Figure 2. Pooled estimate and subgroup analysis of molecular prevalence of Bartonella spp. infections in Iran.

3.4. Seroprevalence of Bartonella spp.

Among humans, the seroprevalence of Bartonella spp. was 18% among cat owners and 5% in hospital patients in Tehran. Among 66 dogs in Hamadan, the sero-prevalence was 74.24%.

3.5. Culture prevalence of Bartonella spp.

In one study involving 40 cats in Shahrekord, five culture-positive blood samples (12.5%) were obtained, while no culture-positive nail samples (0%) were detected, and two saliva samples were considered suspected. The culture-positive blood samples were validated by PCR; however, the PCR method did not confirm the suspected saliva samples. Additionally, in one study involving 100 cats in Tehran, no culture-positive blood samples were obtained.

This systematic review and meta-analysis aimed to estimate the pooled prevalence of Bartonella spp. infections in humans, domestic and wild animals, and invertebrates in Iran.

Based on the findings of this study, the overall pooled estimate of Bartonella infections detected by PCR methods in Iran was 4% (95% CI: 2-8%). It is worth mentioning that the pooled prevalence of Bartonella infections was higher in cats (10%) and dogs (10%) compared to humans, camels, rats, ticks, and fleas. The pooled prevalence of Bartonella spp. infection in dogs in the present study was lower than the global pooled estimate of 15.03%. Furthermore, the molecular prevalence of Bartonella spp. infection in cats in this study was higher than the global pooled estimate of 3.6% ( 2 ). However, based on culture-based methods, the prevalence of Bartonella spp. in cats was 12.5% in Shahrekord and 0% in Tehran ( 19 , 20 ). The domestic cat is not only the definitive host for Toxoplasma gondii ( 21 ), but also serves as the primary reservoir for B. henselae, B. clarridgeiae, and B. koehlerae ( 22 ), with the potential to act as subclinical carriers of Bartonella spp. ( 23 ). All Bartonella spp. identified in sick dogs, such as B. clarridgeiae and B. washoensis, are known to be pathogenic or potentially pathogenic to humans, suggesting that dogs may serve as valuable sentinel species and comparative models for human Bartonella infections ( 10 ). The degree of hygiene compliance among dog owners and handlers following exposure to dogs, the level of intimacy between dogs and their owners and children, and the adequacy of management practices among dog owners and handlers may contribute to the risk of zoonotic canine parasitic infections in humans ( 24 ).

The molecular prevalence of Bartonella spp. in Norway rats (17%) in Iran was higher than Chile. In Chile, 43 (27.7%) out of 155 spleen samples and six out of 50 blood samples (12%) from rodents were identified as positive for Bartonella spp. ( 25 ). More than 20 species of Bartonella have been isolated from wild rodents. Rodents along with bats, are known to harbor the highest diversity of Bartonella spp., with several rodent-adapted strains capable of infecting humans ( 26 ). Due to the close association with humans in urban environments, Norway rats play an important role in the transmission of zoonotic diseases to humans ( 27 ).

In the present study, based on a previous research, the prevalence of B. quintana in Iranian culture-negative endocarditis specimens from military hospitals, as determined by PCR, was zero ( 28 ). B, quintana is transmitted by lice in environments with poor hygiens ( 8 ). Homeless people have been considered the main target of B. quintana, with the period of homelessness, age, and alcoholism being associated with susceptibility to infection ( 29 ).

In this study, the seroprevalence of Bartonella spp. among humans was 18% among cat owners and 5% among patients in a hospital in Tehran ( 19 ). This finding was lower compared to data from Egypt, where the prevalence of B. henselae infection among cat owners and individuals with a history of contact with cats was estimated at 51.4% and 42.9%, respectively ( 30 ).

In the present study, the pooled prevalence of Bartonella spp. in camels was 3% (95% CI: 0-16%). This result is consistent with the findings of Selmi et al. ( 31 ), who reported the prevalence of Bartonella spp. and B. henselae by PCR in camels in Tunisia as 3.6% and 3.1%, respectively ( 31 ).

In the present study, the pooled prevalence of Bartonella spp. in fleas was nearly zero. In one included study, Bartonella spp. was detected by PCR in 10 out of 1,937 Ctenocephalides canis and Pulex Irritans fleas ( 13 ). Fleas such as Ctenocephalides felis are known to play a significant role in transmission of Bartonella spp., which are capable of multiplying within the flea digestive tract ( 2 ). However, given the nearly zero prevalence in this study, fleas seem to play a minimal role in the transmission of Bartonella spp. in Iran.

In the present study, the pooled prevalence of Bartonella spp. in ticks was nearly zero. In one included study, Bartonella spp. was detected by PCR in 1 out of 12 Rhipicephalus sanguineus that were collected from dogs ( 32 ). Our pooled estimate is lower compared to findings from Thailand and Malaysia, where the molecular prevalence of Bartonella spp. in ticks was estimated at 2.5% and 5.26%, respectively ( 33 , 34 ).

In this systematic review, no studies were identified involving other animal species, including wildlife animals, domestic animals such as sheep and cattle, or ectoparasites such as lice. The primary limitation of the individual studies included in this systematic review and meta-analysis was the limited number of studies, particularly those involving humans, rodents, and other animal species. Therefore, further investigations on Bartonella spp. infections in Iran are recommended.

Bartonella infections are diseases of both medical and veterinary importance. Thus, the One Health approach should be applied to collect more data and implement appropriate preventive and control measures ( 2 , 35 ), by linking medicine, veterinary medicine, farming, and the economic sectors to improve public health outcomes ( 36 ).

4. Conclusion

In conclusion, based on the findings of this study, the overall molecular prevalence of Bartonella spp. infections was 4% (95% CI: 2-8%), with the highest values observed in rats [17% (95% CI: 10-26%)], dogs [10% (95% CI: 1-25%)], and cats [10% (95% CI: 7-13%)]. Moreover, the pooled molecular prevalence in camels, humans, ticks, and fleas were 3% (95% CI: 0-16%), 0%, near zero, and near zero, respectively. Among studies utilizing serological methods, in one study among humans, the seroprevalence of Bartonella spp. was 18% among cat owners and 5% among hospital patients in Tehran. Among dogs in Hamadan, the sero-prevalence of Bartonella spp. was estimated to be 74.24%. Moreover, based on culture methods, in one study among cats in Shahrekord, five culture-positive blood samples were reported (12.5%) and, in another study among cats in Tehran, the prevalence was zero. Further investigations on Bartonella spp. infections in Iran, particularly among under-studied hosts, are recommended.

Acknowledgment

Not Applicable.

Authors' Contribution

Study concept and design: A. FD, M. S.

Acquisition of data: A. FD, M. S.

Analysis and interpretation of data: A. FD, P. K.

Drafting of the manuscript: A. FD, H. A.

Critical revision of the manuscript for important intellectual content: A. FD.

Statistical analysis: A. FD, H. A.

Administrative, technical, and material support: A. FD, P. K, H. A, M. S.

Ethics

We hereby declare all ethical standards have been respected in preparation of the submitted article.

Conflict of Interest

The authors declare no conflict of interest.

Funding

This study received no funding.

Data Availability

Datasets and statistical codes are available upon request from the authors.

References

1. Zhang B, Nurland RA, Guan Y, Zhou S, Lu M, Nuli R, et al. Detection of Bartonella in kissing bugs Triatoma rubrofasciata collected from Huizhou City, South China. New Microbes and New Infections. 2023; 54:101170.
2. Zarea AAK, Tempesta M, Odigie AE, Mrenoshki D, Fanelli A, Martella V, et al. The Global Molecular Prevalence of Bartonella spp. in Cats and Dogs: A Systematic Review and Meta-Analysis. Transboundary and Emerging Diseases. 2023; 2023
3. McCormick DW, Rassoulian-Barrett SL, Hoogestraat DR, Salipante SJ, SenGupta D, Dietrich EA, et al. Bartonella spp. Infections Identified by Molecular Methods, United States. Emerging Infectious Diseases. 2023; 29(3):467.
4. Mullins K, Canal E, Ouch P, Prasetyo D, Tagoe J, Attram N, et al. Bartonella Species in Cambodia, Ghana, Laos, and Peru: Results from Vector and Serosurveys. Vector-Borne and Zoonotic Diseases. 2023; 23(1):9-17.
5. Kumadaki K, Suzuki N, Tatematsu K, Doi Y, Tsukamoto K. Comparison of biological activities of BafA family autotransporters within Bartonella species derived from cats and rodents. Infection and Immunity. 2023; 91(3):e00186-22.
6. Tadjbakhsh H, Mokhber Dezfouli M, Akbarein H. A review of the most important Zooneses with a special vision towards emerging and re-emerging diseases and its status in Iran Part (1): Bacterial zoonoses. Veterinary Clinical Pathology The Quarterly Scientific Journal. 2017; 11(3 (43) Autumn): 197-223.
7. Nikolic B, Ivancevic N, Pepic A, Kovacevic M, Mladenovic J, Rovcanin B, et al. Child Neurology: Bartonella henselae Neuroretinitis in 2 Patients. Neurology. 2022; 98(21):896-900.
8. García-Álvarez L, García-García C, Muñoz P, Fariñas-Álvarez MdC, Cuadra MG, Fernández-Hidalgo N, et al. Bartonella endocarditis in spain: case reports of 21 cases. Pathogens. 2022; 11(5):561.
9. Krügel M, Król N, Kempf VA, Pfeffer M, Obiegala A. Emerging rodent-associated Bartonella: a threat for human health? Parasites & Vectors. 2022; 15(1):113.
10. Torrejón E, Sanches GS, Moerbeck L, Santos L, André MR, Domingos A, et al. Molecular survey of Bartonella species in stray cats and dogs, humans, and questing ticks from Portugal. Pathogens. 2022; 11(7):749.
11. Zeppelini CG, Oliveira DD, Kosoy MY, Reis MG, Ko AI, Childs JE, et al. Bartonella in Norway rats (Rattus norvegicus) from the urban slum environment in Brazil. Anais da Academia Brasileira de Ciências. 2023; 95:e20220809.
12. Shamshiri Z, Goudarztalejerdi A, Zolhavarieh SM, Kamalpour M, Sazmand A. Molecular Identification of Bartonella Species in Dogs and Arthropod Vectors in Hamedan and Kermanshah, Iran. Iranian Veterinary Journal. 2022; 19(2):104-16.
13. Seidi S, Tavassoli M, Malekifard F. Cross-sectional Study of Bartonella, Rickettsia and Wolbachia by Molecular Method in Fleas Ctenocephalides canis and Pulex irritans from the West and Northwest of Iran. Journal Of Ardabil University OF Medical Sciences. 2021; 20(4 ): 505-18.
14. Janfaza N, Nezhad MH, Esmaeili S, SeyedAlinaghi SA, Abbasian L, Biazar T, et al. Bacillary angiomatosis by Bartonella quintana in HIV-infected patient: first malleolar confirmed case in Iran. Hiv & Aids Review. 2021; 20(2):147-50.
15. Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. International journal of surgery. 2021; 88:105906.
16. Saydam FN, Erdem H, Ankarali H, El-Arab Ramadan ME, El-Sayed NM, Civljak R, et al. Vector-borne and zoonotic infections and their relationships with regional and socioeconomic statuses: An ID-IRI survey in 24 countries of Europe, Africa and Asia. Travel Med Infect Dis. 2021; 44:102174.
17. Sazmand A, Bahiraie Z, Shamshiri Z, Goudarztalejerdi A. Are ticks of dogs biological vectors for pathogenic Bartonella spp.? Persian Journal of Acarology. 2022;94.
18. Greco G. Zoonotic Bartonella Infections in Cats and Dogs from Iran and Italy. Zoonotic disease panel of the 21st International Microbiology Webinar Series: IRN; 2020.
19. Oskoueizadeh K, Zahraei Salehi MT, Ale Davoud SJ, Majlesi B, Ghafari H, Eshrafi Tamami I, et al. Study in prevalence of Bartonella henselae infection in domestic cats from Tehran. Journal of Veterinary Research. 2008; ;63(4):183-189.
20. Oskouizadeh K, Mahzounieh M, Ziaie B, Zahraei-Salehi T, Ashrafi-Tamaei I. Isolation and identification of Bartonella henselae from domestic cats in Shahrekord-Iran. Iran Vet J. 2011; 7(1):5-12.
21. Mehrabi F, Rassouli M, Chashmi SHE. Molecular detection of Toxoplasma gondii in chicken meats and eggs in Semnan City, Iran. 2023; 17(1):167-172.
22. Zarea A, Tempesta M, Fouad E, Ndiana L, Mahmoud M, Mrenoshki D, et al. Prevalence of Bartonella spp., haemotropic Mycoplasma spp. and others vector-borne pathogens in private-owned dogs and cats, Egypt. Acta Tropica. 2023; 240:106857.
23. Shamshiri Z, Goudarztalejerdi A, Zolhavarieh SM, Greco G, Sazmand A, Chomel BB. Molecular detection and identification of Bartonella species in cats from Hamedan and Kermanshah, Western Iran. Comparative Immunology, Microbiology and Infectious Diseases. 2022; 89:101879.
24. Ola-Fadunsin SD, Abdulrauf AB, Ganiyu IA, Hussain K, Ambali HM, Elelu N. The Intensity of Infection and Public Health Perception of Potentially Zoonotic Intestinal Parasites of Dogs in Kwara Central, Nigeria. Iranian Journal of Veterinary Medicine. 2023; 17(2): 119-128.
25. Sepúlveda-García P, Rubio AV, Salgado R, Riquelme M, Bonacic C, Canales N, et al. 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; 100:102026.
26. Xu A-L, Chen Y-F, Mu L, Liu P-B, Wang J, Li R-X, et al. Bartonella Prevalence and Genome Sequences in Rodents in Some Regions of Xinjiang, China. Applied and Environmental Microbiology. 2023; 89(4):e01964-22.
27. Azimi T, Azimi L, Fallah F, Pourmand MR, Dogaheh HP, Tabatabaei SR. Detection and distribution of zoonotic pathogens in wild Norway rats (Rattus norvegicus) from Tehran, Iran. New Microbes and New Infections. 2021; 42:100908.
28. Dirbazian A, Sadeghimanesh M, Morovvati A, Soleimani M, Mirjani R, Mousavi SH. Molecular Detection of Infectious Endocarditis (Bartonella quintana) Bacteria from Selected Military Hospitals. Iranian Journal of Medical Microbiology. 2022; 16(5):457-64.
29. Mai B-H-A. Seroprevalence of Bartonella quintana infection: a systematic review. Journal of Global Infectious Diseases. 2022; 14(2):50-6.
30. Sayed AS, Alsaadawy RM, Ali MM, El-Hamid A, Rawhia F, Baty RS, et al. Serological and Molecular Detection of Bartonella henselae in Cats and Humans from Egypt: Current Status and Zoonotic Implications. Frontiers in Veterinary Science. 2022; 9:859104.
31. Selmi R, Said MB, Yahia HB, Abdelaali H, Boulouis H-J, Messadi L. First report on Bartonella henselae in dromedary camels (Camelus dromedarius). Infection, Genetics and Evolution. 2020; 85:104496.
32. Shamshiri Z, Goudarztalejerdi A, Zolhavarieh SM, Kamalpour M, Sazmand A. Molecular Identification of Bartonella Species in Dogs and Arthropod Vectors in Hamedan and Kermanshah, Iran. Iranian Veterinary Journal. 2023; 19(2):104-16.
33. Saengsawang P, Kaewmongkol G, Phoosangwalthong P, Chimnoi W, Inpankaew T. Detection of zoonotic Bartonella species in ticks and fleas parasitizing free-ranging cats and dogs residing in temples of Bangkok, Thailand. Veterinary Parasitology: Regional Studies and Reports. 2021; 25:100612.
34. Asyikha R, Sulaiman N, Mohd-Taib F. Detection of Bartonella sp. in ticks and their small mammal hosts in mangrove forests of Peninsular Malaysia. Trop Biomed. 2020; 37:919-31.
35. Gonçalves-Oliveira J, Damasco PV, Assis MRdS, Freitas DE, Pessoa Junior AA, de Sousa LS, et al. Infectious endocarditis caused by Bartonella henselae associated with infected pets: two case reports. Journal of Medical Case Reports. 2023; 17(1):143.
36. Bahonar A, Hessameddin A. One health, concept scope and ongoing activities in the world. 19th Iran Veterinary Congress; 25 April, 2016; Tehran, Iran. 2016.
37. Azimi T, Azimi L, Fallah F, Pourmand MR, Dogaheh HP, Tabatabaei SR. Detection and distribution of zoonotic pathogens in wild Norway rats (Rattus norvegicus) from Tehran, Iran. New Microbes and New Infections. 2021; 42
38. Bahari A, Azami S, Goudarztalejerdi A, Karimi S, Esmaeili S, Chomel BB, et al. Molecular Detection of Zoonotic Pathogens in the Blood and Tissues of Camels (Camelus dromedarius) in Central Desert of Iran. Yale J Biol Med. 2021; 94(2):249-58.
39. Dirbazian A, Sadeghimanesh M, Morovvati A, Soleimani M, Mirjani R, Mousavi SH. Molecular Detection of Infectious Endocarditis (Bartonella quintana) Bacteria from Selected Military Hospitals. Iranian Journal Of Medical Microbiology. 2022; 16(5):457-64.
40. Ghaemi M, Sharifiyazdi H, Heidari F, Nazifi S, Ghane M. 'Candidatus Bartonella dromedarii' in the dromedary camels of Iran: Molecular investigation, phylogenetic analysis, hematological findings, and acute-phase proteins quantitation. Vet Microbiol. 2019; 237:108404.
41. Ghasemi A, Latifian M, Esmaeili S, Naddaf SR, Mostafavi E. Molecular surveillance for Rickettsia spp. and Bartonella spp. in ticks from Northern Iran. PLoS One. 2022; 17(12):e0278579.
42. Greco G, Sazmand A, Goudarztalejerdi A, Zolhavarieh SM, Decaro N, Lapsley WD, et al. High Prevalence of Bartonella sp. in Dogs from Hamadan, Iran. Am J Trop Med Hyg. 2019; 101(4):749-52.
43. Jajarmi M, Akhtardanesh B, Yazdani A, Hajipour P, Mohseni P, Ghanbarpour R, et al. Molecular detection of Bartonella henselae in blood samples obtained from owned cats in Kerman city using Nested-PCR. International Journal of Veterinary Research. 2022; 2(1):31-9.
44. Mazaheri Nezhad Fard R, Vahedi SM, Ashrafi I, Alipour F, Sharafi G, Akbarein H, et al. Molecular identification and phylogenic analysis of Bartonella henselae isolated from Iranian cats based on gltA gene. Veterinary Research Forum. 2016; 7(1):69-72.
45. Mirzadeh H, Zeyghami H, Taghiloo B, Pour Rastgoo F. Bartonella and Rickettsial Infections in Human Flea) Pulex Irritans). Journal of Advances in Medical and Biomedical Research. 2015; 23(100):105-15.
46. Oskouizadeh K, Zahraei-Salehi T, Aledavood S. Detection of Bartonella henselae in domestic cats' saliva. Iran J Microbiol. 2010; 2(2):80-4.
47. Oskouizadeh k, Mosallanejad B, Seyfiabad Shapouri M, Sanaie K. A cross sectional study on Bartonella henselae infection in dogs in Ahvaz district by PCR. Iranian Veterinary Journal. 2013; 9(3):5-12.
48. Samsami S, Ghaemi M, Sharifiyazdi H. Molecular detection and phylogenetic analysis of 'Candidatus Bartonella merieuxii' in dogs and its effect on hematologic parameters. Comp Immunol Microbiol Infect Dis. 2020; 72:101504.
49. Sazmand A, Harl J, Eigner B, Hodžić A, Beck R, Hekmatimoghaddam S, et al. Vector-borne bacteria in blood of camels in Iran: new data and literature review. Comparative Immunology, Microbiology and Infectious Diseases. 2019; 65:48-53.
50. Zurita A, Gutiérrez SG, Cutillas C. Infection Rates of Wolbachia sp. and Bartonella sp. in Different Populations of Fleas. Curr Microbiol. 2016; 73(5):704-13.