@article{Banović2023c,

title = {Evidence of tick-borne encephalitis virus neutralizing antibodies in Serbian individuals exposed to tick bites},

author = {Pavle Banović and Dragana Mijatović and Ivana Bogdan and Verica Simin and Eleftherios Meletis and Polychronis Kostoulas and Katarina Resman Rus and Nataša Knap and Misa Korva and Tatjana Avsic Zupanc and Alejandro Cabezas-Cruz},

doi = {10.3389/fmicb.2023.1314538},

year  = {2023},

date = {2023-12-12},

urldate = {2023-11-23},

journal = {Frontiers in Microbiology},

volume = {14},

abstract = {Tick-borne encephalitis (TBE) is an emerging vector-borne and food-borne disease caused by the tickborne encephalitis virus (TBEV; Orthoflavivirus encephalitidis), with a distribution spanning the Eurasian continent. Despite its significant public health impact in various European regions, TBE remains largely underdiagnosed in Serbia due to limited awareness and diagnostic challenges. In response to this, our study aimed to comprehensively assess TBEV exposure in individuals infested with ticks and to identify potential TBEV foci within Serbia. From 2019 to 2021, we conducted an observational study involving 450 patients who reported tick infestations. Our demographic analysis revealed a median age of 38 years, with a slight male predominance among the participants. We documented tick infestations in 38 municipalities across 14 districts of Serbia, with a notable concentration in proximity to Fruška Gora Mountain. The ticks most frequently removed were Ixodes ricinus, with nymphs and adult females being the predominant stages. On average, nymphs were removed after about 27.1 hours of feeding, while adult females remained attached for approximately 44.4 hours. Notably, we found age as a significant predictor of infestation time for both nymphs and adult females. Furthermore, we detected TBEV-neutralizing antibodies in 0.66% of the serum samples, shedding light on potential TBEV foci, particularly in Fruška Gora Mountain and other regions of Serbia. In conclusion, our study emphasizes the urgent need for active TBE surveillance programs, especially in areas suspected of hosting TBEV foci, in order to assess the true TBE burden, identify atrisk populations, and implement effective preventive measures.},

keywords = {Serbia, tick-borne encephalitis, tick-borne encephalitis (TBEV), ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Banović2023,

title = {Emerging tick-borne spotted fever group rickettsioses in the Balkans},

author = {Pavle Banović and Adrian Alberto Díaz-Sánchez and Angélique Foucault-Simonin and Lourdes Mateos-Hernandez and Alejandra Wu-Chuang and Clemence Galon and Verica Simin and Dragana Mijatović and Ivana Bogdan and Belkis Corona-González and Liani 

 Coronado Báez and Joanna Kulisz and Aneta Woźniak and Zbigniew Zając and Dasiel Obregón and Sara Moutailler and Alejandro Cabezas-Cruz},

doi = {https://doi.org/10.1016/j.meegid.2022.105400},

year  = {2023},

date = {2023-01-05},

urldate = {2023-01-05},

journal = {Infection, Genetics and Evolution},

volume = {107},

abstract = {The impact of tick-borne pathogens (TBPs) on human health has increased in the last decades, since the incidence of emerging and re-emerging infectious and zoonotic tick-borne diseases has increased worldwide. Tick-borne rickettsiae of the Spotted Fever group (SFGR) are considered as emerging pathogens that can infect humans and cause a variety of non-specific clinical symptoms. Here, we report nine cases of atypical tick-borne diseases (9/460; 1.95%) that occurred over a period of four months (from 15 April 2021 to 16 August 2021) in Serbia, from which five cases were classified as confirmed SFGR infection, two cases as probable SFGR infection and two cases as suspected SFGR infection. Within cases of confirmed SFGR infection, R. helvetica was detected as the causative agent in two cases. The most common clinical finding was non-expanding persistent circular redness, followed by eschar and enlargement of regional lymph nodes, and pain at lesion site. Rickettsia outer membrane protein B (ompB) and citrate synthase (gltA) gene fragments were amplified from clinical samples and ticks attached to patients and IgG reacting with Rickettsia conorii antigen were detected in sera samples of patients, which are highly suggestive of exposure to SFGR. Surveillance and monitoring of rickettsial diseases in Serbia should continue and extended to new areas due to the increasing trend of clinical infections caused by SFGR in the country.},

keywords = {rickettsia, Serbia, tick-borne diseases, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Dragonjić2022,

title = {Fatal Case of Imported Tick-Borne Encephalitis in South Serbia},

author = {Lidija Popović Dragonjić and Miodrag Vrbić and Aleksandar Tasić and Verica Simin and Ivana Bogdan and Dragana Mijatović and Alejandro Cabezas-Cruz and Pavle Banović},

editor = {Harunor Rashid},

doi = {https://doi.org/10.3390/tropicalmed7120434},

year  = {2022},

date = {2022-12-13},

journal = {Tropical Medicine and Infectious Disease},

volume = {7},

number = {434},

issue = {12},

abstract = {Tick-borne encephalitis (TBE) is vaccine-preventable neglected zoonotic neuroinvasive disease, caused by tick-borne encephalitis virus (TBEV). Many of the Central and Eastern European countries are affected by TBE, which is often poorly perceived by tourists visiting endemic territories. Here we are reporting a fatal case of imported TBE in Serbian resident who was exposed to a tick bite during a visit to Switzerland.},

keywords = {fatal, Serbia, tick-borne encephalitis, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Banović2022,

title = {Clinical Aspects and Detection of Emerging Rickettsial Pathogens: A “One Health” Approach Study in Serbia, 2020},

author = {Pavle Banović and Adrian Alberto Díaz-Sánchez and Verica Simin and Angelique Foucault-Simonin and Clemence Galon and Alejandra Wu Chuang and Dragana Mijatović and Dasiel Obregon and Sara Moutailler and Alejandro Cabezas-Cruz},

editor = {Antonio Battisti

},

url = {https://www.frontiersin.org/articles/10.3389/fmicb.2021.797399/full},

doi = {doi.org/10.3389/fmicb.2021.797399},

year  = {2022},

date = {2022-01-26},

journal = {Frontiers in Microbiology},

abstract = {Ticks carry numerous pathogens that, if transmitted, can cause disease in susceptible humans and animals. The present study describes our approach on how to investigate clinical presentations following tick bites in humans. To this aim, the occurrence of major tick-borne pathogens (TBPs) in human blood samples (n = 85) and the ticks collected (n = 93) from the same individuals were tested using an unbiased high-throughput pathogen detection microfluidic system. The clinical symptoms were characterized in enrolled patients. In patients with suspected TBP infection, serological assays were conducted to test for the presence of antibodies against specific TBPs. A field study based on One Health tenets was further designed to identify components of a potential chain of infection resulting in Rickettsia felis infection in one of the patients. Ticks species infesting humans were identified as Ixodes ricinus, Rhipicephalus sanguineus sensu lato (s.l.), Dermacentor reticulatus, and Haemaphysalis punctata. Five patients developed local skin lesions at the site of the tick bite including erythema migrans, local non-specific reactions, and cutaneous hypersensitivity reaction. Although Borrelia burgdorferi s.l., Babesia microti, Anaplasma phagocytophilum, and Candidatus Cryptoplasma sp. DNAs were detected in tick samples, different Rickettsia species were the most common TBPs identified in the ticks. The presence of TBPs such as Rickettsia helvetica, Rickettsia monacensis, Borrelia lusitaniae, Borrelia burgdorferi, Borrelia afzelii, A. phagocytophilum, and B. microti in ticks was further confirmed by DNA sequencing. Two of the patients with local skin lesions had IgG reactive against spotted fever group rickettsiae, while IgM specific to B. afzelii, Borrelia garinii, and Borrelia spielmanii were detected in the patient with erythema migrans. Although R. felis infection was detected in one human blood sample, none of the components of the potential chain of infection considered in this study tested positive to this pathogen either using direct pathogen detection in domestic dogs or xenodiagnosis in ticks collected from domestic cats. The combination of high-throughput screening of TBPs and One Health approaches might help characterize chains of infection leading to human infection by TBPs, as well as prevalence of emerging rickettsial pathogens in the Balkan region.},

keywords = {One Health, rickettsia, Serbia, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Charles2021,

title = {Ticks and Tick-Borne Diseases in Central America and the Caribbean: A One Health Perspective},

author = {Roxanne A. Charles and Sergio Bermúdez and Pavle Banović and Dasiel Obregon and Adrian Alberto Díaz-Sánchez and Belkis Corona-González and Eric Marcel Charles Etter and Islay Rodríguez González and Abdul Gaffar and Abdul Jabbar and Sara Moutailler and Alejandro Cabezas-Cruz},

editor = {Mária Kazimírová},

url = {https://www.mdpi.com/2076-0817/10/10/1273},

doi = {https://doi.org/10.3390/pathogens10101273},

year  = {2021},

date = {2021-09-27},

journal = {Pathogens},

volume = {10},

number = {10},

abstract = {Ticks have complex life cycles which involve blood-feeding stages found on wild and

domestic animals, with humans as accidental hosts. At each blood-feeding stage, ticks can transmit

and/or acquire pathogens from their hosts. Therefore, the circulation of tick-borne pathogens (TBPs),

especially the zoonotic ones, should be studied in a multi-layered manner, including all components

of the chain of infections, following the ‘One Health’ tenets. The implementation of such an approach

requires coordination among major stakeholders (such as veterinarians, physicians, acarologists,

and researchers) for the identification of exposure and infection risks and application of effective

prevention measures. In this review, we summarize our current knowledge on the epidemiology of

tick-borne diseases in Central America and the Caribbean and the challenges associated with the

implementation of ‘One Health’ surveillance and control programs in the region.},

keywords = {Caribbean, Central America, One Health, tick-borne diseases, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Banović2021c,

title = {A One Health approach to study the circulation of tick-borne pathogens: A preliminary study},

author = {Pavle Banović and Adrian Alberto Díaz-Sánchez and Clemence Galon and Angélique Foucault-Simonin and Verica Simin and Dragana Mijatović and Luka Papić and Alejandra Wu-Chuang and Dasiel Obregon and Sara Moutailler and Alejandro Cabezas-Cruz },

doi = {https://doi.org/10.1016/j.onehlt.2021.100270},

year  = {2021},

date = {2021-06-01},

journal = {One Health},

abstract = {Tick-borne pathogens (TBPs) have complex life cycles involving tick vectors and vertebrate hosts. However, there is limited empirical evidence on the zoonotic circulation of TBPs. In this study, we used a One Health approach to study the possible circulation of TBPs in ticks, animals and humans within a rural household in the foothills of the Fruška Gora mountain, northern Serbia. The presence of TBP DNA was assessed using microfluidic PCR (25 bacterial species, 7 parasite species, 5 bacterial genera, 3 parasite genera) in animal, human and tick samples and the presence of tick-borne encephalitis virus (TBEV) RNA was screened for using RT-qPCR on tick samples. In addition, Lyme borreliosis serology was assessed in patient sera. Rhipicephalus sanguineus and Ixodes ricinus ticks were identified on dogs and Haemaphysalis punctata was identified on house walls. Rickettsia helvetica was the most common pathogen detected in pooled R. sanguineus and I. ricinus tick samples, followed by Hepatozoon canis. None of the H. punctata tick samples tested positive for the presence of TBPs. Anaplasma phagocytophilum and Rickettsia monacensis were the most frequent pathogens detected in dogs, followed by Rickettsia felis, whereas Anaplasma bovis was the only pathogen found in one of the goats tested. None of the human blood samples collected from family members tested positive for the presence of TBPs. Although microfluidic PCR did not detect Borrelia sp. in any of the tested tick or blood samples, a family member with a history of Lyme disease was seropositive for Borrelia burgdorferi sensu lato (s.l.). We conclude that, despite the presence of TBPs in tick and vertebrate reservoirs, there is no evidence of infection with TBPs across various components of the epidemiological chain in a rural Fruška Gora household.},

keywords = {Anaplasma bovis, One Health, Rickettsia helvetica, Tick-borne-pathogens, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Banović2021,

title = {Tick-Borne Encephalitis Virus Seropositivity among Tick Infested Individuals in Serbia},

author = {Pavle Banović and Dasiel Obregon and Dragana Mijatović and Verica Simin and Srđan Stankov and Vesna Turkulov and Siniša Sević and Zorana Budakov-Obradovic and Nevenka Bujandric and Jasmina Grujic and Adrian Alberto Díaz-Sánchez and Alejandro Cabezas-Cruz},

editor = {Sergio E. Bermúdez},

url = {https://www.mdpi.com/2076-0817/10/3/301/pdf},

doi = {https://doi.org/10.3390/ pathogens10030301},

year  = {2021},

date = {2021-03-05},

journal = {Pathogens},

volume = {10},

abstract = {Tick-borne encephalitis (TBE), caused by the TBE virus (TBEV), is a life-threatening disease

with clinical symptoms ranging from non-specific to severe inflammation of the central nervous

system. Despite TBE is a notifiable disease in Serbia since 2004, there is no active TBE surveillance

program for the serologic or molecular screening of TBEV infection in humans in the country. This

prospective cohort study aimed to assess the TBEV exposure among tick-infested individuals in

Serbia during the year 2020. A total of 113 individuals exposed to tick bites were recruited for the

study and screened for anti-TBEV antibodies using a commercial indirect fluorescent antibody test

(IFA) test. Blood samples from 50 healthy donors not exposed to tick bites were included as a control

group. Most of the enrolled patients reported infestations with one tick, being I. ricinus the most

frequent tick found in the participants. The TBEV seroprevalence was higher (13.27%, 15 total 113)

in tick-infested individuals than in healthy donors (4%, 2 total 50), although the difference was

not significant. Notably, male individuals exposed to tick bites showed five times higher relative

risk (RR) of being TBEV-seropositive than healthy donors of the same gender (RR= 5.1, CI = 1.6–19;

p = 0.007). None of the seropositive individuals developed clinical manifestations of TBE, but the first

clinical-stage of Lyme borreliosis (i.e., erythema migrans) was detected in seven of them. Potential

TBEV foci were identified in rural areas, mostly in proximity or within the Fruška Gora mountain.

We conclude that the Serbian population is at high risk of TBEV exposure. Further epidemiological

studies should focus on potential TBEV foci identified in this study. The implementation of active

surveillance for TBEV might contribute to evaluating the potential negative impact of TBE in Serbia.},

keywords = {foci, Serbia, TBEV, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Banović2020,

title = {Humans infested with Ixodes ricinus are exposed to a diverse array of tick-borne pathogens in Serbia},

author = {Pavle Banović, Adrian Alberto Díaz-Sánchez, Clemence Galon, Verica Simin, Dragana Mijatović, Dasiel Obregón, Sara Moutailler, AlejandroCabezas-Cruz

},

url = {https://www.sciencedirect.com/science/article/abs/pii/S1877959X20304799?fbclid=IwAR3nbGgtSfPEXPX54Vr7DTBcHI_KlKPum63yjfSznOTm7NFkh7PyqLzerTs},

doi = {https://doi.org/10.1016/j.ttbdis.2020.101609},

year  = {2020},

date = {2020-11-24},

journal = {Ticks and Tick-borne Diseases},

keywords = {Borrelia, rickettsia, Serbia, ticks},

pubstate = {published},

tppubtype = {article}

}

@article{Verica2020,

title = {Borellia burgdorferi infection in removed ticks and anti-borrelia antibodies in infested patients admitted to the Pasteur Institute, Novi Sad},

author = {Simin Verica and Dragana Mijatović and Snežana Tomanović and Milan Miljević and Borislav Čabrilo and Bogdan Ivana and Pavle Banović},

doi = {10.2298/VETGL200527008S},

year  = {2020},

date = {2020-10-03},

journal = {Veterinarski glasnik},

abstract = {Introduction. The primary objectives of this study were (1) to determine the presence of Borrelia burgdorferi infection in ticks removed from patients for the purpose of singling out sites with increased risk of Lyme borreliosis, and (2) to determine the presence of IgM and/or IgG antibodies against B.  burgdorferi  sensu lato (s. l.) complex in sera of patients who had ticks removed 

Materials  and  Methods.  From  108  ticks  removed  from  patients,  all  were  examined zoologically and a sub-sample of 91 ticks was tested using PCR analysis to determine the presence of DNA indicating B. burgdorferi infection. To detect anti-Borrelia IgM and/or IgG antibodies in 61 patients bitten by ticks, we used line recombinant immunoblot test.

Results and Conclusions. The most common tick identified was Ixodes ricinus. B. burgdorferi s. l. was present in 37 of 91 tested ticks (40.7%). Seroconversion against B. burgdorferi s. l. antigen was detected in 12 of 61 patients (19.7%). Most of the infected ticks were from the province of Vojvodina (11 municipalities), with the city of Novi Sad proving to be the site with the highest number of infected ticks, 6 in total. },

keywords = {Borrelia, Borrelia burgdorferi, Lyme borreliosis, Novi Sad, ticks},

pubstate = {published},

tppubtype = {article}

}