Group for Medical Entomology

 

Faunistic-ecological and virological investigations of medically significant insects and acarines constituted the main focus of the Group’s scientific work from the foundation in late 1940’s. Up to the beginning of the 2000’s, extensive studies were carried out in regions that are endemic foci of leishmaniasis, haemorrhagic fevers, and Lyme disease (Eastern, Southeastern, Western, and Central Serbia; the wider environs of Belgrade; and the region of Bar and Ulcinj in Montenegro). Since the beginning of the 2000’s, investigations of tick-borne pathogens (Babesia spp., Borrelia spp., Rickettsia spp., Anaplasma spp., Ehrlichia spp., Coxiella burnetii, Francisella spp., Bartonella spp., Crimean-Congo haemorrhagic fever virus, tick-borne encephalitis virus) have undergone intensification. Research activity has developed in several parallel directions: population-genetics and faunistic studies of the vectors; investigations of the enzootic cycles of pathogenic microorganisms transmitted by ticks; isolation, cultivation, and genotyping of tick-borne pathogens of significance for human and veterinary medicine; and research on the functions of tick saliva components and their potential application. The tradition of successful cooperation with other institutions in Serbia and abroad has continued, making possible a multi-disciplinary nature of current research and enabling investigators to keep up with state of the art trends in both the approach to scientific research and its realization. Various entomological, immunological, and molecular methods are now used by the Group’s investigators.  The maintenance of laboratory lines of ticks has been established. Since 2010, associates of the Group have worked on isolation and cultivation of the causative agent of Lyme disease the spirochaete Borrelia burgdorferi sensu lato. A collection of local isolates from the territory of Serbia has been formed that currently numbers more than 30 strains of different Borrelia species, which is exceptionally significant as a basis for development of adequate diagnostic tests and therapy of Lyme disease in our country. One of the key results of research conducted to date is the elaboration of precise ecological profiles of tick vectors, containing condensed information about their geographical distribution, potential hosts, role in transmission of pathogens, bionomy, and the habitats in which they live. The obtained data will be used for formation of a geographical information system (GIS) and for development of mathematical models of prediction.  In 2012 associates of the Group summarized the results of research conducted up to that time in a monograph entitled “Ticks (Acari: Ixodidae, Argasidae) of Serbia”, which was published by the Serbian Academy of Sciences and Arts. The following year this monograph received the prestigious Award of the City of Belgrade. Apart from their scientific importance, the results of research carried out by associates of the Medical Entomology Group are also of applied value in clinical practice, since a knowledge of the diversity and characteristics of pathogens on the local level is of crucial significance for reliable diagnosis and effective prevention of diseases. The knowledge gained in the course of research is utilized through expertise in biological testing for the presence of ticks and tick-borne pathogens, estimation of risks, and design and development of new strategies for controlling the distribution and transmission of pathogens carried by vectors. Associates of the Group participate in teaching on the levels of both basic and doctoral studies at Belgrade University’s of Faculty of Biology.

Since 2010, the Group has been part of the Centre of Excellence for Food and Vector-borne Zoonoses.

Teaching activities

 

- Dr Snežana Tomanović  (since 2014) - acredited mentor, PhD studies at Faculty of Biology, University of Belgrade

- Dr Snežana Tomanović (since 2014) – lecturer, PhD studies at Faculty of Biology, University of Belgrade

RESEARCH PROJECTS (1997-2018)

National projects coordinated by IMR:

Руководилац пројекта: Проф. Др Златибор Петровић, Академик

Сарадник из ИМИ: Марија Милутиновић

Српска академија наука и уметности, 1986-1990

1994-1997: Ecological research of hematophagous arthropods and their role in the transmission of parasitic and viral diseases of humans. Project coordinator: Dr. Zoran Miščević

Руководилац пројекта: Ими, Др Зоран Мишчевић

Министарство науке, технологије и развоја, 1994-1997

1994-1998: Determining the presence of ticks (Acari: Ixodidae) and their protozoa infestation. Project coordinators: Dr. Zoran Miščević, Dr. Marija Milutinović

Руководилац пројекта: ИМИ, Др Зоран Мишчевић, Др Марија Милутиновић

Министарство науке, технологије и развоја, 1994-1998

1996-2000: Research on hematofagous arthropods and their role in the transmission of parasitic and viral diseases. Project coordinators: Dr. Zoran Miščević (1996-1999), Dr. Marija Milutinović (2000)

Руководилац пројекта: ИМИ, Др Зоран Мишчевић (1996-1999), Др Марија Милутиновић (2000)

Министарство науке и технолошког развоја, 1996-2000

2002-2005: Ticks as reservoirs and vectors of infectious agents. Project coordinator: Dr. Marija Milutinović

Руководилац пројекта: ИМИ, Др Марија Милутиновић

Министарство науке, технологије и развоја, 2002-2005

2006-2010: Intracellular microorganism-induced (re)emerging infections: transmission, molecular epidemiology, host-pathogen relationship, and clinical relevance (145002). Project coordinator: Dr. Olgica Đurković 

Руководилац пројекта: ИМИ, Др Олгица Ђурковић Ђаковић

Министарство науке и заштите животне средине Републике Србије, 2006-2010

2011-    : Enzootic transmission cycles of pathogenic microorganisms transmitted by ticks (ОИ173006). Project coordinator: Dr. Snežana Tomanović

Сарадник из ИМИ: Др Снежана Томановић, члан радних група 4 и 5 (WG4 и WG5)

Број пројекта: COST Action TD1303, 2013-2017,

Project financed by European Comission:

Студија случаја болести преносивих комарцима и крпељима у различитим условима станишта, окружења и климатских услова.Билатерална научна сарадња: Научна сарадња између Републике Србије и Италије, 2013-2015

Руководилац пројекта из Србије: Др Душко Ћировић, Билошки факултет, Универзитет у Београду

Сарадник из ИМИ: Др Снежана Томановић, Сања Ћакић докторант, Ратко Сукара докторант, Дарко Михаљица докторант

Руководилац пројекта из Италије: Др Паоло Тицијани, Унивезитет у Торину

Project financed by European Comission:

SERBPARZOON – Reinforcement of the Serbian Centre for Parasitic Zoonoses

Руководилац пројекта/Главни истраживач: ИМИ, Др Олгица Ђурковић Ђаковић

Број пројекта: FP6-2005-INCO-WBC/SSA-3 (2007-2009)

2001-2009 Reinforcement of the Serbian Centre for Parasitic Zoonoses- SERBPARZOON (FP6-2005-INCO-WBC/SSA-3)– SERBPARZOON. Coordinator: Dr Olgica Đurković Đaković

Билатерална научна сарадња: Научна сарадња између Републике Србије и Словеније, 2010-2011

Руководилац пројекта из Србије: ИМИ, Др Снежана Томановић

Руководилац пројекта из Словеније: Медицински факултет, Универзитет у Љубљани, ИМИ, Др Ева Ружић Сабљић

Bibliography


Milutinović M, Bobić B (1997): Ecological investigations on ticks (Acari, Ixodidae) in the area of East Serbia with emphasis on the species Ixodes ricinus and Hyalomma savignyi. Arq Bras Med Vet Zoo 49: 531-541. 

Radulović Ž, Milutinović M, Anđelković M, Vujčić Z, Tomanović S, Božić N, Marinković D (2006): Allozyme polymorphism of Mdh and α-Gpdh in Ixodes ricinus populations: comparison of borreliae-infected and uninfected ticks. Exp Appl Acarol 40: 113-121.

Milutinović M, Pavlović I, Kulišić Z (1997): Fauna of ticks (Acari, Ixodidae, Argasidae) of South-East Kosovo. Acta Vet-Beograd 47: 167-170. 

Pavlović I, Kulišić Z, Milutinović M (1997): The role of foxes (Vulpes vulpes L.) in the epidemiology of Nematode parasitic zoonoses. Acta Vet-Beograd 47:2-3, 177-182. 

Ristanović, E, Kitamura K, Masuzawa T, Milutinovic M, Čekanac R, Stajkovic N, Zivanovic D (2007): Molecular characterization of Borrelia burgdorferi sensu lato strains isolated in the area of Belgrade, Serbia. Braz J Microbiol. 38: 14-16.


Milutinović M, Aleksić-Bakrač N, Pavlović I (1997/8): Faunistic and ecological notes on ticks (Acari: Ixodidae, Argasidae) in the extended area of Belgrade. Magy Allatorvosok 120: 434-436. 

Milutinović M, Masuzawa T, Tomanović S, Radulović Ž, Fukui T, Okamoto Y (2008): Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol 45: 171-183.

Peštalić H, Milutinović M, Kulišić Z, Aleksić-Bakrač N, Pavlović I (1997): Influence of age and education of patients on prevalence Giardia lamblia in human. J Protozool Res 7: 122-126.

Milutinović M, Radulović Ž, Tomanović S (2008): Assessment of the risk of the contracting Lyme disease in areas with significant human presence. Arq Bras Med Vet Zoo 60: 121-129.

Kulišić Z, Pavlović I, Milutinović M, Aleksić-Bakrać N. (1998):  Intestinal parasites of dogs and role of dogs in epidemiology of Larva migrans in the Belgrade area. Helminthologia   35: 79 – 82. 

Radulović Ž, Milutinović M, Tomanović S, Mulenga A (2010): Exon variability of gene encoding glycerol-3-phosphate dehydrogenase of Ixodes ricinus ticks. Parasite 17: 363-368.

Milutinović, M (2000): Diversity and ecology of the ixodid ticks (Acari: Ixodidae) in central Serbia, Yugoslavia. Arch Biol Sci 52: 39-46.

Radulović Ž, Milutinović M, Tomanović S, Mulenga A (2010): Detection of Borrelia-specific 16S rRNA sequence in total RNA extracted from Ixodes ricinus ticks. Arq Bras Med Vet Zoo 62: 862-867.

Milutinović M, Radulović Z (2002): Ecological notes on ticks (Acari: Ixodidae) in Serbia (central regions) Acta Vet-Beograd 52: 49-58. 

Tomanović S, Radulović Ž, Masuzawa T, Milutinović M (2010): Coexistence of emerging bacterial pathogens in Ixodes ricinus ticks in Serbia. Parasite 17: 211-217.

Milutinović M, Radulović Ž, Jovičić V, Oreščanin Z (2004): Population dynamics and Borrelia burgdorferi infection rate of Ixodes ricinus ticks in the Belgrade area. Acta Vet-Beograd 54: 219-225. 

Tomanović S, Radulović Ž, Masuzawa T, Milutinović M, Stanisavljević LJ (2010): Potential infectivity of Anaplasma phagocytophilum strains in Ixodes ricinus ticks from Serbia. Acta Vet Hung 58: 231-242.

Athanassiou CG, Kavallieratos NG, Tomanović Ž, Tomanović S, Milutinović M (2005): Development of a sampling plan for Myzus persicae (Hemiptera: Aphidoidea) and its predator Macrolophus costalic (Hemiptera: Miridae)) on tabaco. Eur J Entomol 102: 399-405

Radulović Ž, Chochlakis D, Tomanović S, Milutinović M, Tselentis Y, Psaroulaki A (2011): First detection of spotted fever group rickettsiae in ticks in Serbia. Vector-Borne Zoonot 11: 111-115.

Ristanović, E, Kitamura K, Masuzawa T, Milutinovic M, Čekanac R, Stajkovic N, Zivanovic D (2007): Molecular characterization of Borrelia burgdorferi sensu lato strains isolated in the area of Belgrade, Serbia. Braz J Microbiol. 38: 14-16. 

Radulović Ž, Milutinović M, Tomanović S, Mihaljica, Ćakić S, Stamenković-Radak M, Anđelković M (2012): Seasonal and spatial occurence of glycerol-3-phosphate dehydrogenase variability in Ixodes ricinus (Acari: Ixodidae) populations. J Med Entomol 49(3): 497-503.

Milutinović M, Masuzawa T, Tomanović S, Radulović Ž,  Fukui T, Okamoto Y (2008): Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum, Francisella tularensis and their co-infections in host-seeking Ixodes ricinus ticks collected in Serbia. Exp Appl Acarol 45: 171-183. 

Tomanović S, Chochlakis D, Radulović Ž, Milutinović M, Ćakić S, Mihaljica D, Tselentis Y, Psaroulaki A (2013): Analysis of pathogen co-occurence in host-seeking adult hard ticks from Serbia. Exp Appl Acarol 59(3): 367-376.

Milutinović M, Radulović Ž, Tomanović S (2008): Assessment of the risk of the contracting Lyme disease in areas with significant human presence. Arq Bras Med Vet Zoo 60: 121-129.

Ćakić S, Mojsilović M, Mihaljica D, Milutinović M, Petrović A, Tomanović S (2014): Molecular characterization of COI gene of Ixodes ricinus (Linnaeus, 1785) from Serbia. Arch Biol Sci 66(2): 683-690.

Radulović Ž, Milutinović M, Tomanović S, Mulenga A (2010): Exon variability of gene encoding glycerol-3-phosphate dehydrogenase of Ixodes ricinus ticks. Parasite 17: 363-368. 

Burazerović J, Ćakić S, Mihaljica D, Sukara R, Ćirović D, Tomanović S (2015): Ticks (Acari: Argasidae, Ixodidae) parasitizing bats in the central Balkans . Exp Appl Acarol 66: 281-291.

Radulović Ž, Milutinović M, Tomanović S, Mulenga A (2010): Detection of Borrelia-specific 16S rRNA sequence in total RNA extracted from Ixodes ricinus ticks. Arq Bras Med Vet Zoo 62: 862-867. 

Davitkov D, Vučićević M, Stevanović J, Krstić V, Tomanović S, Glavinić U, Stanimirović Z (2015): Clinical babesiosis and molecular identification of Babesia canis and Babesia gibsoni infections in dogs from Serbia. Acta Vet Hung 63 (2), 199-208

Tomanović S, Radulović Ž, Masuzawa T, Milutinović M (2010): Coexistence of emerging bacterial pathogens in Ixodes ricinus ticks in Serbia. Parasite 17: 211-217. 

Hornok S, Kontschán J, Estrada-Peña A, Fernández de Mera I, Tomanović S, de la Fuente J (2015) Contributions to the morphology and phylogeny of the newly discovered bat tick species, Ixodes ariadnae in comparison with I. vespertilionis and I. simplex. Parasite Vectors 8:47.

Tomanović S, Radulović Ž, Masuzawa T, Milutinović M, Stanisavljević LJ (2010): Potential infectivity of Anaplasma phagocytophilum strains in Ixodes ricinus ticks from Serbia. Acta Vet Hung 58: 231-242. 

Hornok S, Kontschán J, Plantard O, Kunz B, Mihalca AD, Thabah A, Tomanović S, Burazerović J, Takács N, Görföl T, Estók P, Tan Tu V, Szőke K, Fernández de Mera IG, de la Fuente H, Takahashi M, Yamauchi T,Takano A (2015): “High Degree of Mitochondrial Gene Heterogeneity in the Bat Tick Species Ixodes Vespertilionis, I. Ariadnae and I. Simplex from Eurasia. Parasit Vectors 8(1).

Radulović Ž, Chochlakis D, Tomanović S, Milutinović M, Tselentis Y, Psaroulaki A (2011): First detection of spotted fever group rickettsiae in ticks in Serbia. Vector-Borne Zoonot 11: 111-115. 

Hornok S, Sándor AD, Tomanović S, Beck R,D’Amico G, Kontschán J, Takács N, Görföl T, Bendjeddou ML, Földvári G, Farkas R (2017) : East and West Separation of Rhipicephalus Sanguineus Mitochondrial Lineages in the Mediterranean Basin. Parasit Vectors 10(1).

Mihaljica D, Radulović Ž, Tomanović S, Ćakić S, Penezić A, Milutinović M (2012): Molecular detection of Babesia spp. in northern Serbia. Arch Biol Sci 64(4): 1591-1598. 

Mihaljica D, Marković D, Radulović Ž, Mulenga A, Ćakić S, Sukara R, Samardžić J, Tomanović S (2017): Ixodes ricinus immunogenic saliva protein, homologue to Amblyomma americanum AV422: Determining its potential for use in tick bite confirmation. Ticks Tick-Borne Dis 8: 391-395.

Radulović Ž, Milutinović M, Tomanović S, Mihaljica, Ćakić S, Stamenković-Radak M, Anđelković M (2012): Seasonal and spatial occurence of glycerol-3-phosphate dehydrogenase variability in Ixodes ricinus (Acari: Ixodidae) populations.  J Med Entomol 49(3): 497-503. 

Pajnik J, Stamenić M, Radetić M, Tomanović S, Sukara R, Mihaljica D, Zizović I (2017): Impregnation of cotton fabric with pyrethrum extract in supercritical carbon dioxide. J Supercrit Fluid 128: 66-72.

Tomanović S, Chochlakis D, Radulović Ž, Milutinović M, Ćakić S, Mihaljica D, Tselentis Y, Psaroulaki A (2013): Analysis of pathogen co-occurence in host-seeking adult hard ticks from Serbia. Exp Appl Acarol 59(3): 367-376.

Radulović Ž, Mihaljica D, Ćosić N, Penezić A, Ćakić S, Sukara R, Ćirović D, Tomanović S (2017): Hard Ticks Parasitizing European Ground Squirrel (Spermophilus Citellus) in Serbia. Acta Zool Bulg In press

Starý P, Kavallieratos NG, Petrović A, Žikić V, Rakhshani E, Tomanović S, Tomanović Ž, Havelka J (2014): Interference of Field Evidence, Morphology, and DNA Analyses of Three Related Lysiphlebus Aphid Parasitoids (Hymenoptera: Braconidae: Aphidiinae) . J Insect Sci 14 (1): 171

Ćakić S, Mojsilović M, Mihaljica D, Milutinović M, Petrović A, Tomanović S (2014): Molecular characterization of COI gene of Ixodes ricinus (Linnaeus, 1785) from Serbia. Arch Biol Sci 66(2): 683-690.
Burazerović J, Ćakić S, Mihaljica D, Sukara R, Ćirović D, Tomanović S (2015): Ticks (Acari: Argasidae, Ixodidae) parasitizing bats in the central Balkans . Exp Appl Acarol  66: 281-291.

Davitkov D, Vučićević M, Stevanović J, Krstić V, Tomanović S, Glavinić U, Stanimirović Z (2015): Clinical babesiosis and molecular identification of Babesia canis and Babesia gibsoni infections in dogs from Serbia. Acta Vet Hung 63 (2), 199-208

Hornok S, Kontschán J, Estrada-Peña A, Fernández de Mera I, Tomanović S, de la Fuente J (2015) Contributions to the morphology and phylogeny of the newly discovered bat tick species, Ixodes ariadnae in comparison with I. vespertilionis and I. simplex. Parasite Vectors 8:47.

Hornok S, Kontschán J, Plantard O, Kunz B, Mihalca AD, Thabah A, Tomanović S, Burazerović J, Takács N, Görföl T, Estók P, Tan Tu V, Szőke K, Fernández de Mera IG, de la Fuente H, Takahashi M, Yamauchi T,Takano A (2015): “High Degree of Mitochondrial Gene Heterogeneity in the Bat Tick Species Ixodes vespertilionis, I. ariadnae and I. simplex from Eurasia. Parasit Vectors 8(1).

Rakhshani E , Starý P ,  Hidalgo NP , Čkrkić J, Moghaddam MG , Tomanović S, Petrović A, Tomanović Ž (2015): Revision of the World Monoctonia Starý, Parasitoids of Gall Aphids: Taxonomy, Distribution, Host Range, and Phylogeny (Hymenoptera, Braconidae: Aphidiinae). Zootaxa 3905(1):474–88.

 Hornok S, Sándor AD, Tomanović S, Beck R,D’Amico G, Kontschán J, Takács N, Görföl T, Bendjeddou ML, Földvári G, Farkas R (2017) : East and West Separation of Rhipicephalus sanguineus Mitochondrial Lineages in the Mediterranean Basin. Parasit Vectors 10(1).

Mihaljica D, Marković D, Radulović Ž, Mulenga A, Ćakić S, Sukara R, Samardžić J, Tomanović S (2017): Ixodes ricinus immunogenic saliva protein, homologue to Amblyomma americanum AV422: Determining its potential for use in tick bite confirmation. Ticks Tick-Borne Dis 8: 391-395.

Pajnik J, Stamenić M, Radetić M, Tomanović S, Sukara R, Mihaljica D, Zizović I (2017): Impregnation of cotton fabric with pyrethrum extract in supercritical carbon dioxide. J Supercrit Fluid 128: 66-72.
Radulović Ž, Mihaljica D, Ćosić N, Penezić A, Ćakić S, Sukara R, Ćirović D, Tomanović S (2017): Hard Ticks Parasitizing European Ground Squirrel (Spermophilus citellus) in Serbia. Acta Zool Bulg  

Burazerović J, Orlova M, Obradović M, Ćirović D, Tomanović S. (2017): Patterns of abundance and host specificity of bat ectoparasites in the central Balkans. J Medl Entomol,  DOI. 10.1093/jme/tjx189

Милутиновић М, Радуловић Ж, Томановић С, Петровић З. (2012) Крпељи (Acari: Ixodidae, Argasidae) Србије. Српска академија наука и уметности, Београд.

MONOGRAPH

Milutinović M, Radulović Ž, Tomanović S, Petrović Z (2012): Ticks (Acari: Ixodidae, Argasidae) of Serbia. Serbian Academy of Science and Arts, Belgrade

PhD THESES

 

Radulović Ž (2010): Spatial and temporal distribution of gene variability for glycerol-3-phosphate dehydrogenase in tick populations (Ixodes ricinus L.). PhD thesis. Faculty of Biology, University of Belgrade (Dr Marija Milutinović (IMR), mentor)

 

Tomanović S (2009): Molecular detection and characterization of bacteria Borrelia burgdorferi, Anaplasma phagocytophilum and Francisella tularensis in ticks Ixodes ricinus in Serbia. PhD thesis. Faculty of Biology, University of Belgrade (Dr Marija Milutinović (IMR), mentor)