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Genetic characterization of spotted fever group rickettsiae in questing ixodid ticks collected in Israel and environmental risk factors for their infection

Published online by Cambridge University Press:  23 March 2017

Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel
Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel
Department of Microbiology and Molecular Genetics, The Kuvin Center for the Study of Infectious and Tropical Diseases, Hebrew University–Hadassah Medical School, Jerusalem, Israel
Environment and Life Sciences Research Center, Kuwait Institute for Scientific Research, Kuwait City, Kuwait Department of Veterinary Population Medicine, College of Veterinary Medicine, University of Minnesota, St. Paul, USA
The GIS Center, Hebrew University of Jerusalem, Jerusalem, Israel
Department of Geography and Environment, Bar-Ilan University, Ramat-Gan, Israel
Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel
Al-Quds Public Health Society, Jerusalem, Palestinian territories, Palestine
Al-Quds Public Health Society, Jerusalem, Palestinian territories, Palestine
Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel
*Corresponding author: Koret School of Veterinary Medicine, The Hebrew University of Jerusalem, Rehovot, Israel. E-mail:


This study aimed to genetically characterize spotted fever group rickettsiae (SFGR) in questing ixodid ticks from Israel and to identify risk factors associated with SFGR-positive ticks using molecular techniques and geographic information systems (GIS) analysis. 1039 ticks from the genus Rhipicephalus were collected during 2014. 109/1039 (10·49%) carried SFGR-DNA of either Rickettsia massiliae (95), ‘Candidatus Rickettsia barbariae’ (8) or Rickettsia conorii (6). Higher prevalence of SFGR was found in Rhipicephalus turanicus (18·00%) compared with Rhipicephalus sanguineus sensu lato (3·22%). Rickettsia massiliae was the most commonly detected species and the most widely disseminated throughout Israel (87·15% of all Rickettsia-positive ticks). GIS analysis revealed that Central and Northern coastal regions are at high risk for SFGR. The presence of ticks was significantly associated with normalized difference vegetation index and temperature variation over the course of the year. The presence of rickettsiae was significantly associated with brown type soils, higher land surface temperature and higher precipitation. The latter parameters may contribute to infection of the tick with SFGR. Health care professionals should be aware of the possible exposure of local communities and travellers to R. massillae. Molecular and geographical information can help professionals to identify areas that are susceptible to SFGR-infected ticks.

Research Article
Copyright © Cambridge University Press 2017 

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These authors contributed equally.



Abdel-Shafy, S., Allam, N. A. T., Mediannikov, O., Parola, P. and Raoult, D. (2012). Molecular detection of spotted fever group rickettsiae associated with ixodid ticks in Egypt. Vector Borne and Zoonotic Diseases 12, 346359.Google Scholar
Abramson, J. H. (2011). WINPEPI updated: computer programs for epidemiologists, and their teaching potential. Epidemiologic Perspectives & Innovations 8, 19.Google Scholar
Aharonowitz, G., Koton, S., Segal, S., Anis, E. and Green, M. S. (1999). Epidemiological characteristics of spotted fever in Israel over 26 years. Clinical Infectious Diseases 29, 13211322.CrossRefGoogle ScholarPubMed
Alkhamis, M. A. and VanderWaal, K. (2016). Spatial and temporal epidemiology of lumpy skin disease in the Middle East, 2012–2015. Frontiers in Veterinary Science 3, 112.CrossRefGoogle ScholarPubMed
Alkhamis, M., Hijmans, R. J., Al-Enezi, A., Martínez-López, B. and Perea, A. M. (2016). The use of spatial and spatiotemporal modeling for surveillance of H5N1 highly pathogenic avian influenza in poultry in the Middle East. Avian Diseases 60, 146155.Google Scholar
Bacellar, F., Regnery, R. L., Núncio, M. S. and Filipe, A. R. (1995). Genotypic evaluation of rickettsial isolates recovered from various species of ticks in Portugal. Epidemiology and Infection 114, 169178.CrossRefGoogle ScholarPubMed
Barandika, J. F., Olmeda, S. A., Casado-Nistal, M. A., Hurtado, A., Juste, R. A., Valcárcel, F., Anda, P. and García-Pérez, A. L. (2011). Differences in questing tick species distribution between Atlantic and continental climate regions in Spain. Journal of Medical Entomology 48, 1319.Google Scholar
Beeler, E., Abramowicz, K. F., Zambrano, M. L., Sturgeon, M. M., Khalaf, N., Hu, R., Dasch, G. A. and Eremeeva, M. E. (2011). A focus of dogs and Rickettsia massiliae-infected Rhipicephalus sanguineus in California. American Journal of Tropical Medicine and Hygiene 84, 244249.Google Scholar
Blanco, J. and Oteo, J. (2006). Rickettsiosis in Europe. Annals of the New York Academy of Sciences 1078, 2633.CrossRefGoogle ScholarPubMed
Brumin, M., Levy, M. and Ghanim, M. (2012). Transovarial transmission of rickettsia spp. and organ-specific infection of the whitefly Bemisia tabaci . Applied and Environmental Microbiology 78, 55655574.CrossRefGoogle ScholarPubMed
Chochlakis, D., Ioannou, I., Sandalakis, V., Dimitriou, T., Kassinis, N., Papadopoulos, B., Tselentis, Y. and Psaroulaki, A. (2012). Spotted fever group rickettsiae in ticks in Cyprus. Microbial Ecology 63, 314323.Google Scholar
Chochlakis, D., Ioannou, I., Papadopoulos, B., Tselentis, Y. and Psaroulaki, A. (2014). Rhipicephalus turanicus: from low numbers to complete establishment in Cyprus. Its possible role as a bridge-vector. Parasites & Vectors 7, P11.CrossRefGoogle Scholar
Dantas-Torres, F., Chomel, B. B. and Otranto, D. (2012). Ticks and tick-borne diseases: a One Health perspective. Trends in Parasitology 28, 437446.Google Scholar
Donaldson, T. G., Pèrez de León, A. A., Li, A. I., Castro-Arellano, I., Wozniak, E., Boyle, W. K., Hargrove, R., Wilder, H. K., Kim, H. J., Teel, P. D. and Lopez, J. E. (2016). Assessment of the geographic distribution of Ornithodoros turicata (Argasidae): climate variation and host diversity. PLoS Neglected Tropical Diseases 10, e0004383.Google Scholar
Elith, J. and Leathwick, J. R. (2009). Species distribution models: ecological explanation and prediction across space and time. Annual Reviews of Ecology, Evolution, and Systematics 40, 677697.Google Scholar
Elith, J., Graham, C. H., Anderson, R. P., Dudík, M., Ferrier, S., Guisan, A., Hijmans, R. J., Huettmann, F., Leathwick, J. R., Lehmann, A., Li, J., Lohmann, L. G., Loiselle, B. A., Manion, G., Moritz, C., Nakamura, M., Nakazawa, Y., Overton, J. M. M., Townsend Peterson, A., Phillips, S. J., Richardson, K., Scachetti-Pereira, R., Schapire, R. E., Soberón, J., Williams, S., Wisz, M. S. and Zimmermann, N. E. (2006). Novel methods improve prediction of species’ distributions from occurrence data. Ecography 29, 129151.Google Scholar
Eremeeva, M. E., Bosserman, E. A., Demma, L. J., Zambrano, M. L., Blau, D. M. and Dasch, G. A. (2006). Isolation and identification of Rickettsia massiliae from Rhipicephalus sanguineus ticks collected in Arizona. Applied and Environmental Microbiology 72, 55695577.Google Scholar
Ereqat, S., Nasereddin, A., Al-Jawabreh, A., Azmi, K., Harrus, S., Mumcuoglu, K., Apanaskevich, D. and Abdeen, Z. (2016). Molecular detection and identification of spotted fever group rickettsiae in ticks collected from the West Bank, Palestinian territories. PLoS Neglected Tropical Diseases 10, e0004348.Google Scholar
Estrada-Peña, A. and Jongejan, F. (1999). Ticks feeding on humans: a review of records on human-biting Ixodoidea with special reference to pathogen transmission. Experimental and Applied Acarology 23, 685715.Google Scholar
Estrada-Peña, A., Ayllón, N. and de la Fuente, J. (2012). Impact of climate trends on tick-borne pathogen transmission. Frontiers in Physiology 3, 112.CrossRefGoogle ScholarPubMed
Feldman-Muhsam, B. (1951). A note on east mediterranean species of the Haemaphysalis. Bulletin Research Council Israel 1, 96107.Google Scholar
Fernandez-Soto, P., Perez-Sanchez, P., Alamo-Sanz, P. and Encinas-Grandes, A. (2006). Spotted fever group rickettsiae in ticks feeding on humans in northwestern Spain: is Rickettsia conorii vanishing? Annals of the New York Academy of Sciences 1078, 331333.CrossRefGoogle Scholar
Gray, J., Dantas-Torres, F., Estrada-Peña, A. and Levin, M. (2013). Systematics and ecology of the brown dog tick, Rhipicephalus sanguineus . Ticks and Tick-Borne Diseases 4, 171180.CrossRefGoogle ScholarPubMed
Guberman, D., Mumcuoglu, Y. K., Keysary, A., Ioffe-Uspensky, I., Miller, J. and Galun, R. (1996). Prevalence of spotted fever group rickettsiae in ticks from southern Israel. Journal of Medical Entomology 33, 979982.Google Scholar
Harrus, S., Perlman-Avrahami, A., Mumcuoglu, K. Y., Morick, D. and Baneth, G. (2011). Molecular detection of Rickettsia massiliae, Rickettsia sibirica mongolitimonae and Rickettsia conorii israelensis in ticks from Israel. Clinical Microbiology and Infection 17, 176180.CrossRefGoogle ScholarPubMed
Hijmans, R. J. and van Etten, J. (2013). Raster: geographic data analysis and modeling. R Package Version 2, 15.Google Scholar
Hijmans, R. J., Cameron, S. E., Parra, J. L., Jones, P. G. and Jarvis, A. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25, 19651978.CrossRefGoogle Scholar
Hijmans, R. J., Phillips, S., Leathwick, J. and Elith, J. (2016). Dismo: Species distribution modeling. Accessed September 2016, available at: Scholar
Illoldi-Rangel, P., Rivaldi, C., Sissel, B., Trout Fryxell, R., Gordillo-Pérez, G., Rodríguez-Moreno, A., Williamson, P., Montiel-Parra, G., Sánchez-Cordero, V. and Sarkar, S. (2012). Species distribution models and ecological suitability analysis for potential tick vectors of lyme disease in Mexico. Journal of Tropical Medicine 2012, 110.Google Scholar
Ioffe-Uspensky, I., Mumcuoglu, K. Y., Uspensky, I. and Galun, R. (1997). Rhipicephalus sanguineus and R. turanicus (Acari:Ixodidae): closely related species with different biological characteristics. Journal of Medical Entomology 34, 7481.Google Scholar
Jongejan, F. and Uilenberg, G. (2004). The global importance of ticks. Parasitology 129, S3S14.Google Scholar
Karbowiak, G., Biernat, B., Stańczak, J., Szewczyk, T. and Werszko, J. (2016). The role of particular tick developmental stages in the circulation of tick-borne pathogens affecting humans in Central Europe. 3. Rickettsiae. Annals of Parasitology 62, 89100.Google Scholar
Keysary, A., Eremeeva, M. E., Leitner, M., Din, A. B., Wikswo, M. E., Mumcuoglu, K. Y., Inbar, M., Wallach, A. D., Shanas, U., King, R. and Waner, T. (2011). Spotted fever group rickettsiae in ticks collected from wild animals in Israel. American Journal of Tropical Medicine and Hygiene 85, 919923.Google Scholar
Kidd, L., Maggi, R., Diniz, P. P. V. P., Hegarty, B., Tucker, M. and Breitschwerdt, E. (2008). Evaluation of conventional and real-time PCR assays for detection and differentiation of spotted fever group rickettsia in dog blood. Veterinary Microbiology 129, 294303.CrossRefGoogle ScholarPubMed
Lalzar, I., Harrus, S., Mumcuoglu, K. Y. and Gottlieb, Y. (2012). Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Applied and Environmental Microbiology 78, 41104116.Google Scholar
Levin, M. L., Killmaster, L., Eremeeva, M. E. and Dasch, G. A. (2009). Effects of Rickettsia conorii infection on the survival of Rhipicephalus sanguineus ticks. Clinical Microbiology and Infection 15 (Suppl 2), 277278.Google Scholar
Levin, M. L., Zemtsova, G. E., Montgomery, M. and Killmaster, L. F. (2014). Effects of homologous and heterologous immunization on the reservoir competence of domestic dogs for Rickettsia conorii (israelensis). Ticks and Tick-Borne Diseases 5, 3340.Google Scholar
Márquez, F. J. (2008). Spotted fever group rickettsia in ticks from southeastern Spain natural parks. Experimental and Applied Acarology 45, 185194.Google Scholar
Márquez, F. J., Rodríguez-Liébana, J. J., Soriguer, R. C., Muniaín, M. A., Bernabeu-Wittel, M., Caruz, A. and Contreras-Chova, F. (2008). Spotted fever group rickettsia in brown dog ticks Rhipicephalus sanguineus in southwestern Spain. Parasitology Research 103, 119122.Google Scholar
Matsumoto, K., Ogawa, M., Brouqui, P., Raoult, D. and Parola, P. (2005). Transmission of Rickettsia massiliae in the tick, Rhipicephalus turanicus . Medical and Veterinary Entomology 19, 263270.Google Scholar
Milhano, N., Popov, V., Vilhena, M., Bouyer, D. H., de Sousa, R. and Walker, D. H. (2014). Quantitative study of Rickettsia massiliae in Rhipicephalus sanguineus organs. Ticks and Tick-Borne Diseases 5, 709714.Google Scholar
Mumcuoglu, K. Y., Keysary, A. and Gilead, L. (2002). Mediterranean spotted fever in Israel: a tick-borne disease. IMAJ 4, 4449.Google Scholar
Ogden, N. H., Lindsay, L. R., Beauchamp, G., Charron, D., Maarouf, A., O'Callaghan, C. J., Waltner-Toews, D. and Barker, I. K. (2004). Investigation of relationships between temperature and developmental rates of tick Ixodes scapularis (Acari: Ixodidae) in the laboratory and field. Journal of Medical Entomology 41, 622633.Google Scholar
Parola, P., Socolovschi, C. and Raoult, D. (2009). Deciphering the relationships between Rickettsia conorii conorii and Rhipicephalus sanguineus in the ecology and epidemiology of Mediterranean spotted fever. Annals of the New York Academy of Sciences 1166, 4954.Google Scholar
Pegram, R. G., Clifford, C. M., Walker, J. B. and Keirans, J. E. (1987). Clarification of the Rhipicephalus sanguineus group (Acari, Ixodoidea, Ixodidae). I. R. sulcatus Neumann, 1908 and R. turanicus Pomerantsev, 1936. Systematic Parasitology 10, 326.CrossRefGoogle Scholar
Phillips, S. J. S. J., Anderson, R. P. R. P. and Schapire, R. E. R. E. (2006). Maximum entropy modeling of species geographic distributions. Ecological Modelling 190, 231259.CrossRefGoogle Scholar
Quintana, M., Salomón, O., Guerra, R., De Grosso, M. L., Fuenzalida, A., Lizarralde De Grosso, M. and Fuenzalida, A. (2013). Phlebotominae of epidemiological importance in cutaneous leishmaniasis in northwestern Argentina: risk maps and ecological niche models. Medical and Veterinary Entomology 27, 3948.Google Scholar
R Development Core Team (2015). R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing Vienna Austria 0, {ISBN} 3-900051-07-0.Google Scholar
Randolph, S. E. (2009). Tick-borne disease systems emerge from the shadows: the beauty lies in molecular detail, the message in epidemiology. Parasitology 136, 14031413.CrossRefGoogle ScholarPubMed
Raoult, D. and Roux, V. (1997). Rickettsioses as paradigms of new or emerging infectious diseases. Clinical Microbiology Reviews 10, 694719.CrossRefGoogle ScholarPubMed
Reeves, T., Samy, A. M. and Peterson, A. T. (2015). MERS-CoV geography and ecology in the Middle East: analyses of reported camel exposures and a preliminary risk map. BMC Research Notes 8, 801.Google Scholar
Roux, V., Fournier, P. E. and Raoult, D. (1996). Differentiation of spotted fever group rickettsiae by sequencing and analysis of restriction fragment length polymorphism of PCR-amplified DNA of the gene encoding the protein rOmpA. Journal of Clinical Microbiology 34, 20582065.Google Scholar
Rudakov, N. V., Shpynov, S. N., Samoilenko, I. E. and Tankibaev, M. A. (2003). Ecology and epidemiology of spotted fever group rickettsiae and new data from their study in Russia and Kazakhstan. Annals of the New York Academy of Sciences 990, 1224.Google Scholar
Scholte, R. G. C., Carvalho, O. S., Malone, J. B., Utzinger, J. and Vounatsou, P. (2012). Spatial distribution of Biomphalaria spp., the intermediate host snails of Schistosoma mansoni, in Brazil. Geospatial Health 6, S95S101.Google Scholar
Soberon, J. and Peterson, T. A. (2005). Interpretation of models of fundamental ecological niches and species distributional areas. Biodiversity Informatics 2, 110.Google Scholar
Socolovschi, C., Gaudart, J., Bitam, I., Huynh, T. P., Raoult, D. and Parola, P. (2012). Why are there so few Rickettsia conorii conorii-infected Rhipicephalus sanguineus ticks in the wild? PLoS Neglected Tropical Diseases 6, e1697.CrossRefGoogle ScholarPubMed
Tamura, K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition–transversion and G+C-content biases. Molecular Biology and Evolution 9, 978987.Google ScholarPubMed
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013). MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Molecular Biology and Evolution 30, 27252729.Google Scholar
Vitale, G., Mansuelo, S., Rolain, J.-M. and Raoult, D. (2006). Rickettsia massiliae human isolation. Emerging Infectious Diseases 12, 174175.Google Scholar
Walker, D. H. (1998). Tick-transmitted infectious diseases in the United States. Annual Review of Public Health 19, 237269.Google Scholar
Walker, D. H., Feng, H. M., Saada, J. I., Crocquet-Valdes, P., Radulovic, S., Popov, V. L. and Manor, E. (1995). Comparative antigenic analysis of spotted fever group rickettsiae from Israel and other closely related organisms. The American Journal of Tropical Medicine and Hygiene 52, 7377.Google Scholar
Walker, J. B., Keirans, J. E. and Horak, I. G. eds. (2000). The Genus Rhipicephalus (Acari, Ixodidae): A Guide to the Brown Ticks of the World, 1st Edn. Cambridge University Press, Cambridge.Google Scholar
Walker, D. H., Paddock, C. D. and Dumler, J. S. (2008). Emerging and re-emerging tick-transmitted rickettsial and ehrlichial infections. The Medical clinics of North America 92, 13451361.Google Scholar
Waner, T., Keysary, A., Eremeeva, M. E., Din, A. B., Mumcuoglu, K. Y., King, R. and Atiya-Nasagi, Y. (2014). Rickettsia africae and Candidatus rickettsia barbariae in ticks in Israel. The American Journal of Tropical Medicine and Hygiene 90, 920922.Google Scholar
Weinman, D. and Ristic, M. (1986). The Pathogens, the Infections, and the Consequences: Diseases Caused by Protista, 1st edn. Academic Press, New York.Google Scholar
Ye, J., Coulouris, G., Zaretskaya, I., Cutcutache, I., Rozen, S. and Madden, T. L. (2012). Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction. BMC Bioinformatics 13, 134.Google Scholar
Zhu, Y., Fournier, P.-E., Eremeeva, M. and Raoult, D. (2005). Proposal to create subspecies of Rickettsia conorii based on multi-locus sequence typing and an emended description of Rickettsia conorii . BMC Microbiology 5, 11.Google Scholar
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