Prevalence of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks and assessment of entomological risk index at localities in Belgrade
Abstract
Background/Aim. The first case of human Lyme borreliosis (LB) in Serbia was recorded in 1987. The number of reported LB cases has increased in the past decade. The aim of this study was to estimate the density of Ixodes ricinus (I. ricinus) ticks, the prevalence of Borrelia burgdorferi sensu lato (B. burgdorferi) in them, and entomological risk index (ERI) at 19 Belgrade localities which were grouped into three categories (forests, park-forests, parks). The values of ERI were compared with the number of tick bites in humans. Methods. Ticks were collected monthly by using the flag hours method and the infection rate was determined by using dark field microscopy. The ERI value was calculated for each locality where the ticks were collected. The related data about tick bites was obtained from the patient protocol of the Institute of Epidemiology, Military Medical Academy, Belgrade. Results. The total number of collected ticks, the number of nymphs and the infection rates of the nymphs were significantly higher in forests (p < 0.05) than park-forests and parks. Statistically, the ERI value was significantly higher in forests than parks of Belgrade (χ2 = 7.78, p < 0.01). In March and July, the ERI value was also significantly higher in forests, than park-forests (p < 0.01) and parks (p < 0.01). May was the month with the highest ERI value in each ecological category (forests p < 0.05; park-forests p < 0.01; parks p < 0.001). However, the number of tick bites in humans did not correlate with ERI values. Conclusion. The obtained results indicate that the risk of tick bite and human exposure to B. burgdorferi sensu lato is present at all selected localities in Belgrade. For a more comprehensive Lyme disease risk assessment the method of entomological risk index assessment should be combined with other methods, taking into consideration all tick stages and the behaviour and habits of people who may get infected B. burgdorferi sensu lato.
References
Đordević D, Dmitrović R, Derković V, Drndarević D, Lako B, Obra-dović M, et al. Lyme disease in Yugoslavia. Vojnosanit Pregl 1990; 47(4): 249−53. (Serbian)
Mladenović J, Cekanac R, Stajković N, Krstić M. Risk of Lyme dis-ease development after a tick bite. Vojnosanit Pregl 2010; 67(5): 369−74. (Serbian)
Stafford, III, K. C. 2007. Tick management handbook: an inte-grated guide for homeowners, pest control operators, and public health officials for the prevention of tick-associated dis-ease. The Connecticut Agricultural Experiment Station. New Haven, CT: Bulletin; 2010; 1010: 35−9.
Advisory Committee on Immunization Practices. Recommendations for the Use of Lyme Disease Vaccine. Recommendations of the Advisory Committee on Immunization Practices (ACIP). Morb Mortal Wkly Rep 1999; 48(RR07): 1−17.
Drndarević D, Lako B, Stojanović R, Stajković N, Obradović M, Zi-vanović B, et al. Ixodes ricinus proven as a vector of Lyme bor-reliosis in Yugoslavia. Vojnosanit Pregl 1992; 49(1): 8−11. (Serbian)
Stajković N, Obradović M, Lako B, Drndarević D, Dmitrović R, Đerković V, et al. The first isolation of Borrelia burgdorferi in Apodemus flavicollis in Yugoslavia. Glas Srp Akad Nauka Med 1993; 43: 99−105. (Serbian)
Stajković N, Krstić M, Čekanac R, Marušić P, Lazić S, Mladenović J, et al. Enzootic circulation of Borrelia burgdorferi in Serbia. Proceedings and Abstracts, First International Epizootiologic days; Sijarinska spa, Lebane; 2011 April 6−9. Belgrade: SVD, Sekcija za zoonoze; 2011. p. 38−9.
Cekanac R, Pavlovic N, Gledovic Z, Grgurevic A, Stajkovic N, Lep-sanovic Z, et al. Prevalence of Borrelia burgdorferi in Ixodes ricinus ticks in Belgrade area. Vector Borne Zoonotic Dis 2010; 10(5): 447−52.
Krstić M, Stajković N. Risk for infection by lyme disease cause in green surfaces maintenance workers in Belgrade. Vojnosanit Pregl 2007; 64(5): 313−8.
Maupin GO, Fish D, Zultowsky J, Campos EG, Piesman J. Land-scape ecology of Lyme disease in a residential area of Westchester County, New York. Am J Epidemiol 1991; 133(11): 1105−13.
Daniel M, Cherný V. Distribution and population count of Ix-odes ricinus (L.) in Prague. Med Parazitol (Mosk) 1986; (2): 39−43. (Russian)
Pomerancev BN. Ixodovye klešči. In: Pavlovskii EH, editor. Fauna. SSSR: Paukoobrazovanie. Leningrad: Academii nauk SSSR; 1950. p. 37–92.
Furman PD, Catts EP. Manuel of medical entomology. Lon-don: Cambridge University Press; 1982.
Kovalevskiĭ IV, Korenberg EI, Dauĭotas SV. An evaluation of dif-ferent methods for making vital preparations for the detection of Borrelia in ixodid ticks. Med Parazitol (Mosk) 1990; 1: 33−5. (Russian)
Mather TN, Nicholson MC, Donnelly EF, Matyas BT. Entomologic index for human risk of Lyme disease. Am J Epidemiol 1996; 144(11): 1066−9.
Rizzoli A, Hauffe HC, Carpi G, Vourc'h GI, Neteler M, Rosà R. Lyme borreliosis in Europe. Euro Surveill 2011; 16(27): pii: 19906.
Wang P, Glowacki MN, Hoet AE, Needham GR, Smith KA, Gary RE, et al. Emergence of Ixodes scapularis and Borrelia burgdorferi, the Lyme disease vector and agent, in Ohio. Front Cell Infect Microbiol 2014; 4: 70.
Steere AC, Coburn J, Glickstein L. The emergence of Lyme dis-ease. J Clin Invest 2004; 113(8): 1093−101.
Anderson JF. Epizootiology of Lyme borreliosis. Scand J Infect Dis Suppl 1991; 77: 23−34.
Hayes EB, Piesman J. How Can We Prevent Lyme Disease. N Engl J Med 2003; 348(24): 2424−30.
WHO. Tick-Born Bacterial Infection. In: The Vector-Born Human Infections in Europe. Their Distribution and Burden on Public Health. Copenhagen, Denmark: WHO Regional Office for Europe; 2004. p. 54-67
Center for Prevention and Control of Infectious Diseases. Infectious diseases in the Republic of Serbia within 2010. Belgrade: Insti-tute of Public Health of Serbia "Dr Milan Jovanović Batut"; 2011. (Serbian)
Center for Prevention and Control of Infectious Diseases. Infectious diseases in the Republic of Serbia within 2012. Belgrade: Insti-tute of Public Health of Serbia "Dr Milan Jovanović Batut"; 2013. (Serbian)
Center for Disease Control and Prevention. Lyme disease diagnosis and testing. [updated 2015 March 4]. Available from: http://www.cdc.gov/lyme/diagnosistesting/index.html/. (Serbian)
City Institute of Public Health Belgrade. Center for Disease Control and Prevention. Lyme disease. [update 2013 March 9]. Available from: http://www.zdravlje.org.rs/index.php?option=com_content&view=article&id=98&Itemid=210&lang=sr. (Serbian)
Poland GA. Prevention of Lyme Disease: A Review of the Evi-dence. Mayo Clin Proc 2001; 76(7): 713−24.
Fish D. Environmental risk and prevention of Lyme disease. Am J Med 1995; 98(4): 2−9.
Connally NP, Ginsberg HS, Mather TN. Assessing peridomestic entomological factors as predictors for Lyme disease. J Vector Ecol 2006; 31(2): 364−70.
Mannelli A, Cerri D, Buffrini L, Rossi S, Rosati S, Arata T, et al. Low risk of Lyme borreliosis in a protected area on the Tyr-rhenian coast, in central Italy. Eur J Epidemiol 1999; 15(4): 371−7.
Junttila J, Peltomaa M, Soini H, Marjamäki M, Viljanen MK. Prev-alence of Borrelia burgdorferi in Ixodes ricinus ticks in urban recreational areas of Helsinki. J Clin Microbiol 1999; 37(5): 1361−5.
Stajković N, Drndarević D, Lako B, Dmitrović R, Obradović M, Djerković V, et al. Vectors of Borrelia burgdorferi. Glas Srp Akad Nauka Med 1993; 43: 45−56. (Serbian)
Stepánová-Tresová G, Pet'ko B, Stefancíková A, Nadzamová D. Oc-currence of Borrelia burgdorferi sensu stricto, Borrelia garinii and Borrelia afzelii in the Ixodes ricinus ticks from Eastern Slovakia. Eur J Epidemiol 2000; 16(2): 105−9.
Potkonjak A, Jurisic A, Petrovic A, Nicin S, Rajkovic D, Lako B, et al. Entomological and ecological index for risk of infection causing lyme disease in territory of Vojvodina, Serbia. Vet Glas 2013; 67(1−2): 3−14.
Cinco M, Padovan D, Murgia R, Poldini L, Frusteri L, van de Pol I, et al. Rate of infection of Ixodes ricinus ticks with Borrelia burgdorferi sensu stricto, Borrelia garinii, Borrelia afzelii and group VS116 in an endemic focus of Lyme disease in Italy. Eur J Clin Microbiol Infect Dis 1998; 17(2): 90−4.
Rijpkema S, Golubić D, Molkenboer M, Verbeek-De Kruif N,, Schellekens J. Identification of four genomic groups of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in a Lyme borreliosis endemic region of northern Croatia. Exp Appl Acarol 1996; 20(1): 23−30.
Hubálek Z, Stünzner D, Halouzka J, Sixl W, Wendelin I, Juricová Z, Sanogo YO. Prevalence of borreliae in ixodid ticks from a floodplain forest ecosystem. Wien Klin Wochenschr 2003; 115(3−4): 121−4.
Jensen PM, Hansen H, Frandsen F. Spatial risk assessment for Lyme borreliosis in Denmark. Scand J Infect Dis 2000; 32(5): 545−50.
Baumgarten BU, Röllinghoff M, Bogdan C. Prevalence of Borrelia burgdorferi and granulocytic and monocytic ehrlichiae in Ix-odes ricinus ticks from southern Germany. J Clin Microbiol 1999; 37(11): 3448−51.
Stańczak J, Kubica-Biernat B, Racewicz M, Kruminis-Lozowska W, Kur J. Detection of three genospecies of Borrelia burgdorferi sensu lato in Ixodes ricinus ticks collected in different regions of Poland. Int J Med Microbiol 2000; 290(6): 559−66.
Cisak E, Wójcik-Fatla A, Zając V, Sroka J, Dutkiewicz J. Risk of Lyme disease at various sites and workplaces of forestry workers in eastern Poland. Ann Agric Environ Med 2012; 19(3): 465−8.
Geller J, Nazarova L, Katargina O, Golovljova I. Borrelia burgdor-feri sensu lato prevalence in tick populations in Estonia. Para-sit Vectors 2013; 6(1): 202.
Nadelman RB, Wormser GP. Lyme borreliosis. Lancet 1998; 352(9127): 557−65.
Rijpkema S, Nieuwenhuijs J, Franssen FF, Jongejan F. Infection rates of Borrelia burgdorferi in different instars of Ixodes ricinus ticks from the Dutch North Sea Island of Ameland. Exp App Acarol 1994; 18(9): 531−42.
Nazzi F, Martinelli E, del Fabbro S, Bernardinelli I, Milani N, Iob A, et al. Ticks and Lyme borreliosis in an alpine area in northeast Italy. Med Vet Entomol 2010; 24(3): 220−6.
Zeman P. Borrelia-infection rates in tick and insect vectors ac-companying human risk of acquiring Lyme borreliosis in a highly endemic region in Central Europe. Folia Parasitol (Pra-ha) 1998; 45(4): 319−25.
Stańczak J, Okróy-Rysop G, Racewicz M, Kubica-Biernat B, Kruminis-Łozowska W. Prevalence of Borrelia burgdorferi sensu lato in the selected Ixodes ricinus (Acari: Ixodidae) population in Weilburg forests, Hesse, Germany. Int J Med Microbiol 2002; 291: 206−9.
Barral M, García-Pérez AL, Juste RA, Hurtado A, Escudero R, Sellek RE, et al. Distribution of Borrelia burgdorferi sensu lato in Ixodes ricinus (Acari: Ixodidae) ticks from the Basque Country, Spain. J Med Entomol 2002; 39(1): 177−84.
Pangrácová L, Derdáková M, Pekárik L, Hviščová I, Víchová B, Stanko M, et al. Ixodes ricinus abundance and its infection with the tick-borne pathogens in urban and suburban areas of Eastern Slovakia. Parasit Vectors 2013; 6(1): 238.
Pardanani N, Mather TN. Lack of spatial autocorrelation in fine-scale distributions of Ixodes scapularis (Acari: Ixodidae). J Med Entomol 2004; 41(5): 861−4.
Schulze TL, Taylor RC, Taylor GC, Bosler EM. Lyme disease: a proposed ecological index to assess areas of risk in the north-eastern United States. Am J Pabl Health 1991; 81(6): 714−8.
Walk ST, Xu G, Stull JW, Rich SM. Correlation between tick density and pathogen endemicity, New Hampshire. Emerging Infect Dis 2009; 15(4): 585−7.