Vertical transmission of Bartonella schoenbuchensis in Lipoptena cervi

Particle and Fibre Toxicology

Gábor Földvári⁵  Hein Sprong⁴  László Dremmel³  Mihály Földvári¹  Willem Takken⁴  Setareh Jahfari²  Arieke Docters van Leeuwen²  Arnout de Bruin² 

[1] MTA-DE ‘Lendulet’ Behavioural Ecology Research Group, Department of Evolutionary Zoology, University of Debrecen, Debrecen, Hungary;Centre for Zoonoses & Environmental Microbiology, Centre for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, the Netherlands;Institute of Wildlife Management and Vertebrate Zoology, Faculty of Forestry, University of West Hungary, Sopron, Hungary;Laboratory of Entomology, Wageningen University, Wageningen, the Netherlands;Department of Parasitology and Zoology, Faculty of Veterinary Science, SzentIstván University, Budapest, Hungary

关键词: Ixodes ricinus;    Rickettsia;    Bartonella;    Anaplasma;    Vector;    Pathogen;    Deer ked;    Lipoptena cervi;   

Others  :  1146439
DOI  :  10.1186/s13071-015-0764-y

 received in 2014-12-11, accepted in 2015-02-24,  发布年份 2015

【 摘 要 】

Background

Lipoptena cervi (Diptera: Hippoboscidae) is a hematophagous ectoparasite of cervids, which is considered to transmit pathogens between animals and occasionally to humans. The principal life stage that is able to parasitize new hosts is a winged ked that just emerged from a pupa. To facilitate efficient transmission of pathogens between hosts, vertical transmission from female deer keds to their offspring is necessary. We investigated vertical transmission of several vector-borne pathogens associated with cervids.

Methods

Deer keds from several locations in Hungary were collected between 2009 and 2012. All life stages were represented: winged free-ranging adults, wingless adults collected from Capreolus capreolus and Cervus elaphus, developing larvae dissected from gravid females, and fully developed pupae. The presence of zoonotic pathogens was determined using qPCR or conventional PCR assays performed on DNA lysates. From the PCR-positive lysates, a gene fragment was amplified and sequenced for confirmation of pathogen presence, and/or pathogen species identification.

Results

DNA of Bartonella schoenbuchensis was found in wingless males (2%) and females (2%) obtained from Cervus elaphus, dissected developing larvae (71%), and free-ranging winged males (2%) and females (11%). DNA of Anaplasma phagocytophilum and Rickettsia species was present in L. cervi adults, but not in immature stages. DNA of Candidatus Neoehrlichia mikurensis was absent in any of the life stages of L. cervi.

Conclusions

B. schoenbuchensis is transmitted from wingless adult females to developing larvae, making it very likely that L. cervi is a vector for B. schoenbuchensis. Lipoptena cervi is probably not a vector for A. phagocytophilum, Rickettsia species, and Candidatus N. mikurensis.

【 授权许可】

   
2015 De Bruin et al.; licensee BioMed Central.

【 参考文献 】

• [1]Kynkaanniemi SM, Kettu M, Kortet R, Harkonen L, Kaitala A, Paakkonen T et al.. Acute impacts of the deer ked (Lipoptena cervi) infestation on reindeer (Rangifer tarandus tarandus) behaviour. Parasitol Res. 2014; 113(4):1489-97.
• [2]Madslien K, Ytrehus B, Viljugrein H, Solberg EJ, Braten KR, Mysterud A. Factors affecting deer ked (Lipoptena cervi) prevalence and infestation intensity in moose (Alces alces) in Norway. Parasit Vectors. 2012; 5:251. BioMed Central Full Text
• [3]Kortet R, Harkonen L, Hokkanen P, Harkonen S, Kaitala A, Kaunisto S et al.. Experiments on the ectoparasitic deer ked that often attacks humans; preferences for body parts, colour and temperature. Bull Ent Res. 2010; 100(3):279-85.
• [4]Bequaert JC. A Monograph of the Melophaginae Or Ked-Flies of Sheep, Goats, Deer, and Antelopes (Diptera, Hippoboscidae): Brooklyn Entomological Society. 1942.
• [5]Maa TC. A synopsis of the Lipopteninae (Diptera: Hippoboscidae). J Med Entomol. 1965; 2(3):233-48.
• [6]Baker J. A review of the role played by the Hippoboscidae (Diptera) as vectors of endoparasites. J Parasitol . 1967:412–8
• [7]Kennedy PG. The continuing problem of human African trypanosomiasis (sleeping sickness). An Neur. 2008; 64(2):116-26.
• [8]Korhonen EM, Perez Vera C, Pulliainen AT, Sironen T, Aaltonen K, Kortet R et al.. Molecular detection of Bartonella spp. in deer ked pupae, adult keds and moose blood in Finland. Epidemiol Infect. 2014; 143(3):1-8.
• [9]Paakkonen T, Mustonen AM, Kakela R, Kiljander T, Kynkaanniemi SM, Laaksonen S et al.. Experimental infection of the deer ked (Lipoptena cervi) has no negative effects on the physiology of the captive reindeer (Rangifer tarandus tarandus). Vet Parasitol. 2011; 179(1–3):180-8.
• [10]Dehio C, Sauder U, Hiestand R. Isolation of Bartonella schoenbuchensis from Lipoptena cervi, a blood-sucking arthropod causing deer ked dermatitis. J Clin Microbiol. 2004; 42(11):5320-3.
• [11]Rantanen T, Reunala T, Vuojolahti P, Hackman W. Persistent pruritic papules from deer ked bites. Acta Derm Venereol. 1982; 62(4):307-11.
• [12]Duodu S, Madslien K, Hjelm E, Molin Y, Paziewska-Harris A, Harris PD et al.. Bartonella infections in deer keds (Lipoptena cervi) and moose (Alces alces) in Norway. Appl Environ Microbiol. 2013; 79(1):322-7.
• [13]Halos L, Jamal T, Maillard R, Girard B, Guillot J, Chomel B et al.. Role of Hippoboscidae flies as potential vectors of Bartonella spp. infecting wild and domestic ruminants. Appl Environ Microbiol. 2004; 70(10):6302-5.
• [14]Hornok S, de la Fuente J, Biro N, de Fernandez Mera IG, Meli ML, Elek V et al.. First molecular evidence of Anaplasma ovis and Rickettsia spp. in keds (Diptera: Hippoboscidae) of sheep and wild ruminants. Vec Zoon Dis. 2011; 11(10):1319-21.
• [15]Haarløv N. Life cycle and distribution pattern of Lipoptena cervi (L.)(Dipt., Hippobosc.) on Danish deer. Oikos. 1964; 15(1):93-129.
• [16]Hackman W, Rantanen T, Vuojolahti P. Immigration of Lipoptena cervi (Diptera, Hippoboscidae) in Finland, with notes on its biology and medical significance. Not Ent. 1983; 63:53-9.
• [17]Samuel W, Trainer D. Lipoptena mazamae Rondani, 1878 (Diptera: Hippoboscidae) on white-tailed deer in southern Texas. J Med Entomol. 1972; 9(1):104-6.
• [18]Tijsse-Klasen E, Fonville M, Gassner F, Nijhof AM, Hovius EK, Jongejan F et al.. Absence of zoonotic Bartonella species in questing ticks: first detection of Bartonella clarridgeiae and Rickettsia felis in cat fleas in the Netherlands. Parasit Vectors. 2011; 4:61. BioMed Central Full Text
• [19]Stuen S, Granquist EG, Silaghi C. Anaplasma phagocytophilum–a widespread multi-host pathogen with highly adaptive strategies. Front Cell Inf Microbiol. 2013; 3:31.
• [20]Jin H, Wei F, Liu Q, Qian J. Epidemiology and control of human granulocytic anaplasmosis: a systematic review. Vec Zoon Dis. 2012; 12(4):269-74.
• [21]Víchová B, Majláthová V, Nováková M, Majláth I, Čurlík J, Bona M et al.. PCR detection of re-emerging tick-borne pathogen, Anaplasma phagocytophilum, in deer ked (Lipoptena cervi) a blood-sucking ectoparasite of cervids. Biologia. 2011; 66(6):1082-6.
• [22]Jahfari S, Coipan EC, Fonville M, van Leeuwen AD, Hengeveld P, Heylen D et al.. Circulation of four Anaplasma phagocytophilum ecotypes in Europe. Parasit Vectors. 2014; 7:365. BioMed Central Full Text
• [23]Merhej V, Angelakis E, Socolovschi C, Raoult D. Genotyping, evolution and epidemiological findings of Rickettsia species. Infection, genetics and evolution. J Mol Epidemiol Evol Gen Infect Dis. 2014; 25:122-37.
• [24]Nilsson K, Lindquist O, Pahlson C. Association of Rickettsia helvetica with chronic perimyocarditis in sudden cardiac death. Lancet. 1999; 354(9185):1169-73.
• [25]Nilsson K. Septicaemia with Rickettsia helvetica in a patient with acute febrile illness, rash and myasthenia. J Infect. 2009; 58(1):79-82.
• [26]Nilsson K, Elfving K, Pahlson C. Rickettsia helvetica in patient with meningitis, Sweden. Emerg Infect Dis. 2010; 16(3):490-2.
• [27]Wielinga PR, Gaasenbeek C, Fonville M, de Boer A, de Vries A, Dimmers W et al.. Longitudinal analysis of tick densities and Borrelia, Anaplasma, and Ehrlichia infections of Ixodes ricinus ticks in different habitat areas in The Netherlands. Appl Environ Microbiol. 2006; 72(12):7594-601.
• [28]Jahfari S, Fonville M, Hengeveld P, Reusken C, Scholte EJ, Takken W et al.. Prevalence of Neoehrlichia mikurensis in ticks and rodents from North-west Europe. Parasit Vectors. 2012; 5:74. BioMed Central Full Text
• [29]De Sousa R, Edouard-Fournier P, Santos-Silva M, Amaro F, Bacellar F, Raoult D. Molecular detection of Rickettsia felis, Rickettsia typhi and two genotypes closely related to Bartonella elizabethae. Am J Trop Med Hyg. 2006; 75(4):727-31.
• [30]Stenos J, Graves SR, Unsworth NB. A highly sensitive and specific real-time PCR assay for the detection of spotted fever and typhus group Rickettsiae. Am J Trop Med Hyg. 2005; 73(6):1083-5.
• [31]Roux V, Rydkina E, Eremeeva M, Raoult D. Citrate synthase gene comparison, a new tool for phylogenetic analysis, and its application for the rickettsiae. Int J Syst Bacteriol. 1997; 47(2):252-61.
• [32]Maurer FP, Keller PM, Beuret C, Joha C, Achermann Y, Gubler J et al.. Close geographic association of human neoehrlichiosis and tick populations carrying “Candidatus Neoehrlichia mikurensis” in eastern Switzerland. J Clin Microbiol. 2013; 51(1):169-76.
• [33]Andersson M, Raberg L. Wild rodents and novel human pathogen candidatus Neoehrlichia mikurensis, Southern Sweden. Emerg Infect Dis. 2011; 17(9):1716-8.
• [34]Vayssier-Taussat M, Le Rhun D, Buffet JP, Maaoui N, Galan M, Guivier E et al.. Candidatus Neoehrlichia mikurensis in bank voles, France. Emerg Infect Dis. 2012; 18(12):2063-5.
• [35]Szekeres S, Claudia Coipan E, Rigo K, Majoros G, Jahfari S, Sprong H et al.. Candidatus Neoehrlichia mikurensis and Anaplasma phagocytophilum in natural rodent and tick communities in Southern Hungary. Ticks Tickborne Dis. 2014; 6(2):111-116.
• [36]Jaenson TG, Tälleklint L. Incompetence of roe deer as reservoirs of the Lyme borreliosis spirochete. J Med Entomol. 1992; 29(5):813-7.
• [37]Telford SR, Wormser GP. Bartonella spp. transmission by ticks not established. Emerg Infect Dis. 2010; 16(3):379-84.
• [38]Rosef O, Paulauskas A, Radzijevskaja J. Prevalence of Borrelia burgdorferi sensu lato and Anaplasma phagocytophilum in questing Ixodes ricinus ticks in relation to the density of wild cervids. Acta Vet Scand. 2009; 51:47. BioMed Central Full Text
• [39]Pacilly F, Benning M, Jacobs F, Leidekker J, Sprong H, Van Wieren S et al.. Blood feeding on large grazers affects the transmission of Borrelia burgdorferi sensu lato by Ixodes ricinus. Ticks Tickborne Dis. 2014; 5(6):810-7.
• [40]Paakkonen T, Mustonen AM, Roininen H, Niemela P, Ruusila V, Nieminen P. Parasitism of the deer ked, Lipoptena cervi, on the moose, Alces alces, in eastern Finland. Med Vet Ent. 2010; 24(4):411-7.
• [41]Lehane MJ. The biology of blood-sucking in insects: Cambridge University Press. 2005.
• [42]Unckless RL, Jaenike J. Maintenance of a male-killing Wolbachia in Drosophila innubila by male-killing dependent and male-killing independent mechanisms. Evolution; Int J Org Evol. 2012; 66(3):678-89.
• [43]Morse SF, Dick CW, Patterson BD, Dittmar K. Some like it hot: evolution and ecology of novel endosymbionts in bat flies of cave-roosting bats (hippoboscoidea, nycterophiliinae). Appl Environ Microbiol. 2012; 78(24):8639-49.
• [44]Duron O, Schneppat UE, Berthomieu A, Goodman SM, Droz B, Paupy C et al.. Origin, acquisition and diversification of heritable bacterial endosymbionts in louse flies and bat flies. Mol Ecol. 2014; 23(8):2105-17.
• [45]Dehio C, Lanz C, Pohl R, Behrens P, Bermond D, Piemont Y et al.. Bartonella schoenbuchii sp. nov., isolated from the blood of wild roe deer. Int JSyst Eevol Microbiol. 2001; 51(Pt 4):1557-65.
• [46]Skotarczak B, Adamska M. Detection of Bartonella DNA in roe deer (Capreolus capreolus) and in ticks removed from deer. Eur J Wildlife Res. 2005; 51(4):287-90.
• [47]Rar V, Golovljova I. Anaplasma, Ehrlichia, and “Candidatus Neoehrlichia” bacteria: pathogenicity, biodiversity, and molecular genetic characteristics, a review. Infect Genet Evol J Mol Epidemiol Evol Gen Inf Dis. 2011; 11(8):1842-61.
• [48]Malmsten J, Widen DG, Rydevik G, Yon L, Hutchings MR, Thulin CG et al.. Temporal and spatial variation in Anaplasma phagocytophilum infection in Swedish moose (Alces alces). Epidemiol Infect. 2014; 142(6):1205-13.
• [49]Overzier E, Pfister K, Herb I, Mahling M, Bock G, Silaghi C. Detection of tick-borne pathogens in roe deer (Capreolus capreolus), in questing ticks (Ixodes ricinus), and in ticks infesting roe deer in southern Germany. Ticks Tickborne Dis. 2013; 4(4):320-8.