Interactions between hard ticks (Ixodidae) and bacterial tick-borne pathogens

Authors

  • Dorota Kiewra Department of Microbial Ecology and Acaroentomology, University of Wrocław, Wrocław, Poland
  • Alicja Krysmann Department of Microbial Ecology and Acaroentomology, University of Wrocław, Wrocław, Poland

Keywords:

ticks, tick-borne pathogens, interactions, Borrelia burgdorferi s.l., Anaplasma phagocytophilum, Rickettsia spp.

Abstract

In Europe, ticks are particularly important vectors of pathogens known as tick-borne pathogens (TBP). TBP can influence hosts, including domestic animals and humans as well as ticks. This review focuses on interactions between hard ticks and medically and veterinary significant bacterial pathogens i.e. Borrelia burgdorferi s.l., Anaplasma spp, and Rickettsia spp. The interactions between ticks and bacteria include among others the impact on gene expression and tick behaviour. Infection with TBP may influence tick salivary proteins and midgut receptors. Infection with B. burgdorferi s.l. changes the bahaviour of the tick allowing them for longer questing and increased mobility, while A. phagocytophilum increases survive in low temperatures by upregulating the expression of antifreeze glycoprotein (IAFGP). Whereas Rickettsia spp. increases ticks attraction towards the 900 MHz electromagnetic field.

References

Estrada-Peña A., 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: 685–715. https://doi.org/10.1023/a:1006241108739

Boulanger N., Boyer P., Talagrand-Reboul E., Hansmann Y. 2019. Ticks and tick-borne diseases. Médecine et Maladies Infectieuses 49(2): 87–97. https://doi.org/10.1016/j.medmal.2019.01.007

Hussain S., Hussain A., Aziz U., Song B., Zeb J., George D., Li J., Sparagano O. 2021. The role of ticks in the emergence of Borrelia burgdorferi as a zoonotic pathogen and its vector control: a global systemic review. Microorganisms 9(12): 2412. https://doi.org/10.3390/microorganisms9122412

Kahl O., Gray J.S. 2023. The biology of Ixodes ricinus with emphasis on its ecology. Ticks and Tick- Borne Diseases 14(2): 102114. https://doi.org/10.1016/j.ttbdis.2022.102114

Rochlin I., Toledo A. 2020. Emerging tick-borne pathogens of public health importance: a mini-review. Journal of Medical Microbiology 69(6): 781–791. https://doi.org/10.1099/jmm.0.001206

Hajdušek O., Šíma R., Ayllón N., Jalovecká M., Perner J., Fuente J., Kopáček P. 2013. Interaction of the tick immune system with transmitted pathogens. Frontiers in Cellular Infection Microbiology 3: 26. https://doi.org/10.3389/fcimb.2013.00026

Wikel S.K. 2018. Ticks and tick-borne infections: complex ecology, agents, and host interactions. Veterinary Sciences 5(2): 60. https://doi.org/10.3390/vetsci5020060

Wikel S.K. 2018. Tick-host-pathogen systems immunobiology: an interactive trio. Frontiers in Bioscience 23(2): 265–283. https://doi.org/10.2741/4590

Cowdry E.V. 1925. A group of microorganisms transmitted hereditarily in ticks and apparently unassociated with disease. Journal of Experimental Medicine 41: 817–830. https://doi.org/10.1084/jem.41.6.817

Tokarz R., Lipkin W.I. 2021. Discovery and surveillance of tick-borne pathogens. Journal of Medical Entomology 58(4): 1525–1535. https://doi.org/10.1093/jme/tjaa269

MacLeod J., Gordon W.S. 1933. Studies in tick- borne fever of sheep. I. Transmission by the tick, Ixodes ricinus, with a description of the disease produced. Parasitology 25(2): 273–283. https://doi.org/10.1017/s0031182000019442

Burgdorfer W., Barbour A., Hayes S., Benach J., Grunwaldt E., Davis J. 1982. Lyme disease – a tick- borne spirochetosis? Science 216(4552): 1317–1319. https://doi.org/10.1126/science.7043737

Hubbard M.J., Baker A.S., Cann K.J. 1998. Distribution of Borrelia burgdorferi s.l. spirochaete DNA in British ticks (Argasidae and Ixodidae) since the 19th Century, assessed by PCR. Medical and Veterinary Entomology 12(1): 89–97. https://doi.org/10.1046/j.1365-2915.1998.00088.x

Poinar G. 2014. Spirochete-like cells in a Dominican amber Ambylomma tick (Arachnida: Ixodidae). Historical Biology 27(5): 565–570. https://doi.org/10.1080/08912963.2014.897699

Oppler Z.J., O’Keeffe K.R., McCoy K.D., Brisson D. 2021. Evolutionary genetics of Borrelia. Current Issues in Molecular Biology 42: 97–112. https://doi.org/10.21775/cimb.042.097

Benelli G. 2020. Pathogens manipulating tick behavior – through a glass, darkly. Pathogens 9(8): 664. https://doi.org/10.3390/pathogens9080664

Adeolu M., Gupta R.S. 2014. A phylogenomic and molecular marker based proposal for the division of the genus Borrelia into two genera: the emended genus Borrelia containing only the members of the relapsing fever Borrelia, and the genus Borreliella gen. nov. containing the members of the Lyme disease Borrelia (Borrelia burgdorferi sensu lato complex). Antonie van Leeuwenhoek 105(6): 1049–1072. https://doi.org/10.1007/s10482-014-0164-x

Fukunaga M., Takahashi Y., Tsuruta Y., Matsushita O., Ralph D., Mcclelland M., Nakao M. 1995. Genetic and phenotypic analysis of Borrelia miyamotoi sp. nov., isolated from the Ixodid tick Ixodes persulcatus, the vector for Lyme disease in Japan. International Journal of Systematic Bacteriology 45(4): 804–810. https://doi.org/10.1099/00207713-45-4-804

Kiewra D., Stańczak J., Richter M. 2014. Ixodes ricinus ticks (Acari, Ixodidae) as a vector of Borrelia burgdorferi sensu lato and Borrelia miyamotoi in Lower Silesia, Poland – preliminary study. Ticks and Tick-Borne Diseases 5(6): 892–897. https://doi.org/10.1016/j.ttbdis.2014.07.004

Madison-Antenucci S., Kramer L. D., Gebhardt L. L., Kauffman, E. 2020. Emerging tick-borne diseases. Clinical Microbiology Reviews 33(2). https://doi.org/10.1128/CMR.00083-18

Steinbrink A., Brugger K., Margos G., Kraiczy P., Klimpel S. 2022. The evolving story of Borrelia burgdorferi sensu lato transmission in Europe. Parasitology Research 121: 781–803. https://doi.org/10.1007/s00436-022-07445-3

Murray T.S., Shapiro E.D. 2010. Lyme disease. Clinics in Laboratory Medicine 30(1): 311–328. https://doi.org/10.1016/j.cll.2010.01.003

Marques A.R., Strle F., Wormser G.P. 2021. Comparison of Lyme disease in the United States and Europe. Emerging Infectious Diseases 27(8): 2017–2024. https://doi.org/10.3201/eid2708.204763

Blazejak K., Raulf M.K., Janecek E., Jordan D., Fingerele V., Strube C. 2018. Shifts in Borrelia burgdorferi (s.l.) geno-species infections in Ixodes ricinus over a 10-year surveillance period in the city of Hanover (Germany) and Borrelia miyamotoi- specific Reverse Line Blot detection. Parasites and Vectors 11(304). https://doi.org/10.1186/s13071-018-2882-9

Sykes R.A., Makiello P. 2017. An estimate of Lyme borreliosis incidence in Western Europe. Journal of Public Health 39(1): 74–81. https://doi.org/10.1093/pubmed/fdw017

Collares-Pereira M., Couceiro S., Franca I., Kurtenbach K., Schäfer S. M., Vitorino L., Gonçalves L., Baptista S., Vieira M. L., Cunha C. 2004. First isolation of Borrelia lusitaniae from a human patient. Journal of Clinical Microbiology 42(3): 1316–1318. https://doi.org/10.1128/JCM.42.3.1316-1318.2004

Dulipati V., Meri S., Panelius J. 2020. Complement evasion strategies of Borrelia burgdorferi sensu lato. FEBS Letters 594: 2645–2656. https://doi.org/10.1002/1873-3468.13894

Kim C.M., Park S.Y., Kim D.M., Park J.W., Chung J.K. 2021. First report of Borrelia burgdorferi sensu stricto detection in a commune genospecies in Apodemus agrarius in Gwangju, South Korea. Scientific Reports 11: 18199. https://doi.org/10.1038/s41598-021-97411-3

Filisiak R., Pancewicz S. 2008. Diagnostics and treatment of Lyme borreliosis. Recommendations of Polish Society of Epidemiology and Infectious Diseases. Przegląd Epidemiologiczny 62(1): 193–199.

Mendoza-Roldan J.A., Colella V., Lia R.P., Nguyen V.L., Barros-Battesti D.M., Iatta R., Dantas-Torres F., Otranto D. 2019. Borrelia burgdorferi (sensu lato) in ectoparasites and reptiles in southern Italy. Parasites and Vectors 12(35). https://doi.org/10.1186/s13071-019-3286-1

Hoxmeier J.C., Fleshman A.C., Broeckling C.D., Prenni J.E., Dolan M.C., Gage K.L, Eisen L. 2017. Metabolomics of the tick-Borrelia interaction during the nymphal tick blood meal. Scientific Reports 7(44394). https://doi.org/10.1038/srep44394

Cook M.J., Puri B.K. 2020. Estimates for Lyme borreliosis infections based on models using sentinel canine and human seroprevalence data. Infectious Disease Modelling 5: 871–888. https://doi.org/10.1016/j.idm.2020.10.004

Narodowy Instytut Zdrowia Publicznego. Państwowy Zakład Higieny 2022. Meldunki Epidemiologiczne. http://wwwold.pzh.gov.pl/oldpage/epimeld/index_p. html

McCormick D.W., Kugeler K.J., Marx G.E., Jayanthi P., Dietz S., Mead P., Hinckley A.F. 2021. Effects of COVID-19 pandemic on reported Lyme disease, United States, 2020. Emerging Infectious Diseases 27(10): 2715–2717. https://doi.org/10.3201/eid2710.210903

Moniuszko-Malinowska A., Pancewicz S., Czupryna P. 2020. Has COVID-19 influenced on tick- borne epidemiology? Przegląd Epidemiologiczny 74(4): 740–741. https://doi.org/10.32394/pe.74.65

Rogulska K., Piątek P., Grzeszczak K. 2021. The impact of pandemic COVID-19 on cases of borreliosis infection in 2020. Journal of Education, Health and Sport 11(9): 232–237. https://doi.org/10.12775/JEHS.2021.11.09.029

Michalik J., Zajkowska J. 2013. Ecology of the most common clinical manifestations of Lyme borreliosis in Poland and Europe. In: Wydawnictwo Stawonogi. Aspekty medyczne i weterynaryjne. (Eds. A. Buczek, C. Błaszak). Koliber Oficyna Wydawnicza Fundacji na Rzecz Zwalczania Kleszczy i Profilaktyki w Chorobach Odkleszczowych, Lublin 2013: 207–225.

Stafford K.C.3rd, Cartter M.L., Magnarelli L.A., Ertel S.H., Mshar P.A. 1998. Temporal correlations between tick abundance and prevalence of ticks infected with Borrelia burgdorferi and increasing incidence of Lyme disease. Journal of Clinical Microbiology. 36(5): 1240–1244. https://doi.org/10.1128/JCM.36.5.1240-1244.1998

Diuk-Wasser M.A., Brinkerhoff R., Kitron U., Fish D., Melton F., Cislo P., Brinkerhoff R., Hamer S.A., Rowland M., Cortinas R., Vourc’h G., Melton F., Hickling G.J., Tsao J.I., Bunikis J., Barbour A.G., Kitron U., Piesman J., Fish D. 2012. Human risk of infection with Borrelia burgdorferi, the Lyme disease agent, in eastern united states. The American Journal of Tropical Medicine and Hygiene 86(2): 320–327. https://doi.org/10.4269/ajtmh.2012.11-039

Hickling G.J., Kelly J.R., Auckland L.D., Hamer S.A. 2018. Increasing prevalence of Borrelia burgdorferi sensu stricto-infected blacklegged ticks in Tennessee Valley, Tennessee, USA. Emerging Infectious Diseases 24(9): 1713–1716. https://doi.org/10.3201/eid2409.180343

Rauter C., Hartung T. 2005. Prevalence of Borrelia burgdorferi sensu lato genospecies in Ixodes ricinus ticks in Europe: a metaanalysis. Applied and Environmental Microbiology 71(11): 7203–7216. https://doi.org/10.1128/AEM.71.11.7203-7216.2005

Estrada-Peña A., Cutler S., Potkonjak A., Vassier- Tussaut M., Van Bortel W., Zeller H., Fernández-Ruiz N., Mihalca A. D. 2018. An updated meta-analysis of the distribution and prevalence of Borrelia burgdorferi s.l. in ticks in Europe. International Journal of Health Geographics 17(41). https://doi.org/10.1186/s12942-018-0163-7

Siński E., Rijpkema S.G.T. 1997. Występowanie zakażeń Borrelia burgdorferi s.l. u kleszczy Ixodes ricinus w miejskim i podmiejskim biotypie leśnym [Prevalence of Borrelia burgdorferi s. 1. infection in Ixodes ricinus at urban and suburban forest habitats]. Przegląd Epidemiologiczny 51(4): 431–435 (in Polish with summary in English).

Cisak E., Chmielewska-Badora J., Zwoliński J., Wójcik-Fatla A., Polak J., Dutkiewicz J. 2005. Risk of tick-borne bacterial diseases among workers of Roztocze National Park (south-eastern Poland). Annals of Agricultural and Environmental Medicine 12(1): 127–132.

Kasprzak J., Brochocka A., Klimberg A. 2016. Występowanie krętków Borrelia spp. w kleszczach Ixodes ricinus z terenów endemicznych województwa kujawsko- pomorskiego [Occurrence of Borrelia spp. spirochetes in Ixodes ricinus ticks from endemic areas in Kuyavian, Pomeranian province]. Problemy Higieny i Epidemiologii 97(4): 363–370 (in Polish with summary in English).

Strnad M., Hönig V., Ružek D., Grubhoffer L., Rego R.O.M. 2017. Europe-wide meta-analysis of Borrelia burgdorferi sensu lato prevalence in questing Ixodes ricinus ticks. Applaied and Environmental Microbiology 83(15). https://doi.org/10.1128/AEM.00609-17

Kingry L.C., Anacker M., Pritt B., Bjork J., Respicio-Kingry L., Liu G., Sheldon S., Boxrud D., Strain A., Oatman S., Berry J., Sloan L., Mead P., Neitzel D., Kugeler K.J., Petersen J.M. 2018. Surveillance for and discovery of Borrelia species in US patients suspected of tick-borne illness. Clinical Infectious 66(12): 1864–1871. https://doi.org/10.1093/cid/cix1107

Ramamoorthi N., Narasimhan S., Pal U., Bao F., Yang X. F., Fish D., Anguita J., Norgard M.V., Kantor F.S., Anderson J. F., Koski R.A., Fikrig E. 2005. The Lyme disease agent exploits a tick protein to infect the mammalian host. Nature 436(7050): 573–577. https://doi.org/10.1038/nature03812

Narasimhan S., Sukumaran B., Bozdogan U., Thomas V., Liang X., DePonte K., Marcantonio N., Koski R.A., Anderson J.F., Kantor F., Fikrig E. 2007. A tick antioxidant facilitates the Lyme disease agent’s successful migration from the mammalian host to the arthropod vector. Cell Host and Microbe 2(1): 7–18. https://doi.org/10.1016/j.chom.2007.06.001

Tyson K., Elkins C., Patterson H., Fikrig E., de Silva A. 2007. Biochemical and functional characterization of Salp20, an Ixodes scapularis tick salivary protein that inhibits the complement pathway. Insect Molecular Biology 16(4): 469–479. https://doi.org/10.1111/j.1365-2583.2007.00742.x

Pichu S., Ribeiro J.M.C., Mather T.N. 2009. Purification and characterization of a novel salivary antimicrobial peptide from the tick, Ixodes scapularis. Biochemical and Biophysical Research Communications 390(3): 511–515. https://doi.org/10.1016/j.bbrc.2009.09.127

Dai J., Narasimhan S., Zhang L., Liu L., Wang P., Fikrig E. 2010. Tick histamine release factor is critical for Ixodes scapularis engorgement and transmission of the Lyme disease agent. PLOS Pathogens 6(11). https://doi.org/0.1371/journal.ppat.1001205

Schuijt T.J., Coumou J., Narasimhan S., Dai J., DePonte K., Wouters D., Brouwer M., Oei A., Roelofs J.J.T.H., van Dam A.P., van der Poll T., van’t Veer C., Hovius J.W., Fikrig E. 2011. A tick mannose- binding lectin inhibits the vertebrate complement cascade to enhance transmission of the Lyme disease agent. Cell Host Microbe 10(2): 136–146. https://doi.org/10.1016/j.chom.2011.06.010

Wen S., Wang F., Ji Z., Pan Y., Jian M., Bi Y., Zhou G., Luo L., Chen T., Li L., Ding Z., Abi M-E, Liu A., Bao F. 2020. Salp15, a multifunctional protein from tick saliva with potential pharmaceutical effects. Frontiers in Immunology 10: 3067. https://doi.org/10.3389/fimmu.2019.03067

Šimo L., Kazimirova M., Richardson J., Bonnet S.I. 2017. The essential role of tick salivary glands and saliva in tick feeding and pathogen transmission. Frontiers in Cellular an Infection Microbiology 7(281). https://doi.org/10.3389/fcimb.2017.00281

Lewandowski D., Urbanowicz A., Figlerowicz M. 2013. Molekularne podłoże oddziaływań pomiędzy Borrelia burgdorferi, kleszczem i kręgowcem [Molecular interactions between Borrelia burgdorferi ticks and mammals]. Postępy Mikrobiologii 52(1): 9–16 (in Polish with summary in English).

Pal U., Li X., Wang T., Montgomery R.R., Ramamoorthi, N., deSilva, A.M., Bao F., Yang X., Pypaert M., Pradhan D., Kantor F.S., Telford S., Anderson J.F., Fikrig E. 2004. TROSPA, an Ixodes scapularis receptor for Borrelia burgdorferi. Cell 119(4): 457–468. https://doi.org/10.1016/j.cell.2004.10.027

Coumou J., Narasimhan S., Trentelman J.J., Wagemakers A., Koetsveld J., Ersoz J.I., Oei A., Fikrig E., Hovius J.W. 2016. Ixodes scapularis dystroglycan-like protein promotes Borrelia burgdorferi migration from the gut. Journal of Molecular Medicine 94: 361–370. https://doi.org/10.1007/s00109-015-1365-0

Rudenko N., Golovchenko M., Edwards M.J., Grubhoffer L. 2005. Differential expression of Ixodes ricinus tick genes induced by blood feeding or Borrelia burgdorferi infection. Journal of Medical Entomology 42(1): 36–41.

Herrmann C., Gern L. 2015. Search for blood or water is influenced by Borrelia burgdorferi in Ixodes ricinus, Parasites and Vectors 8(6). https://doi.org/10.1186/s13071-014-0526-2

Alekseev A.N., Jensen P.M., Dubinina H.V., Smirnova L.A., Makrouchina N.A., Zharkov S.D. 2000. Peculiarities of behaviour of taiga (Ixodes persulcatus) and sheep (Ixodes ricinus) ticks (Acarina: Ixodidae) determined by different methods. Folia Parasitologica 47(2): 147–153. https://doi.org/10.14411/fp.2000.029

Lefcort H, Durden LA. 1996. The effect of infection with Lyme disease spirochetes (Borrelia burgdorferi) on the phototaxis, activity, and questing height of the tick vector Ixodes scapularis. Parasitology 113(2): 97–103. https://doi.org/10.1017/s0031182000066336

Michalski M.M., Dmitryjuk M. 2018. Czy zagraża nam anaplazmoza? [An imminent threat of anaplasmosis?] In: Choroby zakaźne i pasożytnicze – perspektywy badawcze. (Eds. M. Maciąg, K. Maciąg). Lublin, Wydawnictwo Naukowe TYGIEL: 7–13 (in Polish).

Bakken J.S., Dumler S. 2008. Human granulocytic anaplasmosis. Infectious Disease Clinics of North America 22(3): 433–448. https://doi.org/10.1016/j.idc.2008.03.011

Chen S.M., Dumler J.S., Bakken J.S., Walker D.H. 1994. Identification of a granulocytotropic Ehrlichia species as the etiologic agent of human disease. Journal of Clinical Microbiology 32(3): 589–595. https://doi.org/10.1128/jcm.32.3.589-595.1994

Dumler J.S., Choi K.S., Garcia-Garcia J.C., Barat N.S., Scorpio D.G., Garyu J.W., Grab D.J., Bakken J.S. 2005. Human granulocytic anaplasmosis and Anaplasma phagocytophilum. Emerging Infectious Diseases 11(12): 1828–1834. https://doi.org/10.3201/eid1112.050898

Zawilińska B. 2014. Inne bakterie – Rickettsiaceae, Anaplasmataceae i Coxiellaceae. In: Mikrobiologia lekarska (Eds. P.B. Heczko, A. Pietrzyk, M. Wróblewska). PZWL. Warszawa: 229–236 (in Polish).

Matei I.A., Estrada-Peña A., Cutler S.J.. Vayssier- Tausat M., Varela-Castro L., Potkonjak A., Zeller H., Mihalca A.D. 2019. A review on the eco- epidemiology and clinical management of human granulocytic anaplasmosis and its agent in Europe. Parasites and Vectors 12(599). https://doi.org/10.1186/s13071-019-3852-6

Jahfari S., Ruyts S.C., Frazer-Mendelewska E., Jaarsma R., Verheyen K., Sprong H. 2017. Melting pot of tick-borne zoonoses: the European hedgehog contributes to the maintenance of various tick-borne diseases in natural cycles urban and suburban areas. Parasites and Vectors 10(134). https://doi.org/10.1186/s13071-017-2065-0

Russell A., Prusinski M., Sommer J., O’Connor C., White J., Falco R., Kokas J., Vinci V., Gall W., Tober K., Haight J., Oliver J., Meehan L., Sporn L.A., Brisson D., Backenson P.B. 2021. Epidemiology and spatial emergence of anaplasmosis, New York, USA, 2010‒2018. Emerging Infectious Diseases 27(8): 2154–2162. https://doi.org/10.3201/eid2708.210133

Stańczak J., Gabre R., Kruminis-Łozowska W., Racewicz M., Biernat B. 2004. Ixodes ricinus as a vector of Borrelia burgdorferi sensu lato, Anaplasma phagocytophilum and Babesia microti in urban and suburban forests. Annals of Agricultural and Environmental Medicine 11(1): 109–114.

Grzeszczuk A., Stańczak J., Biernat B., Racewicz M., Kruminis-Łozowska, W., Prokopowicz D. 2004. Human anaplasmosis in north-eastern Poland: seroprevalence in humans and prevalence in Ixodes ricinus ticks. Annals of Agricultural and Environmental Medicine 11(1): 99–103.

Karbowiak G., Biernat B., Stańczak J., Werszko J., Wróblewski P., Szewczyk T., Sytykiewicz H. 2016. The role of particular ticks developmental stages in the circulation of tick-borne pathogens in Central Europe. 4. Anaplasmataceae. Annals of Parasitology 62(4): 267–284. https://doi.org/10.17420/ap6204.62

Hidano A., Konnai S., Yamada S., Githaka N., Isezaki M., Higuchi H., Nagahata H., Ito T., Takano A., Ando S., Kawabata H., Murata S., Ohahsi K. 2014. Suppressive effects of neutrophil by Salp16- like salivary gland proteins from Ixodes persulcatus Schulze tick. Insect Molecular Biology 23(4): 466–474 https://doi.org/10.1111/imb.12101

Sultana H., Neelakanta G., Kantor F.S., Malawista S.E., Fish D., Montgomery R.R., Fikrig E. 2010. Anaplasma phagocytophilum induces actin phosphorylation to selectively regulate gene transcription in Ixodes scapularis ticks. Journal of Experimental Medicine 207(8): 1727–1743 https://doi.org/10.1084/jem.20100276

Soukumaran B., Narasimhan S., Anderson J.F., DePonte K, Marcantonio N., Krishnan M.N., Fish D., Telford S.R., Kantor F.S., Fikrig E. 2006. An Ixodes scapularis protein required for survival of Anaplasma phagocytophilum in tick salivary glands. Journal of Experimental Medicine 203(6): 1507–1517 https://doi.org/0.1084/jem.20060208

Liu L., Narasimhan S., Dai J., Zhang L., Cheng G., Fikrig E. 2011. Ixodes scapularis salivary gland protein P11 facilitates migration of Anaplasma phagocytophilum from the tick gut to salivary glands. EMBO Reports 12(11): 1196–1203. https://doi.org/10.1038/embor.2011.177

Ayllón N., Villar M., Busby A.T., Kocan K.M., Blouin E.F., Bonzón Kulichenko E., Galindo R.C., Mangold A.J., Alberdi P., Pérez de la Lastra J.M., Vázquez J., de la Fuente J. 2013. Anaplasma phagocytophilum inhibits apoptosis and promotes cytoskeleton rearrangement for infection of tick cells. Infection and Immunity 81(7): 2415–2425. https://doi.org/0.1128/IAI.00194-13

de la Fuente J., Blouin E.F., Manzano-Roman R., Naranjo V., Almazan C., de la Lastra J.M.P., Zivkovic Z., Massung R.F., Jongejan F., Kocana K.M. 2008. Differential expression of the tick protective antigen subolesin in Anaplasma marginale and A. phagocytophilum-infected host cells. Annals of the New York Academy of Sciences 1149(1): 27-35. https://doi.org/10.1196/annals.1428.056

Neelakanta G., Sultana H., Fish D., Anderson J.F., Fikrig E. 2010. Anaplasma phagocytophilum induces Ixodes scapularis ticks to express an antifreeze glycoprotein gene that enhances their survival in the cold. The Journal of Clinical Investigation 120(9): 3179-3190. https://doi.org/10.1172/JCI42868

Ross D,E., Levin M.L. 2004. Effects of Anaplasma phagocytophilum infection on the molting success of Ixodes scapularis (Acari: Ixodidae) larvae. Journal of Medical Entomology 41(3): 476-483. https://doi.org/10.1603/0022-2585-41.3.476

Sahni A., Fang R., Sahni S. K., Walker D. H. 2019. Pathogenesis of rickettsial diseases: pathogenic and immune mechanisms of an endotheliotropic infection. Annual Review of Pathology 14: 127-152. https://doi.org/10.1146/annurev-pathmechdis-012418-012800

Zając V., Sroka J., Sawczyn-Domańska A., Kloc A., Wójcik-Fatla A. 2019. Wystńôpowanie riketsji z grupy gorńÖczek plamistych w Polsce. Environmental Medicine 22(1-2): 13-19. https://doi.org/10.26444/ms/119717

Biernat B., Stańczak J., Michalik J., Sikora B., Wierzbicka A. 2016. Prevalence of infection with Rickettsia helvetica in Ixodes ricinus ticks feeding on non-rickettsiemic rodent hosts in sylvatic habitats of west-central Poland. Ticks and Tick-Borne Diseases 7(1): 135-141. https://doi.org/10.1016/j.ttbdis.2015.10.001

Chmielewski T., Podsiadly E., Karbowiak G., Tylewska-Wierzbanowska S. 2009. Rickettsia spp. in ticks, Poland. Emerging Infectious Diseases 15(3): 486-488. https://doi.org/10.3201/eid1503.080711

Hussain S., Perveen N., Hussain A., Song B., Aziz MU., Zeb J., Li J., George D., Cabezas-Cruz A., Sparagano O. 2022. The symbiotic continuum within ticks: opportunities for disease control. Frontiers in Microbiology 13: 854803. https://doi.org/10.3389/fmicb.2022.854803

Frątczak M., Vargová B., Tryjanowski P., Majláth I., Jerzak L., Kurimský J., Cimbala R., Jankowiak Ł., Conka Z., Majláthová V. 2020. Infected Ixodes ricinus ticks are attracted by electromagnetic radiation of 900MHz. Ticks and Tick-Borne Diseases 11(4): 101416. https://doi.org/10.1016/j.ttbdis.2020.101416

Downloads

Published

2023-09-25

How to Cite

Kiewra, D., & Krysmann, A. (2023). Interactions between hard ticks (Ixodidae) and bacterial tick-borne pathogens. Annals of Parasitology, 69(1), 7–16. Retrieved from https://annals-parasitology.eu/index.php/AoP/article/view/8

Issue

Section

Review articles