Comparative Clinical Pathology

, Volume 28, Issue 3, pp 585–592 | Cite as

Applications of electron microscopy in ticks: description, detection of pathogens, and control

  • Sobhy Abdel-Shafy
  • Alaa A. Ghazy
  • Raafat M. ShaapanEmail author
Review Article


Electron microscopy (EM) is a very good tool in the biological researches. It is mainly used in the morphological description of adult and immature stages of ticks. In this review, different applications of EM in identification of ticks were discussed. In general, the applications of EM have been presented in four topics: morphological descriptions, comparative taxonomy, detection of pathogens in tick organs, and drug efficacy on ticks. EM was used in the description of a new tick or description of a tick which was described before to clarify additional characters that were not observed before by light microscope (LM). It is obvious that the EM provides all the morphological characters clearly in details. However, ticks have ornamented characters on their scutum, so it is necessary to use LM as well as molecular biology to confirm the morphological characters. EM is also used in detection of ultrastructure of pathogenic organisms in the cell lines or tissues of tick vectors that infected experimentally or naturally by pathogen. EM also helps to know the effect of new drugs or its mode of action by photography of the alterations which may occur on the integument or other tick organs such as the digestive system.


Ticks Electron microscopy Morphology Taxonomy Drug efficacy Pathogens 



This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Compliance with ethical standards

Ethical approval

Ethical clearance and approval were obtained from the National Research Centre Ethics Committee. Approval permission and written consents were obtained from all the participants in the study before collecting the data, and all had the right to withdraw from the study at any time without any explanation.

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdel-Shafy S (2005) Scanning electron microscopy and comparative morphology of argasid larvae (Acari: Ixodida: Argasidae) infesting birds in Egypt. Acarologia 45:3–12Google Scholar
  2. Abdel-Shafy S (2008a) Scanning electron microscopy and comparative morphology of Hyalomma anatolicum excavatum, H. dromedarii and H. marginatum marginatum (Acari: Ixodidae) based on nymphs. Acarologia 48:3–18Google Scholar
  3. Abdel-Shafy S (2008b) Scanning electron microscopy and comparative morphology of Hyalomma anatolicum excavatum, H. dromedarii and H. marginatum marginatum (Acari: Ixodidae) based on larvae. Acarologia 48:19–31Google Scholar
  4. Abdel-Shafy S, Habeeb SM, El Namaky AH, Abou-Zeina HAA (2013) Scanning electron microscopy of nymphal and larval stages of the cattle tick Rhipicephalus (Boophilus) annulatus (say) 1821(Acari: Ixodidae). Global Vet 10:1–8CrossRefGoogle Scholar
  5. Abdel-Shafy S, Shaapan RM, Abdelrahman KA, El-Namaky AH, Abo-Aziza FAM, Abou Zeina HA (2015) Detection of Toxoplasma gondii (Apicomplexa: Sarcocystidae) in the brown dog tick Rhipicephalus sanguineus (Acari: Ixodidae) fed on infected rabbits. Res J Parasitol 10:142–150CrossRefGoogle Scholar
  6. Abdel-Shafy S, Gabr HS, Abdullah HH, Mahmoud MS (2016) Morphological and molecular description of immature stages of Ornithodoros savignyi (Acari: Argasidae). Parasitol Res 115:3033–3040CrossRefGoogle Scholar
  7. Abdullah HHAM, El-Molla A, Salib FA, Allam NAT, Ghazy AA, Abdel-Shafy S (2016) Morphological and molecular identification of the brown dog tick Rhipicephalus sanguineus and the camel tick Hyalomma dromedarii (Acari: Ixodidae) vectors of rickettsioses in Egypt. Vet World 9:1087–1101CrossRefGoogle Scholar
  8. Amosova LI (2000) Ultrastructural investigation of Borreliae in females of the tick Ixodes persulcatus. Parazitologiya 34:239–240Google Scholar
  9. Baker GT (1997) Spiracular plate of nymphal and adult hard ticks (Acarina: Ixodidae): morphology and cuticular ultrastructure. Invert Biol 116:341–347CrossRefGoogle Scholar
  10. Balashov IS, Amosova LI, Grigor'eva LA (1998) Transovarial and transphasic transmissions of Borrelia by the taiga tick Ixodes persulcatus (Ixodidae). Parazitologiia 32:489–494Google Scholar
  11. Barros-Battesti DM, Arzua M, Rebello VM, da Barbieri SF, Famadas KM (2005) Description of the larva of Amblyomma longirostre (Koch,1844)(Acari: Ixodidae) by light and scanning electron microscopy. Rev Bras Parasitol Vet 14:51–57Google Scholar
  12. Billeter SA, Diniz PPVP, Battisti JM, Munderloh UG, Breitschwerdt EB, Levy MG (2009) Infection and replication of Bartonella species within a tick cell line. Exp Appl Acarol 49:193–208CrossRefGoogle Scholar
  13. Braet F, De Zanger R, Wisse E (1997) Drying cells for SEM, AFM and TEM by hexamethyldisilazane: a study on hepatic endothelial cells. J Microsc 186:84–87CrossRefGoogle Scholar
  14. Brahma RK, Dixit V, Sangwan AK, Doley R (2014) Identification and characterization of Rhipicephalus (Boophilus) microplus and Haemaphysalis bispinosa ticks (Acari: Ixodidae) of North East India by ITS2 and 16S rDNA sequences and morphological analysis. Exp Appl Acarol 62:253–265CrossRefGoogle Scholar
  15. Bray DF, Bagu J, Koegler P (1993) Comparison of hexamethyldisilazane (HMDS), Peldri II, and critical-point drying methods for scanning electron microscopy of biological specimens. Microsc Res Tech 26:489–495CrossRefGoogle Scholar
  16. Buczek A, Jasik K, Buczek L (1998) Sense organs in post-embryonic stages of Hyalomma marginatum marginatum Koch, 1844 (Acari: Ixodida: Ixodidae). I Tarsal sensory system. Parassitologia 40:279–282Google Scholar
  17. Contini C, Palmas C, Seu V, Stancampiano L, Usai F (2011) Redescription of the male of Ixodes festai Rondelli, 1926 (Ixodida: Ixodidae) on specimens from Sardinia (Italy). Parasite 18:235–240CrossRefGoogle Scholar
  18. Danilatos GD (1988) In: Hawkes PW (ed) In advances in electronics and electron physics. Academic Press, London, pp 109–250Google Scholar
  19. Danilatos GD (1990) In: Hawkes PW (ed) In advances in electronics and electron physics. Academic Press, New York, pp 4–102Google Scholar
  20. de Souza W, Campanati L, Attias M (2008) Strategies and results of field emission scanning electron microscopy (FE-SEM) in the study of parasitic protozoa. Micron 39:77–87CrossRefGoogle Scholar
  21. Duh D, Punda-Polic V, Avsic-Zupanc T, Bouyer D, Walker DH, Popov VL, Jelovsek M, Gracner M, Trilar T, Bradaric N, Kurtti TJ, Strus J (2010) Rickettsia hoogstraalii sp. nov., isolated from hardand soft-bodied ticks. Int J Syst Evol Microbiol 60:977–984CrossRefGoogle Scholar
  22. Echlin P (2009) Handbook of sample preparation for scanning electron microscopy and x-ray microanalysis. Cambridge Analytical Microscopy, UKCrossRefGoogle Scholar
  23. Ghosh HS, Misra KK (2012) Scanning electron microscope study of a snake tick, Amblyomma gervaisi (Acari: Ixodidae). J Parasit Dis 36:239–250CrossRefGoogle Scholar
  24. Ghosh HS, Roy S, Sanyal AK, Misra KK (2017) Microscopic anatomy of the Haller’s organ of snake ticks. Int J Acarol 43:1–9CrossRefGoogle Scholar
  25. Goldberg MW (2008) Immunolabeling for scanning electron microscopy (SEM) and field emission SEM. Methods Cell Biol 88:109–130CrossRefGoogle Scholar
  26. Goldstein J, Yakowitz H (1975) Practical scanning electron microscopy. Plenum, New YorkCrossRefGoogle Scholar
  27. Guimaräes AM (1997) Ultrastructure of sporogony in Babesia equi in salivary glands of adult female Boophilus microplus ticks. Parasitol Res 84:69–74CrossRefGoogle Scholar
  28. Habeeb SM, Abdel-Shafy S, Youssef AE (2007) Light, scanning electron microscopy and SDS-PAGE studies on the effect of the essential oil, Citrus sinensis var. balady on the embryonic development of camel tick Hyalomma dromedarii (Koch, 1818) (Acari: Ixodidae). Pak J Biol Sci 10:1151–1160CrossRefGoogle Scholar
  29. Hayat MA (1974) Principles and techniques of scanning electron microscopy, vol 1–6. Van Nostrand Reinhold, New YorkGoogle Scholar
  30. Hirsch JG, Fedorko ME (1968) Ultrastructure of human leukocytes after simultaneous fixation with glutaraldehyde and osmium tetroxide and “postfixation” in uranyl acetate. J Cell Biol 38:615–627CrossRefGoogle Scholar
  31. Holt DB, Muir MD, Grant PR, Boswarva IM (1974) Quantitative scanning electron microscopy. Academic Press, LondonGoogle Scholar
  32. Huxley HE, Zubay G (1961) Preferential staining of nucleic acid-containing structures for electron microscopy. J Biophys Biochem Cytol 11:273–296CrossRefGoogle Scholar
  33. Ishigaki Y, Nakamura Y, Oikawa Y, Yano Y, Kuwabata S, Nakagawa H, Tomosugi N, Takegami T (2012) Observation of live ticks (Haemaphysalis flava) by scanning electron microscopy under high vacuum pressure. PLoS ONE 7:e32676CrossRefGoogle Scholar
  34. Johari O (1968) Proceedings of the Annual Scanning Electron Microscopy Symposium. Annual Conferences since. IIT Research Institute; since 1987 Scanning Microscopy. Scanning Microsc. Intl., ChicagoGoogle Scholar
  35. Karnovsky MJ (1965) A formaldehyde-gluteraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137AGoogle Scholar
  36. Klyachko O, Stein BD, Grindle N, Clay K, Fuqua C (2007) Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl Environ Microbiol 73:6584–6594CrossRefGoogle Scholar
  37. Knoll M (1935) Aufladepotentiel und Sekundäremission elektronenbestrahlter Körper. Z Tech Phys 11:467Google Scholar
  38. Leemon DM, Jonsson NN (2012) Comparative studies on the invasion of cattle ticks (Rhipicephalus (Boophilus) microplus) and sheep blowflies (Lucilia cuprina) by Metarhizium anisopliae (Sorokin). J Invertebr Pathol 109:248–259CrossRefGoogle Scholar
  39. Leonovich SA (2009) Fine structural features of the sensory system in the ixodid tick Dermacentor niveus (parasitiformes, ixodidae). Parazitologiya 43:3–11Google Scholar
  40. Marques S, Barros-Battesti DM, Onofrio VC, Famadas KM, Faccini JLH, Keirans JE (2004) Redescription of larva, nymph and adults of Ixodes (I.) loricatus Neumann, 1899 (Acari: Ixodidae) based on light and scanning electron microscopy. Syst Parasitol 59:135–146CrossRefGoogle Scholar
  41. Martins TF, Onofrio VC, Barros-Battesti DM, Labruna MB (2010) Nymphs of the genus Amblyomma (Acari: Ixodidae) of Brazil: descriptions, redescriptions, and identification key. Ticks Tick Borne Dis 1:75–99CrossRefGoogle Scholar
  42. Massoud AM, Kutkat MA, Abdel-Shafy S, El-Khateeb RM, Labib IM (2005) Acaricidal efficacy of myrrh (Commiphora molmol) on the fowl tick Argas persicus (Acari: Argasidae). J Egypt Soc Parasitol 35:667–686Google Scholar
  43. Millonig G, Marinozzi V (1968) Fixation and embedding in electron microscopy. Adv Opt & Elec Micros 2:251–341Google Scholar
  44. Miyoshi N, Isogai E, Hiramatsu K, Sasaki T (2017) Activity of tick antimicrobial peptide from Ixodes persulcatus (persulcatusin) against cell membranes of drug-resistant Staphylococcus aureus. J Antibiot 70:142–146CrossRefGoogle Scholar
  45. Mizuhira V, Futaesaku Y (1972) New fixation method for biological membranes using tannic acids. Acta Histochem Cytochem 5:233–236CrossRefGoogle Scholar
  46. Mollenhauer HH (1993) Artifacts caused by dehydration and epoxy embedding in transmission electron microscopy. Microsc Res Tech 26:496–512CrossRefGoogle Scholar
  47. Montasser AA (2006) The camel tick, Hyalomma (Hyalomma) dromedarii koch, 1844 (ixodoidea: ixodidae): description of the egg and redescription of the larva by scanning electron microscopy. Inter J Zool Res 2:14–29CrossRefGoogle Scholar
  48. Montasser AA (2010) The fowl tick, Argas (Persicargas) persicus (Ixodoidea: Argasidae): description of the egg and redescription of the larva by scanning electron microscopy. Exp Appl Acarol 52:343–361CrossRefGoogle Scholar
  49. Montasser AA, Amin A (2005) Fine structure of the integument of Argas (Persicargas) persicus (Oken) (Ixodoidea: Argasidae). Entomologica Fennica 16:193–200Google Scholar
  50. Moreira LH, Figueiredo TFB, Alves LP, Fernandes AB, Zângaro RA, Mendes ALS, Gaudêncio FN, de Lima CJ (2018) Effect of ozone as Acaricide: action of the ozone on the cuticle and respiratory spiracle of tick Rhipicephalus sanguineus sensu lato. Ozone Sci Eng 40:183–190CrossRefGoogle Scholar
  51. Müllerová I, Frank L (2003) In: Hawkes PW (ed) Advances in imaging and Electron physics. Academic Press, Amsterdam, pp 310–443Google Scholar
  52. Muňoz L, Casanueva ME (2002) Ticks (Acari: Ixodidae) on dogs in Concepción city, Chile. Arch Med Vet 34:131–134Google Scholar
  53. Nava S, Mangold AJ, Mastropaolo M, Venzal JM, Oscherov EB, Guglielmone AA (2009) Amblyomma boeroi n. sp. (Acari: Ixodidae), a parasite of the Chacoan peccary Catagonus wagneri (Rusconi) (Artiodactyla: Tayassuidae) in Argentina. Syst Parasitol 73:161–174CrossRefGoogle Scholar
  54. Oatley CW (1972) The scanning electron microscope—part 1: the instrument. Cambridge University Press, CambridgeGoogle Scholar
  55. Ohnsorge J, Holm R (1973) Rasterelektronenmikroskopie—Eine Einführung für Mediziner und Biologen. Georg Thieme Publishers, StuttgartGoogle Scholar
  56. Onofrio VC, Barros-Battesti DM, Marques S, Faccini JLH, Labruna MB, Beati L, Guglielmone AA (2008) Redescription of Amblyomma varium Koch, 1844 (Acari: Ixodidae) based on light and scanning electron microscopy. Syst Parasitol 69:137–144CrossRefGoogle Scholar
  57. Pfefferkorn G (1968) Beiträge zur elektronenmikroskopischen Direktabbildung und Analyse von Oberfl ächen (BEDO) (Engl.: Proceedings of Direct Electron Microscopic Imaging and Analysis of Surfaces). Annual Conferences sinceGoogle Scholar
  58. Reimer L (1978) Scanning electron microscopy—present state and trends. Scann 1:3–16CrossRefGoogle Scholar
  59. Reimer L, Pfefferkorn G (1973) Raster-Elektronenmikroskopie. Springer, Berlin, p 241CrossRefGoogle Scholar
  60. Reimer L, Pfefferkorn G (1977) Raster-Elektronenmikroskopie. Springer, Berlin, p 290CrossRefGoogle Scholar
  61. Reipert S, Kotisch H, Wysoudil B, Wiche G (2008) Rapid microwave fixation of cell monolayers preserves microtubule-associated cell structures. J Histochem Cytochem 56:697–709CrossRefGoogle Scholar
  62. Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212CrossRefGoogle Scholar
  63. Ribeiro MFB, Lima JD (1996) Morphology and development of Anaplasma marginale in midgut of engorged female ticks of Boophilus microplus. Vet Parasitol 61:31–39CrossRefGoogle Scholar
  64. Ribeiro MFB, Passos LMF (2006) Natural co-infection of Babesia caballi and Encephalitozoon-like microsporidia in the tick Anocentor nitens (Acari: Ixodidae). J Invertebr Pathol 93:183–185CrossRefGoogle Scholar
  65. Ruska E (1979) Die frühe Entwicklung der Elektronenlinsen und der Elektronenmikroskopie. (Deutsche Akademie der Naturforscher Leopoldina, Halle). Acta Hist Leopoldina 12:7–136Google Scholar
  66. Saito KC, Bechara GH, Nunes ET, De Oliveira PR, Denardi SE, Mathias MIC (2005) Morphological, histological, and ultrastructural studies of the ovary of the cattle-tick Boophilus microplus (Canestrini, 1887) (Acari: Ixodidae). Vet Parasitol 129:299–311CrossRefGoogle Scholar
  67. Santos AS, Bacellar F, Santos-Silva M, Formosinho P, Grácio AJ, Franca S (2002) Ultrastructural study of the infection process of Rickettsia conorii in the salivary glands of the vector tick Rhipicephalus sanguineus. Vector Borne Zoonotic Dis 2:165–177CrossRefGoogle Scholar
  68. Sawyer LC, Grubb DT (1996) Polymer microscopy. Chapman & Hall, LondonCrossRefGoogle Scholar
  69. Silva MT, Guerra FC, Magalhaes MM (1968) The fixative action of uranyl acetate in electron microscopy. Experientia 24:1074CrossRefGoogle Scholar
  70. Simser JA, Palmer AT, Fingerle V, Wilske B, Kurtti TJ, Munderloh UG (2002) Rickettsia monacensis sp. nov., a spotted fever group rickettsia, from ticks (Ixodes ricinus) collected in a European city park. Appl Environ Microbiol 68:4559–4566CrossRefGoogle Scholar
  71. Stein O, Stein Y (1971) Light and electron microscopic radioautography of lipids: techniques and biological applications. Adv Lipid Res 9:1–72CrossRefGoogle Scholar
  72. Sunyakumthorn P, Bourchookarn A, Pornwiroon W, David C, Barker SA, Macaluso KR (2008) Characterization and growth of polymorphic Rickettsia felis in a tick cell line. Appl Environ Microbiol 74:3151–3158CrossRefGoogle Scholar
  73. Vannier-Santos MA, de Castro SL (2009) Electron microscopy in antiparasitic chemotherapy: a (close) view to a kill. Curr Drug Targets 10:246–260CrossRefGoogle Scholar
  74. Venzal JM, Estrada-Peňa A, Barros-Battesti DM, Onofrio VC, Beldoménico PM (2005) Ixodes (Ixodes) pararicinus Keirans & Clifford, 1985 (Acari: Ixodidae): description of the immature stages, distribution, hosts and medical/veterinary importance. Syst Parasitol 60:225–234CrossRefGoogle Scholar
  75. von Ardenne M (1938) Das Elektronen Rastermikroskop, Praktische Auftihrung. Z Tech Phys 19:407Google Scholar
  76. Watson ML (1958) Staining of tissue sections for electron microscopy with heavy metals. II. Application of solutions containing lead and barium. J Biophys Biochem Cytol 4:727–730CrossRefGoogle Scholar
  77. Webster P (2007) Microwave-assisted processing and embedding for transmission electron microscopy. Methods Mol Biol 369:47–65CrossRefGoogle Scholar
  78. Wells OC (1974) Scanning electron microscopy. McGraw-Hill, New YorkGoogle Scholar
  79. Wells OC (1975) Scanning electron microscopy. McGraw-Hill, New YorkGoogle Scholar
  80. Weston AE, Armer HEJ, Collinson LM (2010) Towards native-state imaging in biological context in the electron microscope. J Chem Biol 3:101–112CrossRefGoogle Scholar
  81. Williams DB, Carter CB (2009) Transmission electron microscopy a textbook for materials science. Springer ScienceBusiness Media, LLC, pp 3–22CrossRefGoogle Scholar
  82. Zworykin VK, Hillier J, Snyder RL (1942) A scanning electron microscope. ASTM Bull 117:15Google Scholar

Copyright information

© Springer-Verlag London Ltd., part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Parasitology and Animal Diseases, Veterinary Research DivisionNational Research CentreGizaEgypt
  2. 2.Giza, National Research CentreGizaEgypt

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