The Importance of Ticks in Q Fever Transmission: What Has (and Has Not) Been Demonstrated?

Trends in Parasitology

Volumn 31, Issue 11, 2015, Pages 536-552

  Duron, Olivier ^a   Sidi Boumedine, Karim ^b   Rousset, Elodie ^b   Moutailler, Sara ^c   Jourdain, Elsa ^d  

^a University de Montpellier   (France)

^b FRENCH AGENCY FOR FOOD   (France)

^c ECOLE NATIONALE VÉTÉRINAIRE D ALFORT   (France)

^d EPIA   (France)

Author keywords

[No Author keywords available]

Indexed keywords

VIRULENCE FACTOR;

BACTERIUM DETECTION; COXIELLA BURNETII; DISEASE CARRIER; DISEASE TRANSMISSION; HUMAN; NONHUMAN; Q FEVER; REVIEW; TICK; ZOONOSIS; ANIMAL; CLASSIFICATION; COXIELLA; GENETICS; MICROBIOLOGY; PHYSIOLOGY; TICK BORNE DISEASE; TRANSMISSION;

ANIMALS; COXIELLA; COXIELLA BURNETII; HUMANS; Q FEVER; TICK-BORNE DISEASES; TICKS;

EID: 84946488709     PISSN: 14714922     EISSN: 14715007     Source Type: Journal    
DOI: 10.1016/j.pt.2015.06.014     Document Type: Review

References (123)

1. Lang G.H. Coxiellosis (Q fever) in animals. Q FEVER (Vol. 1) The Disease 1990, 23-48. CRC Press. T.J. Marrie (Ed.).
2. EFSA Panel on Animal Health and Welfare (AHAW) Scientific Opinion on Q fever. EFSA J. 2010, 8:1595.
3. Rousset E., et al. Q Fever. Manual of Diagnostic Tests and Vaccines for Terrestrial Animals 2010, 13. Office International des Epizooties (OIE) - World Organisation for Animal Health.
4. Angelakis E., Raoult D. Q Fever. Vet. Microbiol. 2010, 140:297-309.
5. Raoult D., et al. Natural history and pathophysiology of Q fever. Lancet Infect. Dis. 2005, 5:219-226.
6. van Asseldonk M.A.P.M., et al. Economic assessment of Q fever in the Netherlands. Prev. Vet. Med. 2013, 112:27-34.
7. van der Hoek W., Morroy G. Epidemic Q fever in humans in the Netherlands. Coxiella burnetii: Recent Advances and New Perspectives in Research of the Q Fever bacterium 2012, 329-364. Springer. R. Toman (Ed.).
8. Madariaga M.G., et al. Q fever: a biological weapon in your backyard. Lancet Infect. Dis. 2003, 3:709-721.
9. Khavkin T. Q fever studies in the U.S.S.R. Q fever: The Biology of Coxiella burnetti 1991, 311-326. CRC Press. J.C. Williams, H.A. Thompson (Eds.).
10. McDade J.E. Historical aspects of Q fever. Q FEVER (Vol. 1) The Disease 1990, 5-22. CRC Press. T.J. Marrie (Ed.).
11. Babudieri B. Q fever: a zoonosis. Adv. Vet. Sci. 1959, 5:81-154.
12. Pacheco R.C., et al. Coxiella burnetii in ticks, Argentina. Emerg. Infect. Dis. 2013, 19:344-346.
13. Loftis A.D., et al. Rickettsial agents in Egyptian ticks collected from domestic animals. Exp. Appl. Acarol. 2006, 40:67-81.
14. Philip C.B. Observations on experimental Q fever. J. Parasitol. 1948, 34:457-464.
15. Parker R.R., Davis G.E. A filter-passing infectious agent isolated from ticks. II. Transmission by Dermacentor andersoni. Public Health Rep. 1938, 53:2267-2276.
16. Smith D.J.W. Studies in the Epidemiology of Q fever. 3. Transmission of Q fever by the tick Haemaphysalis humerosa. Aust. J. Exp. Biol. Med. Sci. 1940, 103-118.
17. Davis G.E. American Q fever: experimental transmission by the argasid ticks Ornithodoros moubata and O. hermsi. Public Health Rep. 1943, 58:984-987.
18. Stuen S., et al. Anaplasma phagocytophilum-a widespread multi-host pathogen with highly adaptive strategies. Front. Cell Infect. Microbiol. 2013, 3:31.
19. Mediannikov O., et al. Coxiella burnetii in humans and ticks in rural Senegal. PLoS Negl. Trop. Dis. 2010, 4:8.
20. Stein A., Raoult D. Pigeon pneumonia in Provence: a bird-borne Q fever outbreak. Clin. Infect. Dis. 1999, 29:617-620.
21. Davoust B., et al. Three-toed sloth as putative reservoir of Coxiella burnetii, Cayenne, French Guiana. Emerg. Infect. Dis. 2014, 20:1760-1761.
22. Bennett M.D., et al. Coxiella burnetii in western barred bandicoots (Perameles bougainville) from Bernier and Dorre Islands in Western Australia. Ecohealth 2011, 8:519-524.
23. Lapointe J.M., et al. Placentitis due to Coxiella burnetii in a Pacific harbor seal (Phoca vitulina richardsi). J. Vet. Diagn. Investig. 1999, 11:541-543.
24. Enright J.B., et al. Coxiella burnetii in a wildlife-livestock environment: distribution of Q fever in wild mammals. Am. J. Epidemiol. 1971, 94:62-71.
25. Kersh G.J., et al. Coxiella burnetii infection of marine mammals in the Pacific Northwest, 1997-2010. J. Wildlife Dis. 2012, 48:201-206.
26. Gonzalez-Barrio D., et al. Coxiella burnetii shedding by farmed red deer (Cervus elaphus). Transboundary Emerg. Dis. 2013, Published online October 15 2013. 10.1111/tbed.12179.
27. Sprong H., et al. Prevalence of Coxiella burnetii in ticks after a large outbreak of Q fever. Zoonoses Public Health 2012, 59:69-75.
28. Cardinale E., et al. Emergence of Coxiella burnetii in ruminants on Reunion Island? Prevalence and risk factors. PLoS Negl. Trop. Dis. 2014, 8:e3055.
29. Psaroulaki A., et al. Epidemiological study of Q fever in humans, ruminant animals, and ticks in Cyprus using a geographical information system. Eur. J. Clin. Microbiol. Infect. Dis. 2006, 25:576-586.
30. Cantas H., et al. Q fever abortions in ruminants and associated on-farm risk factors in Northern Cyprus. BMC Vet. Res. 2011, 7:13.
31. van Engelen E., et al. Prevalence and risk factors for Coxiella burnetii (Q fever) in Dutch dairy cattle herds based on bulk tank milk testing. Prev. Vet. Med. 2014, 117:103-109.
32. Asadi J., et al. Risk factors of Q fever in sheep and goat flocks with history of abortion. Comp. Clin. Pathol. 2012, 23:625-630.
33. Eklund C.M., et al. A case of Q fever probably contracted by exposure to ticks in nature. Public Health Rep. 1947, 62:1413-1416.
34. Pascual-Velasco F., et al. Fiebre Q tras picadura de garrapatas. Enferm. Infecc. Microbiol. Clín. 2007, 25:360.
35. Dubourg G., et al. Scalp eschar and neck lymphadenopathy after tick bite: an emerging syndrome with multiple causes. Eur. J. Clin. Microbiol. Infect. Dis. 2014, 33:1449-1456.
36. Beaman M.H., Hung J. Pericarditis associated with tick-borne Q fever. Aust. N. Z. J. Med. 1989, 19:254-256.
37. Nett R.J., et al. Q Fever with unusual exposure history: a classic presentation of a commonly misdiagnosed disease. Case Rep. Infect. Dis. 2012, 2012:916142.
38. Janbon F., et al. Concomitant human infection due to Rickettsia conorii and Coxiella burnetii. J. Infect. Dis. 1989, 160:354-355.
39. Rolain J.M., et al. Concomitant or consecutive infection with Coxiella burnetii and tickborne diseases. Clin. Infect. Dis. 2005, 40:82-88.
40. Loukaides F., et al. Active surveillance of Q fever in human and animal population of Cyprus. BMC Infect. Dis. 2006, 6:48.
41. Astobiza I., et al. Molecular investigation of the occurrence of Coxiella burnetii in wildlife and ticks in an endemic area. Vet. Microbiol. 2011, 147:190-194.
42. Cooper A., et al. Detection of Coxiella burnetii DNA in wildlife and ticks in Northern Queensland, Australia. Vector Borne Zoonotic Dis. 2013, 13:12-16.
43. Russell-Lodrigue K.E., et al. Coxiella burnetii isolates cause genogroup-specific virulence in mouse and guinea pig models of acute Q fever. Infect. Immun. 2009, 77:5640-5650.
44. Kocianova E., et al. Comparison of virulence of Coxiella burnetii isolates from bovine milk and from ticks. Folia Parasitol. (Praha) 2001, 48:235-239.
45. Skerman V.B.D., et al. Approved lists of bacterial names. Int. J. Syst. Bacteriol. 1980, 30:225-420.
46. Tan C.K., Owens L. Infectivity, transmission and 16S rRNA sequencing of a rickettsia, Coxiella cheraxi sp nov. from the freshwater crayfish Cherax quadricarinatus. Dis. Aquat. Organ. 2000, 41:115-122.
47. Noda H., et al. Endosymbionts of ticks and their relationship to Wolbachia spp. and tick-borne pathogens of humans and animals. Appl. Environ. Microbiol. 1997, 63:3926-3932.
48. Zhong J. Coxiella-like endosymbionts. Coxiella burnetii: Recent Advances and New Perspectives in Research of the Q Fever Bacterium 2012, 365-379. Springer. R. Toman (Ed.).
49. Duron O., et al. The recent evolution of a maternally-inherited endosymbiont of ticks led to the emergence of the Q fever pathogen, Coxiella burnetii. PLoS Pathog. 2015, 11:e1004892.
50. Shivaprasad H.L., et al. Coxiella-like infection in psittacines and a toucan. Avian Dis. 2008, 52:426-432.
51. Vapniarsky N., et al. Systemic Coxiella-like infection With myocarditis and hepatitis in an eclectus parrot (Eclectus roratus). Vet. Pathol. 2012, 49:717-722.
52. Woc-Colburn A.M., et al. Fatal coxiellosis in swainson's blue mountain rainbow lorikeets (Trichoglossus haematodus moluccanus). Vet. Pathol. 2008, 45:247-254.
53. Almeida A.P., et al. Coxiella symbiont in the tick Ornithodoros rostratus (Acari: Argasidae). Ticks Tick Borne Dis. 2012, 3:203-206.
54. Machado-Ferreira E., et al. Coxiella symbionts in the Cayenne tick Amblyomma cajennense. Microb. Ecol. 2011, 62:134-142.
55. Klyachko O., et al. Localization and visualization of a Coxiella-type symbiont within the lone star tick, Amblyomma americanum. Appl. Environ. Microbiol. 2007, 73:6584-6594.
56. Smith T.A., et al. A Coxiella-like endosymbiont is a potential vitamin source for the lone star Ttck. Genome Biol. Evol. 2015, 7:831-838.
57. Zhong J.M., et al. Antibiotic treatment of the tick vector Amblyomma americanum reduced reproductive fitness. PLoS ONE 2007, 2:7.
58. Parker R.R., Kohls G.M. American Q fever: the occurrence of Rickettsia diaporica in Amblyomma americanum in eastern Texas. Public Health Rep. 1943, 58:1510-1511.
59. Philip C.B., White J.S. Disease agents recovered incidental to a tick survey of the Mississippi Gulf coast. J. Econ. Entomol. 1955, 48:396-400.
60. Jasinskas A., et al. Highly prevalent Coxiella sp. bacterium in the tick vector Amblyomma americanum. Appl. Environ. Microbiol. 2007, 73:334-336.
61. Clay K., et al. Microbial communities and interactions in the lone star tick, Amblyomma americanum. Mol. Ecol. 2008, 17:4371-4381.
62. Williams-Newkirk A.J., et al. Characterization of the bacterial communities of life stages of free living lone star ticks (Amblyomma americanum). PLoS ONE 2014, 9:e102130.
63. Qiu Y., et al. Microbial population analysis of the salivary glands of ticks; a possible strategy for the surveillance of bacterial pathogens. PLoS ONE 2014, 9:e103961.
64. Andreotti R., et al. Assessment of bacterial diversity in the cattle tick Rhipicephalus (Boophilus) microplus through tag-encoded pyrosequencing. BMC Microbiol. 2011, 11:6.
65. Lee J.H., et al. Identification of the Coxiella sp. detected from Haemaphysalis longicornis ticks in Korea. Microbiol. Immunol. 2004, 48:125-130.
66. Tozer S.J., et al. Potential animal and environmental sources of Q fever infection for humans in Queensland. Zoonoses Public Health 2014, 61:105-112.
67. Vilcins I.M., et al. Molecular detection of Rickettsia, Coxiella and Rickettsiella DNA in three native Australian tick species. Exp. Appl. Acarol. 2009, 49:229-242.
68. Reeves W.K., et al. Molecular and biological characterization of a novel Coxiella-like agent from Carios capensis. Ann. N. Y. Acad. Sci. 2005, 1063:343-345.
69. Reeves W.K., et al. Borrelia, Coxiella, and Rickettsia in Carios capensis (Acari: Argasidae) from a brown pelican (Pelecanus occidentalis) rookery in South Carolina, USA. Exp. Appl. Acarol. 2006, 39:321-329.
70. Reeves W.K. Molecular evidence for a novel Coxiella from Argas monolakensis (Acari: Argasidae) from Mono Lake, California, USA. Exp. Appl. Acarol. 2008, 44:57-60.
71. Sidi-Boumedine K., Rousset E. Épidémiologie moléculaire de la fièvre Q: une revue des méthodes de génotypage de Coxiella burnetii et des principales réalisations. Les cahiers de la Référence (ANSES) 2011, 5:30-38.
72. Glazunova O., et al. Coxiella burnetii genotyping. Emerg. Infect. Dis. 2005, 11:1211-1217.
73. Arricau-Bouvery N., et al. Molecular characterization of Coxiella burnetii isolates by infrequent restriction site-PCR and MLVA typing. BMC Microbiol. 2006, 6:38.
74. Svraka S., et al. Establishment of a genotyping scheme for Coxiella burnetii. FEMS Microbiol. Lett. 2006, 254:268-274.
75. Huijsmans C.J.J., et al. Single-nucleotide polymorphism genotyping of Coxiella burnetii during a Q fever outbreak in The Netherlands. Appl. Environ. Microbiol. 2011, 77:2051-2057.
76. Parola P., Raoult D. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin. Infect. Dis. 2001, 32:897-928.
77. Mariconti M., et al. Humans parasitized by the hard tick Ixodes ricinus are seropositive to Midichloria mitochondrii: is Midichloria a novel pathogen, or just a marker of tick bite?. Pathog. Glob. Health 2012, 106:391-396.
78. Hamilton P.T., Perlman S.J. Host defense via symbiosis in Drosophila. PLoS Pathog. 2013, 9:e1003808.
79. Brownlie J.C., Johnson K.N. Symbiont-mediated protection in insect hosts. Trends Microbiol. 2009, 17:348-354.
80. Oliver K.M., et al. Facultative symbionts in aphids and the horizontal transfer of ecologically important traits. Annu. Rev. Entomol. 2010, 55:247-266.
81. LePage D., Bordenstein S.R. Wolbachia: can we save lives with a great pandemic?. Trends Parasitol. 2013, 29:385-393.
82. Moreira L.A., et al. A Wolbachia symbiont in Aedes aegypti limits infection with Dengue, Chikungunya, and Plasmodium. Cell 2009, 139:1268-1278.
83. Ahantarig A., et al. Hard ticks and their bacterial endosymbionts (or would be pathogens). Folia Microbiol. (Praha) 2013, 58:419-428.
84. Sjodin A., et al. Genome characterisation of the genus Francisella reveals insight into similar evolutionary paths in pathogens of mammals and fish. BMC Genomics 2012, 13:268.
85. Michelet L., et al. Discriminating Francisella tularensis and Francisella-like endosymbionts in Dermacentor reticulatus ticks: evaluation of current molecular techniques. Vet. Microbiol. 2013, 163:399-403.
86. Baldo L., Werren J.H. Revisiting Wolbachia supergroup typing based on WSP: spurious lineages and discordance with MLST. Curr. Microbiol. 2007, 55:81-87.
87. Duron O. Lateral transfers of insertion sequences between Wolbachia, Cardinium and Rickettsia bacterial endosymbionts. Heredity 2013, 111:330-337.
88. Nikoh N., et al. Evolutionary origin of insect-Wolbachia nutritional mutualism. Proc. Natl. Acad. Sci. U.S.A. 2014, 111:10257-10262.
89. ECDC ECDC Technical Report: Risk Assessment on Q Fever 2010, European Centre for Disease Prevention and Control.
90. Roest H.I.J., et al. Clinical microbiology of Coxiella burnetii and relevant aspects for the diagnosis and control of the zoonotic disease Q fever. Vet. Q. 2013, 33:148-160.
91. Kersh G.J., et al. Presence and persistence of Coxiella burnetii in the environments of goat farms associated with a Q fever outbreak. Appl. Environ. Microbiol. 2013, 79:1697-1703.
92. Derrick E.H., et al. Studies in the epidemiology of Q fever. 9. The role of the cow in the transmission of human infection. Aust. J. Exp. Biol. Med. Sci. 1942, 20:105-110.
93. Davis G.E., Cox H.R. A filter-passing infectious agent isolated from ticks. I. Isolation from Dermacentor andersoni, reactions in animals, and filtration experiments. Public Health Rep. 1938, 53:2259-2267.
94. Smith D.J.W. Studies in the epidemiology of Q fever. 11. Experimental infection of the ticks Haemaphysalis bispinosa and Ornithodoros sp. with Rickettsia burneti. Aust. J. Exp. Biol. Med. Sci. 1942, 20:295-296.
95. Siroky P., et al. Tortoise tick Hyalomma aegyptium as long term carrier of Q fever agent Coxiella burnetii-evidence from experimental infection. Parasitol. Res. 2010, 107:1515-1520.
96. Daiter A.B. Transovarial and transspermal transmission of Coxiella burnetii by the tick Hyalomma asiaticum and its role in Q-rickettsiosis ecology. Parazitologiya 1977, 11:403-411.
97. Smith D.J.W. Studies in the epidemiology of Q fever. 10. The transmission of Q fever by the tick Ixodes holocyclus (with notes on tick-paralysis in bandicoots). Aust. J. Exp. Biol. Med. Sci. 1942, 20:213-217.
98. Smith D.J.W. Studies in the epidemiology of Q fever. 8. The transmission of Q fever by the tick Rhipicephalus sanguineus. Aust. J. Exp. Biol. Med. Sci. 1941, 19:133-136.
99. Mantovani A., Benazzi P. The isolation of Coxiella burnetii from Rhipicephalus sanguineus on naturally infected dogs. J. Am. Vet. Med. Assoc. 1953, 122:117-118.
100. Pautov V.N., Morozov Y.N. Study of Rickettsia burnetii reactivation in argasid ticks Alveonasus canestrinii. Zh. Mikrobiol. 1974, 51:29-32.
101. Pautov V.N., Morozov Y.N. Use of argasid ticks in studying apathogenic Rickettsia burneti. Med. Parazit. 1974, 43:176-179.
102. Daiter A.B. Susceptibility of Ornithodoros papillipes ticks (Argasidae) to Coxiella burneti rickettsiae. Parazitologiya 1984, 18:128-134.
103. Davis G.E. Rickettsia diaporica: its persistence in the tissues of Ornithodoros turicata. Public Health Rep. 1943, 55:1862-1864.
104. Smith D.J.W. Studies in the epidemiology of Q fever. 4. The failure to transmit Q fever with the cat-flea Ctenocephalides felis. Aust. J. Exp. Biol. Med. Sci. 1940, 18:119.
105. Heise S.R., et al. Bacterial diversity in Amblyomma americanum (Acari: Ixodidae) with a focus on members of the genus Rickettsia. J. Med. Entomol. 2010, 47:258-268.
106. Rounds M.A., et al. Identification of endosymbionts in ticks by broad-range polymerase chain reaction and electrospray ionization mass spectrometry. J. Med. Entomol. 2012, 49:843-850.
107. Wilkinson D.A., et al. Massive infection of seabird ticks with bacterial species related to Coxiella burnetii. Appl. Environ. Microbiol. 2014, 80:3327-3333.
108. Liu L.M., et al. Coinfection of Dermacentor silvarum Olenev (Acari: Ixodidae) by Coxiella-like, Arsenophonus-like, and Rickettsia-like symbionts. Appl. Environ. Microbiol. 2013, 79:2450-2454.
109. Arthan W., et al. Detection of Coxiella-like endosymbiont in Haemaphysalis tick in Thailand. Ticks Tick Borne Dis. 2015, 6:63-68.
110. Mediannikov O. Molecular evidence of Coxiella-like microorganism harbored by Haemaphysalis concinnae ticks in the Russian far east. Rickettsiology: Present and Future Directions 2003, 226-228. New York Academy of Sciences. K.E. Hechemy (Ed.).
111. Reeves W.K., et al. Rickettsial diseases and ectoparasites from military bases in Japan. J. Parasitol. 2015, 101:150-155.
112. Ahantarig A., et al. Detection of Rickettsia and a novel Haemaphysalis shimoga symbiont bacterium in ticks in Thailand. Curr. Microbiol. 2011, 62:1496-1502.
113. Schabereiter-Gurtner C., et al. Application of broad-range 16S rRNA PCR amplification and DGGE fingerprinting for detection of tick-infecting bacteria. J. Microbiol. Methods 2003, 52:251-260.
114. Bernasconi M.V., et al. Rhipicephalus ticks infected with Rickettsia and Coxiella in Southern Switzerland (Canton Ticino). Infect. Genet. Evol. 2002, 2:111-120.
115. Lalzar I., et al. Composition and seasonal variation of Rhipicephalus turanicus and Rhipicephalus sanguineus bacterial communities. Appl. Environ. Microbiol. 2012, 78:4110-4116.
116. Lalzar I., et al. Tissue tropism and vertical transmission of Coxiella in Rhipicephalus sanguineus and Rhipicephalus turanicus ticks. Environ. Microbiol. 2014, 16:3657-3668.
117. Duron O., et al. Diversity and global distribution of the Coxiella intracellular bacterium in seabird ticks. Ticks Tick Borne Dis. 2014, 5:557-563.
118. Moran N.A., et al. Genomics and evolution of heritable bacterial symbionts. Annu. Rev. Genet. 2008, 42:165-190.
119. Wernegreen J.J. Endosymbiosis. Curr. Biol. 2012, 22:R555-R561.
120. Ferrari J., Vavre F. Bacterial symbionts in insects or the story of communities affecting communities. Philos. Trans. R. Soc. Lond. B: Biol. Sci. 2011, 366:1389-1400.
121. Duron O., et al. The diversity of reproductive parasites among arthropods: Wolbachia do not walk alone. BMC Biol. 2008, 6:27.
122. Engelstadter J., Hurst G.D.D. The ecology and evolution of microbes that manipulate host reproduction. Annu. Rev. Ecol. Evol. Syst. 2009, 40:127-149.
123. Duron O., Hurst G.D. Arthropods and inherited bacteria: from counting the symbionts to understanding how symbionts count. BMC Biol. 2013, 11:45.