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Table of Contents
SHORT RESEARCH COMMUNICATION
Year : 2018  |  Volume : 55  |  Issue : 3  |  Page : 239-241

Attempt to uncover reservoirs of human spotted fever rickettsiosis on the Fleurieu Peninsula, South Australia


1 School of Animal and Veterinary Sciences, University of Adelaide, Adelaide, Australia
2 Faculty of Veterinary and Agricultural Sciences, University of Melbourne, Parkville, Australia
3 School of Biological Sciences, University of Adelaide, Adelaide, Australia

Date of Submission18-Feb-2018
Date of Acceptance16-May-2018
Date of Web Publication4-Jan-2019

Correspondence Address:
Patrick L Taggart
University of Adelaide, Veterinary Health Centre, Building E40, Mudla Wirra RD, Roseworthy, South Australia
Australia
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0972-9062.249483

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  Abstract 


Keywords: Bothriocroton hydrosauri; Ixodes hirsti; Rickettsia honei; South Australia; spotted fever; vector


How to cite this article:
Taggart PL, Traub R, Fui S, Weinstein P. Attempt to uncover reservoirs of human spotted fever rickettsiosis on the Fleurieu Peninsula, South Australia. J Vector Borne Dis 2018;55:239-41

How to cite this URL:
Taggart PL, Traub R, Fui S, Weinstein P. Attempt to uncover reservoirs of human spotted fever rickettsiosis on the Fleurieu Peninsula, South Australia. J Vector Borne Dis [serial online] 2018 [cited 2019 May 27];55:239-41. Available from: http://www.jvbd.org/text.asp?2018/55/3/239/249483



During the years 2001–2003, multiple outbreaks of human spotted fever group rickettsioses occurred on the south coast of South Australia[1],[2]. The causative agent of Flinders Island spotted fever, Rickettsia honei, identified in the reptile tick Bothriocroton hydrosauri[3], was implicated as the likely vector involved in these epidemics. Larvae, nymphs, and adults of B. hydrosauri infest reptiles almost exclusively[4]. Very few reports exist documenting B. hydrosauri as an ectoparasite of mammals; in one report it was reported to parasitise a human[5] and in another it was reported parasitising an ox[4].

Whilst the transmission of R. honei from B. hydrosauri to humans is possible through accidental parasitism of humans, multiple rickettsioses outbreaks transmitted by B. hydrosauri is unexpected based on current knowledge of its host range. With this in mind, the question arises, if R. honei could have reservoirs other than B. hydrosauri, as has been suggested by Unsworth et al[2]. One potential reservoir and vector of R. honei could be the three-host tick Ixodes hirsti. Larvae and nymphs of I. hirsti parasitise birds in the same area where the documented human rickettsioses outbreaks occurred, with the adult life stages parasitising mammals. Whilst there are no documented reports of I. hirsti parasitising humans, it is expected that they are within its mammalian host range. Further, Rickettsiales spp have been identified in I. hirsti through the amplification and sequencing of the V4 region of the 16S rRNA gene, but are too short and conserved to allow differentiation of genera (unpublished data), and Ixodes ticks are documented vectors of human spotted fever group rickettsiosis within the Oceania region[6]. This study aimed to determine, if I. hirsti is a potential reservoir of human spotted fever group rickettsiosis on the south coast of South Australia, by amplifying the citrate synthase (gltA) gene of spotted fever and typhus group Rickettsia spp[7] in I. hirsti ticks.

Ticks were collected from 40 birds, mist-netted within the following South Australian conservation parks on the Fleurieu Peninsula: Newland Head (–35° 37′ 46.7394″; 138° 30′ 12.7758″); Cox Scrub (–35° 20′ 3.12″; 138° 43′ 59.8476″); Deep Creek (–35° 37′ 0.0114″; 138° 15′ 24.876″); Flinders Chase (–35° 57′ 6.192″; 136° 44′ 10.1868″); Vivonne Bay (–35° 57′ 6.192″; 136° 44′ 10.1868″); and Pelican Lagoon (–35° 48′ 16.7574″; 137° 46′ 46.6638″) [Figure 1]. All ticks were preserved in 90% ethanol.
Figure 1: (a) Location of the Fleurieu Peninsula (box) in South Australia; and (b) Location of the conservation parks (black dots) where tick samples were collected within the study region. FC— Flinders Chase; VB—Vivonne Bay; PL—Pelican Lagoon; DC—Deep Creek; NH—Newland Head; and CS—Cox Scrub.

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DNA was extracted from crushed ticks using a DNeasy blood and Tissue kit (QIAGEN, Chadstone Centre, Victoria, Australia) following the manufacturer's instructions. A diagnostic TaqMan probe real-time PCR assay targeting the gltA gene of spotted fever and typhus group rickettsia was used for the detection of Rickettsia spp[7] with modifications according to Hii et al[8]. Reactions were performed in duplicate in a total volume of 10 μl containing KAPA Probe Fast qPCR mastermix (KAPA Biosystems, Wilmington, Massachusetts, United States), 400 nM of each forward and reverse primer, 200 nM of probe and 2 μl of extracted DNA. For each run, a negative control of sterile PCR-grade water and a positive control of cultured R. honei was included in the real-time PCR assay. The reactions were run, detected and analysed on a Rotor-Gene 6.1.8.1. (QIAGEN, Chadstone Centre, Victoria, Australia).

DNA from 40 Rickettsiales-positive I. hirsti ticks were screened for spotted fever and typhus group rickettsiae by the real-time PCR. No samples returned a positive for Rickettsia spp (both spotted fever and typhus group). The specific real-time PCR is capable of amplifying all spotted fever and typhus group riskettsiae, except the ancestral group rickettsia, R. bellii, and all other members of the order Rickettsiales[7]. It is, therefore, suggested that the Rickettsiales originally detected in the microbiome study of I. hirsti in Australia are likely to be a common endosymbiont of Ixodes spp, such as Candidatus midichloria mitochondrii (CMM), and not Rickettsia spp, due to the CMM's ubiquitous nature in Ixodid ticks[9].

The vector of human rickettsiosis outbreaks on the Fleurieu Peninsula, South Australia must be assumed to be B. hydrosauri until proven otherwise. However, a recent survey of B. hydrosauri collected from the lizard Tiliqua rugosa in close proximity to the Fleurieu Peninsula, failed to detect R. honei[10]. Instead, 100% of the ticks harboured an uncharacterised Rickettsia sp[10]. The ability of B. hydrosauri to potentially harbour R. honei at a high prevalence, as it does for other Rickettsia spp, increases its probability of transmission to humans, despite infrequent report of it parasitising mammalian hosts[4],[11]. Surprisingly, R. honei was neither detected by PCR nor by cell culture in the blood of three reptile species (T. nigrolutea, Austrelaps sepurbus and Notechis scutatus)[12].

Rickettsia honei has been isolated from a range of tick genera in addition to Bothriocroton, including Haemaphyalis from humans[13], Ixodes from black rats (Rattus rattus)[14] and Amblyomma from cattle[12]. Hence, potential candidate vectors of human rickettsiosis infection on the Fleurieu Peninsula/south coast of South Australia may include other ticks associated with the parasitisation of mammals. It is important to identify such potential vectors of human rickettsiosis for effective management and proper understanding of the disease risk. Further investigation is required to identify tick species commonly parasitising mammals in the study area to ascertain their ability in harbouring and transmitting spotted fever and typhus group Rickettsiae.

Ethical issues/Conflict of interest

The authors declare no conflict of interest or ethical issues.



 
  References Top

1.
Dyer JR, Einsiedel L, Ferguson PE, Lee AS, Unsworth NB, Graves SR, et al. A new focus of Rickettsia honei spotted fever in South Australia. Med J Aust 2005; 182(5): 231–4.  Back to cited text no. 1
    
2.
Unsworth NB, Stenos J, McGregor AR, Dyer JR, Graves SR. Not only ‘Flinders Island’ spotted fever. Pathology 2005; 37(3): 242–5.  Back to cited text no. 2
    
3.
Stenos J, Graves S, Popov VL, Walker DH. Aponomma hydrosauri, the reptile-associated tick reservoir of Rickettsia honei on Flinders Island, Australia. Am J Trop Med Hyg 2003; 69(3): 314–7.  Back to cited text no. 3
    
4.
Roberts FHS. Australian ticks. Melbourne: The Commonwealth Scientific and Industrial Research Organization 1970; p. 267.  Back to cited text no. 4
    
5.
Graves SR, Stewart L, Stenos J, Stewart RS, Schmidt E, Hudson S, et al. Spotted fever group rickettsial infection in south-eastern Australia: Isolation of rickettsiae. Comp Immunol Microbiol Infect Dis 1993; 16(3): 223–33.  Back to cited text no. 5
    
6.
Derne B, Weinstein P, Musso D, Lau C. Distribution of rickettsioses in Oceania: Past patterns and implications for the future. Acta Trop 2015; 143: 121–33.  Back to cited text no. 6
    
7.
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.  Back to cited text no. 7
    
8.
Hii S-F, Abdad MY, Kopp SR, Stenos J, Rees RL, Traub RJ. Seroprevalence and risk factors for Rickettsia felis exposure in dogs from southeast Queensland and the northern Territory, Australia. Parasit Vectors 2013; 6(1): 1.  Back to cited text no. 8
    
9.
Gofton AW, Oskam CL, Lo N, Beninati T, Wei H, McCarl V, et al. Inhibition of the endosymbiont “Candidatus midichloria mitochondrii” during 16S rRNA gene profiling reveals potential pathogens in Ixodes ticks from Australia. Parasit Vectors 2015; 8: 345.  Back to cited text no. 9
    
10.
Whiley H, Custance G, Graves S, Stenos J, Taylor M, Ross K, et al. Rickettsia detected in the reptile tick Bothriocroton hydrosauri from the lizard Tiliqua rugosa in South Australia. Pathogens 2016; 5(2): 41.  Back to cited text no. 10
    
11.
Smyth M. The distribution of three species of reptile ticks, Aponomma hydrosauri (Denny), Amblyomma albolimbatum Neumann, and Amb. limbatum Neumann. I: Distribution and hosts. Aust J Zool 1973; 21(1): 91–101.  Back to cited text no. 11
    
12.
Graves S, Stenos J. Rickettsia honei: A spotted fever group Rickettsia on three continents. Ann N Y Acad Sci 2003; 990: 62–6.  Back to cited text no. 12
    
13.
Unsworth NB, Stenos J, Graves SR, Faa AG, Cox GE, Dyer JR, et al. Flinders Island spotted fever rickettsioses caused by “marmionii” strain of Rickettsia honei, eastern Australia. Emerg Infect Dis 2007; 13: 566–73.  Back to cited text no. 13
    
14.
Kollars TM, Tippayachai B, Bodhidatta D. Short report: Thai tick typhus, Rickettsia honei, and a unique rickettsia detected in Ixodes granulatus (Ixodidae: Acari) from Thailand. Am J Trop Med Hyg 2001; 65: 535–7.  Back to cited text no. 14
    


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