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No Evidence for Widespread Babesia Microti Transmission in Australia

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No Evidence for Widespread Babesia Microti Transmission in Australia Faddy Helen (Orcid ID: 0000-0002-3446-8248) Viennet Elvina (Orcid ID: 0000-0002-1418-1426) No evidence for widespread Babesia microti transmission in Australia Helen M Faddy1,2, Kelly M Rooks1, Peter J Irwin3, Elvina Viennet1, Andrea Paparini3, Clive R Seed4, Susan L Stramer5, Robert J Harley6, Hiu-Tat Chan7, Peta M Dennington8, Robert LP Flower1 1Research and Development, Australian Red Cross Blood Service, Brisbane, Queensland, Australia 2School of Biomedical Sciences, University of Queensland, Brisbane, Queensland, Australia 3Murdoch University, Perth, Western Australia, Australia 4Clinical Services and Research, Australian Red Cross Blood Service, Perth, Western Australia, Australia 5American Red Cross Scientific Affairs, Gaithersburg, Maryland, USA 6Clinical Services and Research, Australian Red Cross Blood Service, Brisbane, Queensland, Australia 7Clinical Services and Research, Australian Red Cross Blood Service, Melbourne, Victoria, Australia 8Clinical Services and Research, Australian Red Cross Blood Service, Sydney, New South Wales, Australia Corresponding author: Helen Faddy; 44 Musk Avenue, Kelvin Grove, Queensland, Australia, 4059; TEL: +617 3838 9262 FAX: +617 3838 9428; [email protected] Source of support: Australian governments fund the Australian Red Cross Blood Service to provide blood, blood products and services to the Australian community. Conflict of interest: All authors report no conflicts of interest. This is the author manuscript accepted for publication and has undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process, which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1111/trf.15336 This article is protected by copyright. All rights reserved. Running title: Babesia microti prevalence in Australia Word count (excluding abstract, references and illustrations): 3668 This article is protected by copyright. All rights reserved. Abstract BACKGROUND: A fatal case of autochthonous Babesia microti infection was reported in Australia in 2012. This has implications for Australian public health, and, given babesiosis is transfusion- transmissible, has possible implications for Australian blood transfusion recipients. We investigated the seroprevalence of antibodies to B. microti in Australian blood donors and in patients with clinically- suspected babesiosis. STUDY DESIGN AND METHODS: Plasma samples (n = 7,000) from donors donating in at risk areas and clinical specimens from patients with clinically-suspected babesiosis (n = 29) were tested for B. microti IgG by immunofluorescence assay (IFA). IFA initially reactive samples were tested for B. microti IgG and IgM by immunoblot and B. microti DNA by PCR. RESULTS: Although five donors were initially reactive for B. microti IgG by IFA, none was confirmed for B. microti IgG (zero estimate; 95% CI: 0–0.05%) and all were negative for B. microti DNA. None of the patient samples had B. microti IgG, IgM or DNA. CONCLUSIONS: This study does not provide evidence for widespread exposure to B. microti in Australian blood donors at local theoretical risk, nor does it provide evidence of B. microti infection in Australian patients with clinically-suspected babesiosis. Given that confirmed evidence of previous exposure to B. microti was not seen, these data suggest transmission of this pathogen is currently uncommon in Australia, and unlikely to pose a risk to transfusion safety at present. Key words: babesiosis, Babesia microti, transmission, Australia, transfusion, safety This article is protected by copyright. All rights reserved. INTRODUCTION Babesiosis is an emerging tick-borne zoonotic infectious disease.1-4 The first human case of autochthonous babesiosis in Australia, a fatality associated with Babesia microti infection, was reported in 2012.5 This case was a 56 year old male with no history of transfusion, intravenous drug use or travel to countries endemic for babesiosis. 5 The infection was therefore believed to have been from a tick bite.5 This has implications for Australian public health and blood transfusion safety, as transfusion-transmitted (TT) babesiosis has been documented.6 Furthermore, this finding prompted questions in relation to the scale of autochthonous babesiosis in Australia. Babesiosis presents as a blood-borne haemolytic disease caused by intracellular tick-borne protozoan parasites of the genus Babesia. Over 100 Babesia spp. have been identified worldwide, with a subset being pathogenic in humans. Infection in humans can be low-grade and persistent; however, can be more severe in the immunosuppressed, asplenic, and elderly. Human babesiosis occurs sporadically in Europe, Asia, Africa and the Americas, with endemic transmission in the northeastern and upper midwestern regions of the USA. In the USA, the rodent species B. microti is the most common species associated with human disease,6 as well as being the species implicated in the only autochthonous Australian case to date.5 In Europe, the majority of cases in humans are due to the cattle species B. divergens.4 Other species of Babesia can infect animals; indeed babesiosis is well known as an introduced disease in Australian cattle and dogs, and as an endemic infection in native mammals.7-10 The life cycle of B. microti involves a reservoir vertebrate host and a vector tick. Transmission to humans and other mammalian hosts is usually through the bite of an infected ixodid tick.6 A myriad of Ixodes ticks reside in Australia, the most common and perhaps medically relevant being Ixodes holocyclus, which can be found along the east coast.11,12 Ixodes holocyclus has been implicated in tick paralysis and transmission of rickettsial infections.13-15 To date, no Australian ticks have been shown to transmit B.microti. This article is protected by copyright. All rights reserved. The report of locally acquired babesiosis in Australia5 heightened public and governmental concern in relation to this disease. Thus, the risks posed by this parasite to Australian blood transfusion safety and public health needed to be assessed. This study investigated the prevalence of B. microti in blood donors residing in areas with theoretical risk, based on proximity to where the Australian case resided and also within the distribution range of I. holocyclus, the most common and perhaps medically relevant tick within Australia and in a cohort of Australian patients with clinically-suspected babesiosis. Although other species of Babesia are capable of causing disease in humans, we focused on B. microti as this organism was responsible for the majority of historical TT cases (159/162 cases between 1979-2009 in the USA),16 and was the cause of the only known case of autochthonous babesiosis in Australia,5 the identification of which was the impetus for this study. MATERIALS AND METHODS Blood donor samples This was a de-linked cross-sectional study of Australian blood donors aged 16 to 80 years inclusive, donating in areas considered ‘at-theoretical risk’ for potential exposure to B. microti. To the best of our knowledge there has been no previous investigation of seroprevalence of antibodies to Babesia spp. in Australia, therefore sample size calculations were based on overseas estimates available when the study was designed. Although not ideal, as such estimates are from areas endemic for babesiosis and were based on unconfirmed results, they were used to provide some insight into an approximate required sample size. Assuming a similar seroprevalence to that recorded for B. microti in endemic regions of the USA (1.1%),17 testing ~7,000 samples would give a 95% confidence interval (CI) that was considered acceptable and fundable. ‘At-theoretical risk’ regions were defined as those in the North/South Coast of New South Wales (NSW; region where the Australian case resided and also within the distribution range of I. holocyclus) or in coastal Queensland (QLD; also areas enzootic for I. holocyclus).5,18 Samples were collected between 29 December 2012 and 26 September 2013 from donors residing in the following areas and their surrounds: Cairns (n = 162), Townsville (n = 498), Mackay (n = 261), Rockhampton (n = 586), Gladstone (n = 244), Fraser Coast (n = 503), Sunshine This article is protected by copyright. All rights reserved. Coast (n = 522), Toowoomba (n = 257), and Ipswich (n = 458) in QLD (n = 3,491 total); as well as Lismore (n = 323), Coffs Harbour (n = 118), Port Macquarie (n = 232), Newcastle (n = 577), Gosford (n = 310), Wollongong (n = 827), Camden (n = 383), Bateman’s Bay (n = 480) and Bega (n = 259) in NSW (n = 3,509 total). Where possible, samples were collected from mobile collection facilities in the above areas; for many centres/mobile sites, particularly those with small collection numbers, these samples represented all available donors/samples during the study period. Samples were collected into 6 mL dipotassium ethylenediaminetetraacetic acid (K2EDTA) sample preparation tubes (Becton Dickinson) and centrifuged (1,000 g, 10 min) within 72 h of collection. Samples were sourced from those remaining after routine infectious disease testing was complete and where adequate volume remained. Plasma was aliquoted and stored at -30 ºC. Demographic information (age, sex, postcode, residence state and a basic travel history) was obtained for each sample prior to de-identification. Ethical approval was obtained from the Australian Red Cross Blood Service (Blood Service) Human Research
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