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Detection of Heartworm Antigen Without Cross-Reactivity to Helminths

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Detection of Heartworm Antigen Without Cross-Reactivity to Helminths Gruntmeir et al. Parasites Vectors (2021) 14:71 https://doi.org/10.1186/s13071-020-04573-6 Parasites & Vectors SHORT REPORT Open Access Detection of heartworm antigen without cross-reactivity to helminths and protozoa following heat treatment of canine serum Jef M. Gruntmeir1, Nina M. Thompson1, Maureen T. Long1, Byron L. Blagburn2 and Heather D. S. Walden1* Abstract Background: Detection of Diroflaria immitis, or heartworm, through antigen in sera is the primary means of diag- nosing infections in dogs. In recent years, the practice of heat-treating serum prior to antigen testing has demon- strated improved detection of heartworm infection. While the practice of heat-treating serum has resulted in earlier detection and improved sensitivity for heartworm infections, it has been suggested that heat treatment may cause cross reactivity with A. reconditum and intestinal helminth infections of dogs. No studies have assessed the potential cross-reactivity of these parasites with heartworm tests before and after heat treatment using blood products and an appropriate gold standard reference. Methods: Canine sera (n 163) was used to evaluate a heartworm antigen-ELISA (DiroCHEK®) and potential cross- reactivity with common parasitic= infections. The heartworm status and additional parasite infections were confrmed by necropsy and adult helminth species verifed morphologically or by PCR, and feces evaluated by centrifugal fecal fotation. Results: Intestinal parasites were confrmed in 140 of the dogs by necropsy, and 130 by fecal fotation. Acan- thocheilonema reconditum microflariae were confrmed in 22 dogs. Prevalence of heartworm infection confrmed by necropsy was 35.6% (58/163). In the 105 dogs without heartworms, specifcity remained unchanged at 100% both before and after heat treatment despite confrmed infections with A. reconditum, Ancylostoma caninum, Ancylostoma brasiliense, Trichuris vulpis, Toxocara canis, Dipylidium caninum, Spirometra mansonoides, Macracanthorynchus ingens, Cystoisospora sp., Giardia sp., and Sarcocystis sp. Conclusions: These fndings suggest that the use of heat treatment improves sensitivity of heartworm tests and is unlikely to cause false positive antigen results due to Acanthocheilonema reconditum, intestinal helminths, and proto- zoal parasites in dogs. Keywords: Diroflaria immitis, Acanthocheilonema reconditum, Heat treatment, Intestinal parasites, Microflariae, Cross reactivity, Antigen Background *Correspondence: [email protected] Te use of antigen testing to aid in the diagnosis of canine 1 Department of Comparative, Diagnostic and Population Medicine, heartworm infections has been a vital tool for veterinar- University of Florida College of Veterinary Medicine, 1945 SW 16th ians since 1985. Commercialized antigen tests, primarily Avenue, Gainesville, FL 32610, USA Full list of author information is available at the end of the article based on monoclonal antibodies generated from adult © The Author(s) 2021. This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creat iveco mmons .org/licen ses/by/4.0/. The Creative Commons Public Domain Dedication waiver (http://creat iveco mmons .org/publi cdoma in/ zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data. Gruntmeir et al. Parasites Vectors (2021) 14:71 Page 2 of 8 heartworm antigen preparations following acid and heat soakings of intestinal helminths, to assess cross-reactiv- purifcation [1], or other identifed non-cross-reactive ity with heartworm tests, are potentially misleading [23]. antigens [2], demonstrated high specifcity [3–5]. Te Currently no published studies suggesting cross reactiv- relative high specifcity of commercial Diroflaria immitis ity of A. reconditum or intestinal helminths with heart- antigen tests is in contrast to the cross-reactive nature of worm antigen tests, with or without heat ICD of naturally antibody tests historically used for D. immitis [6, 7] and sourced canine serum, have ruled out occult D. immitis more recently described as a diagnostic approach exam- infection by necropsy. ining human exposure to Diroflaria sp. [8, 9] and poten- In this study, using sera from 163 dogs, 100 of which tial application for D. repens infected dogs [10]. were previously characterized based on heartworm com- Prior to 1995, manufacturer protocols for many com- position (adults and microflariae) and antigen results mercial heartworm antigen tests used chemical and/or with and without heat ICD [28], we assessed heartworm low heat (60–70Cº) immune complex dissociation (ICD) antigen detection in relation to potential cross-reactivity steps. However recently heat ICD treatment of serum with A. reconditum, intestinal helminths and protozoan at an elevated temperature of 104 Cº has been shown to infections using a commercially available heartworm allow earlier detection and improved sensitivity for D. antigen test. immitis antigen [3]. No decrease in specifcity has been observed in pathogen free dogs when using this elevated heating step or an acid ICD prior to antigen testing [3, Methods 11]. Heat ICD is also unlikely to cause false positive From 2017 to 2020, 163 previously euthanized dogs were results on heartworm tests in dogs infected by O. lupi collected and necropsied at the University of Florida Col- [13]. lege of Veterinary Medicine. All dogs collected during Studies evaluating commercial antigen test specifc- this time period were included in this study. Te abdomi- ity have used blood products from dogs experimentally nal and thoracic cavities were thoroughly inspected for or naturally infected with Acanthocheilonema recondi- parasites prior to and following removal of the heart, tum, Diroflaria repens, Onchocerca lupi, Toxocara lungs, caudal esophagus, thoracic aorta, and gastro- canis, Ancylostoma caninum, Ancylostoma brasiliense, intestinal (GI) tract. Te entire GI tract was opened Uncinaria stenocephala, Trichuris vulpis, Dipylidium and mucosa scraped and rinsed into a 355 µm sieve for caninum, Strongyloides stercoralis, Spirocerca lupi and parasite recovery. Helminths were rinsed in phosphate Angiostrongylus vasorum [1, 4, 6, 12–19, 21]. In most bufered saline (PBS) and stored in 70% ethanol. Feces instances, no cross reactivity with antigen tests was removed from the colon was examined by centrifugal observed using serum from dogs both with or without fotation using Sheather’s sugar (SG 1.26), and when the historical ICD steps [1, 4, 6, 12–16, 19], however two necessary, by acid fast staining (i.e. Cryptosporidium commercially available tests were shown to cross-react verifcation) [29]. Antigen testing was completed using with A. vasorum [17], and three demonstrated cross- the DiroCHEK® assay (Zoetis LLC, Parsippany, NJ) reactivity with S. lupi [18]. In a rare case, an exceptionally both before and after heat ICD of serum [3]. Heat ICD high infection intensity by Acanthocheilonema dracuncu- was performed with a reduced starting serum volume of loides, induced a false antigen positive result using nor- 400 µl [28]. mal manufacturer protocols [20]. Diroflaria repens has Whole blood from all dogs was examined for micro- recently been confrmed to cross-react with 3 heartworm flariae by direct smear and Modifed Knott’s technique tests following heat ICD in a small number of experimen- (MKT). Microflariae recovered from whole blood by tally infected n=3 dogs [21]. Although some but not all MKT were identifed morphometrically [3, 29, 30]. cases of naturally infected, patent D. repens infections, Microflariae from whole blood samples were processed have positive antigen results post-heat ICD [22]. for DNA extraction (DNeasy Blood and Tissue kit, Qia- Several recent publications have added confusion to gen) [31], modifed by using elution bufer heated to the literature by stating Acanthocheilonema recondi- 70 °C. Microflariae species were confrmed by con- tum causes false positives with heartworm tests [23–27] ventional PCR, specifc for D. immitis (12S rDNA) and misciting a study using a non-commercialized ELISA D. repens (12S rDNA), using single-plex reactions to based antibody test [7], or based on interpretation of increase sensitivity [32]. Specifc PCR for A. recondi- study results using an inappropriate gold standard refer- tum (cox1) was performed as described [31] modifed ence (PCR results) [26], which can neither verify nor rule by using 54 °C as the optimal annealing temperature. A out an occult (amicroflaremic) D. immitis infection or Filariid-generic PCR assay targeting cox1 and 12S rDNA D. repens infection. Additionally, conclusions of studies genes were also used for mono-infections [31]. using non-biologically relevant samples, such as saline Gruntmeir et al. Parasites Vectors (2021) 14:71 Page 3 of 8 Te prevalence (PR),
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