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Impact of Heat Treatment on Dirofilaria Immitis Antigen Detection in Shelter Dogs Brian A

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Impact of Heat Treatment on Dirofilaria Immitis Antigen Detection in Shelter Dogs Brian A The Author(s) Parasites & Vectors 2017, 10(Suppl 2):483 DOI 10.1186/s13071-017-2443-7 RESEARCH Open Access Impact of heat treatment on Dirofilaria immitis antigen detection in shelter dogs Brian A. DiGangi1,10*, Carly Dworkin1, Jason W. Stull2, Jeanette O’Quin2, Morgan Elser2, Antoinette E. Marsh2, Lesli Groshong3, Wendy Wolfson4, Brandy Duhon4, Katie Broaddus5, Elise N. Gingrich6, Emily Swiniarski7,9 and Elizabeth A. Berliner8 From 15th American Heartworm Society Triennial Symposium New Orleans, LA, USA. September 11-13, 2016 Abstract Background: The diagnosis and management of canine heartworm disease is a growing concern for shelter veterinarians. Although the accuracy of commercial antigen test kits has been widely studied, recent reports have renewed interest in antigen blocking as a causative factor for false “no antigen detected” results. The objectives of this study were to determine the prevalence of false “no antigen detected” results in adult dogs entering shelters in northern, southern, and western regions of the country and to identify historical and clinical risk factors for such results. Methods: Serum samples were evaluated for Dirofilaria immitis antigen using a commercially available point-of-care ELISA; samples in which no antigen was detected underwent a heat treatment protocol and repeat antigen testing. Whole blood samples underwent Knott testing to identify the presence of microfilariae. Historical and clinical findings were analyzed using exact logistic regression. Results: A total of 616 samples were analyzed. Overall prevalence of positive antigen test results (prior to heat treatment) was 7.3% and frequency of false “no antigen detected” results due to antigen blocking (ie, samples with no antigen detected prior to heat treatment and positive after heat treatment) was 5.2%. Among dogs that had no detectable antigen on the initial tests, dogs that had microfilariae detected via modified Knott testing (OR = 32.30, p-value = 0.013) and dogs that previously received a heartworm preventive (OR = 3.81, p-value = 0.016) had greater odds of antigen blocking than dogs without these factors. Among dogs that were heartworm positive, those without microfilariae detected had greater odds of antigen blocking than dogs with this factor (OR = 11.84, p-value = 0.0005). Geographic region of origin was significantly associated with occurrence of antigen blocking (p = 0.0036); however, blocking occurred in all regions sizably contributing to heartworm diagnoses. Of the 74 dogs found to be infected with heartworms in this study, 39.2% (29) had no detectable antigen prior to heat treatment. Conclusions: Heat treatment of serum samples should be considered to improve diagnostic test accuracy, particularly in dogs that reportedly received a heartworm preventive prior to antigen testing regardless of region of origin. Keywords: Canine, Heartworm, Dirofilaria immitis, Antigen test, Diagnosis, Immune complex, Heat treatment * Correspondence: [email protected] 1Department of Small Animal Clinical Sciences, University of Florida, College of Veterinary Medicine, PO Box 142275, Gainesville, FL 32614, USA 10Present address: ASPCA, PO Box 142275, Gainesville, FL 32614, USA Full list of author information is available at the end of the article © The Author(s). 2017 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. The Author(s) Parasites & Vectors 2017, 10(Suppl 2):483 Page 124 of 235 Background protocol would be an effective method of disrupting im- The diagnosis and management of canine heartworm mune complex formation and improving accuracy of test disease is a growing concern for shelter veterinarians na- results. tionwide [1–4]. A recent survey of shelter veterinarians indicated that the majority of shelter practitioners rely Methods exclusively on point-of-care antigen testing for the diag- Animal shelters in Florida, Louisiana, and Texas (South); nosis of Dirofilaria immitis in shelter dogs [5]. The re- Ohio and New York (North); and Colorado and California sults of these tests often determine the management of (West) were recruited to participate in this study in order the dog throughout its stay in the shelter system, includ- to represent three geographic regions with similar re- ing its likelihood of a live release. Given the emphasis on ported regional prevalence of canine heartworm infection such diagnostic testing for the determination of [9]. Individual shelters were selected based on their will- heartworm-related medical and management decisions ingness to collect and test samples according to the study in the shelter environment, ensuring accuracy of the protocol and the ability to collect a sufficient number testing methodology is of the utmost importance. of samples during the data collection period (June– Although the accuracy of commercially available anti- November 2015). gen test kits has been widely studied, recent reports have Adult dogs six months of age or older (based on renewed interest in causative factors for false “no antigen known age or estimated by dentition) were eligible for detected” (NAD) test results [6–8]. One explanation for inclusion. Historical data were collected for each dog in- such results is the phenomenon of antigen blocking due cluding the state of origin, intake type (ie, stray, relin- to immune complex formation within the host. Al- quished, seizure, adoption return), whether the dog was though unknown whether such immune complexes are transferred from another geographic region, and history specific to D. immitis, their presence can hinder detec- of heartworm prophylaxis administered by a previous tion of the parasite in as many as 7% of samples [8]. De- owner or shelter of origin. Dogs transferred from regions struction of immune complexes through heat treatment other than the study site were analyzed using their re- of samples prior to testing reduces this occurrence and gion of origin. Clinical data for each dog were also col- improves test accuracy. In addition, serum with NAD lected at the time of intake including age, sex and neuter test results in highly microfilaremic dogs has also been status, predominant breed, body condition score, signs shown to test positive after heat treatment [6]. of infectious disease, and signs of noninfectious disease. Given the geographic variation in prevalence of heart- A uniform data collection log was completed for each worm infection as well as in other disease characteristics animal. Generally, this information was collected by a (eg, anthelmintic resistance, vector species), it is antici- member of the medical staff within 24 h of admission. pated that there may be geographic differences in the oc- A minimum of three milliliters of whole blood was currence of antigen blocking [8]. Determining the collected from each dog. One milliliter was placed in prevalence of antigen blocking in populations of shelter EDTA and refrigerated at 1.6–4.4 °C (35–40 °F) until dogs and identifying risk factors for false NAD test re- shipment to the diagnostic laboratory where samples sults are important to elevate the care of shelter dogs underwent Knott testing with morphologic examination and better prepare sheltering organizations and future and estimation of microfilarial count within 7 days of adopters to meet medical needs. collection [10]. The remaining blood sample was placed The objectives of the current study were to 1) deter- in a sterile collection tube with no additive and allowed mine the prevalence of false NAD antigen tests due to to clot. Once separated, the serum was removed and antigen blocking in shelter dogs in three different re- placed in a new sterile tube in preparation for antigen gions of the United States, 2) identify clinical and histor- testing. Unless tested immediately, serum samples were ical risk factors for antigen blocking, and 3) to assess the refrigerated at 1.6–4.4 °C (35–40 °F) and tested within feasibility of a simple, in-shelter heat treatment protocol 7 days of collection. to disrupt immune complex formation and subsequent Antigen testing was conducted with a commercially false NAD test results. We hypothesized that overall available ELISA antigen test kit (DiroCHEK® Heartworm prevalence of positive antigen test results will vary be- Antigen Test Kit, Zoetis) according to the manufac- tween geographic regions (ie, highest in southern re- turer’s instructions. Sera from NAD samples were di- gions, followed by western and northern) and that the luted with an equal volume of 0.9% saline to minimize frequency of antigen blocking would mirror regional coagulation (personal communication, Susan E. Little). prevalence. In addition, it was expected that microfilare- A 500 mL beaker was filled with 250 mL of water, placed mia would result in greater immune complex formation in a microwave, and heated to the point of boiling (ap- and therefore increased risk of false NAD antigen test proximately 2 min in a 1000 W unit). The heated water results. Finally, a simple, in-shelter heat treatment was removed from the microwave and up to five diluted The Author(s) Parasites & Vectors 2017, 10(Suppl 2):483 Page 125 of 235 serum samples were immersed in the hot water bath for Results 10 min. After heating, each sample underwent repeat Samples from 616 dogs were eligible for inclusion antigen testing as previously described. (see Additional file 1). A total of 45 samples (7.3%, Prior to treating study samples, two serum samples CI = 5.4–9.7) tested positive for D. immitis antigen known to exhibit antigen blocking on previous testing prior to heat treatment. Most positive samples origi- (personal communication, Susan E.
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