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Dirofilaria Immitis Laidoudi et al. Parasites Vectors (2020) 13:319 https://doi.org/10.1186/s13071-020-04185-0 Parasites & Vectors RESEARCH Open Access Development of a multiplex qPCR-based approach for the diagnosis of Diroflaria immitis, D. repens and Acanthocheilonema reconditum Younes Laidoudi1,2, Bernard Davoust1,2, Marie Varloud3, El Hadji Amadou Niang1,2, Florence Fenollar2,4 and Oleg Mediannikov1,2* Abstract Background: Diroflaria immitis, D. repens and Acanthocheilonema reconditum are the main causative agents of zoonotic canine flariosis. Methods: We developed a combined multiplex approach for flaria and Wolbachia detection using the 28S-based pan-flarial and 16S-based pan-Wolbachia qPCRs, respectively, involving a fast typing method of positive samples using triplex qPCR targeting A. reconditum, D. immitis and D. repens, and a duplex qPCR targeting Wolbachia of D. immitis and D. repens. The approach was complemented by a duplex qPCR for the diferential diagnosis of heart- worms (D. immitis and Angiostrongylus vasorum) and pan-flarial cox1 and pan-Wolbachia ftsZ PCRs to identify other flarial parasites and their Wolbachia, respectively. A total of 168 canine blood and sera samples were used to validate the approach. Spearmanʼs correlation was used to assess the association between flarial species and the strain of Wolbachia. Positive samples for both the heartworm antigen-test after heating sera and at least one DNA-positive for D. immitis and its Wolbachia were considered true positive for heartworm infection. Indeed, the presence of D. repens DNA or that of its Wolbachia as well as A. reconditum DNA indicates true positive infections. 1 4 Results: The detection limit for Wolbachia and flariae qPCRs ranged from 5 10− to 1.5 10− mf/ml of blood. When tested on clinical samples, 29.2% (49/168) tested positive for flariae or× Wolbachia DNA.× Filarial species and Wolbachia genotypes were identifed by the combined multiplex approach from all positive samples. Each species of Diroflaria was signifcantly associated with a specifc genotype of Wolbachia. Compared to the true positives, the approach showed excellent agreement (k 0.98–1). Unlike D. immitis DNA, no A. vasorum DNA was detected by the duplex qPCR. The immunochromatographic= test for heartworm antigen showed a substantial (k 0.6) and a weak (k 0.15) agreements before and after thermal pre-treatment of sera, respectively. = = Conclusions: The proposed approach is a reliable tool for the exploration and diagnosis of occult and non-occult canine flariosis. The current diagnosis of heartworm disease based on antigen detection should always be confrmed by qPCR essays. Sera heat pre-treatment is not efective and strongly discouraged. Keywords: Canine flariosis, Multiplex qPCRs, Diferential diagnosis, Heartworm disease, Diroflaria immitis Background Canine flariosis includes diseases caused by parasitic *Correspondence: [email protected] nematodes called flariae, belonging to the order Spiru- 1 Microbes, Evolution, Phylogeny and Infection (MEPHI), UMR Aix- Marseille University, IRD, APHM, IHU Méditerranée Infection, 19–21, Bd rida. Tere are several species of veterinary and human Jean Moulin, 13005 Marseille, France importance. Dogs seem to be the natural hosts for sev- Full list of author information is available at the end of the article eral species, such as Diroflaria immitis, D. repens, © The Author(s) 2020. 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. Laidoudi et al. Parasites Vectors (2020) 13:319 Page 2 of 15 Acanthocheilonema reconditum, A. dracunculoides, even more challenging. Te association of the heartworm Cercopithiflaria grassii, Brugia ceylonensis, B. patei, B. with D. repens infection may result in an unexplained malayi, B. pahangi, Onchocerca lupi and Telazia calli- suppressive efect on the production of microflariae of paeda [1–4]. Tese arthropod-borne flarioids produce D. immitis [18, 19]. In such cases, the cross-reactivity blood, cutaneous or mucous microflariae, where they are between D. immitis and D. repens may result in misdi- available to arthropod vectors [5]. Te most common and agnosis. Terefore, there is an urgent need for a more medically important species afecting dogs are D. immi- sensitive diagnostic method to detect occult as well as tis, D. repens and A. reconditum [6]. In addition to their non-occult canine flariosis and to identify the pathogen. veterinary importance, they can also afect human health. Detection of D. immitis has gained more and more atten- Diroflaria immitis causes pulmonary and cardiopul- tion; many trials have been performed for improving the monary diroflariosis in humans and dogs, respectively. quality of heartworm diagnostic tools, such as the detec- Cardiopulmonary diroflariosis usually called heartworm tion of a specifc antigen released by these worms [20], or disease has recently been considered as an emerging the use of a recombined antigen of D. immitis for specifc disease in Europe. In the USA, D. immitis is the most antibody detection [21]. important life-threatening parasitic infection in dogs Te endosymbiotic intracellular bacteria of the genus [7]. Elsewhere in the world, particularly in eastern Euro- Wolbachia are associated with some flarial species of two pean countries, D. repens is the most endemic parasitic subfamilies of the Onchocercidae: Onchocercinae and nematode causing subcutaneous infection, which is less Diroflariinae [22]. Tese bacteria are host-specifc, and virulent but more zoonotic than that caused by D. immi- each species of flarial worm is associated with a specifc tis [8]. Acanthocheilonema reconditum is an occasional bacterial genotype. Wolbachia spp. have been targeted zoonotic agent that afects the subcutaneous tissue and for the indirect diagnosis of D. immitis infection in dead- the perirenal fat [9, 10] causing a common but clinically end hosts such as humans and cats, whereby the strong less important infection in dogs [11]. reaction of the host against the parasite prevents them to Once mature, these flarioids can produce microflariae achieving their maturation, and, therefore, the produc- circulating in the bloodstream. Tis larval stage (L1) is tion of microflariae may not be achieved [23]. In such also a target for the diagnosis by microscopic detection of cases, the detection of flaria-specifc Wolbachia may the larvae or by detection of their DNA in the host blood indicate a flarial infection and can serve as an alterna- [10]. Diroflaria immitis, the agent of heartworm dis- tive diagnostic tool in endemic areas [23, 24]. In around ease, is distributed worldwide and is responsible for heart 40–60% of canine heartworm cases, both Wolbachia and failure in dogs after colonization of pulmonary arteries parasite DNA may be detected using conventional PCR and the right ventricle, where it can be fatal if untreated. [25–27]. Indeed, the combined detection of Wolbachia Due to the gravity of the disease, it remains the most and Diroflaria DNA was suggested to improve heart- commonly diagnosed flariosis in dogs due to the detec- worm detection [27]. tion of antigen circulating in the blood [11–13]. Several In the present study, we developed a multiplex real- problems with the current diagnostic methods have been time PCR-based approach allowing a specifc, rapid and raised, such as morphological confusion between the simultaneous detection of D. immitis, D. repens and A. microflariae of D. immitis, A. reconditum and D. repens. reconditum as well as the occult Diroflaria spp. infec- Commercially available diagnostic kits for the detec- tions in dogs. In addition, it was completed by a duplex tion of D. immitis antigens may also cross-react with real-time PCR-based assay for the simultaneous detec- flarial and non-flarial nematodes, such as D. repens, A. tion of D. immitis and A. vasorum as a diferential diag- reconditum and Onchocerca spp. [14], Spirocerca lupi and nostic for canine heartworms. Te approach can be used Angiostrongylus vasorum, especially the latter which can in routinely in a diagnostic laboratory. We also evaluated cause a cross-reaction without prior heat pre-treatment the efectiveness of a novel molecular approach to con- of the sera [15–17]. Angiostrongylus vasorum, the agent ventional serological diagnosis and assessed the impor- of French heartworm disease, should also be taken into tance of serum heating. account in the diferential diagnosis of pulmonary disease [17]. Tis so-called occult heartworm is characterized Methods by the absence of microflaremia or an amicroflaremia. Probes, primers design and PCR amplifcation protocol Tis may result from the hostʼs immune response, low Custom protocol and in silico validation parasite load and infertility or, incidentally, the microfla- First, for each PCR assay, the target gene was chosen to ricidal efect observed in dogs receiving macrocyclic lac- meet the objective of each system. Fasta fles were con- tone prevention [14]. When the occult heartworm occurs structed from the sequences of the representative mem- in a co-infection with another flariosis, the diagnosis is bers of the family Onchocercidae or Wolbachia genotypes Laidoudi et al.
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