Comparison of Diagnostic Tools for the Detection of Dirofilaria immitis Infection in Dogs
Abstract
1. Introduction
2. Results
3. Discussion
4. Materials and Methods
4.1. Study Design
4.2. Diagnostic Procedures
4.3. Data Handling and Statistical Analysis
Author Contributions
Funding
Acknowledgments
Conflicts of Interest
References
- Simón, F.; Siles-Lucas, M.; Morchón, R.; González-Miguel, J.; Mellado, I.; Carretón, E.; Montoya-Alonso, J.A. Human and animal dirofilariasis: The emergence of a zoonotic mosaic. Clin. Microbiol. Rev. 2012, 25, 507–544. [Google Scholar] [CrossRef]
- Dantas-Torres, F.; Otranto, D. Dirofilariosis in the Americas: A more virulent Dirofilaria immitis? Parasit Vectors 2013, 6, 288. [Google Scholar] [CrossRef]
- Colella, V.; Nguyen, V.L.; Tan, D.Y.; Lu, N.; Fang, F.; Zhijuan, Y.; Wang, J.; Liu, X.; Chen, X.; Dong, J.; et al. Zoonotic vectorborne pathogens and ectoparasites of dogs and cats in Eastern and Southeast Asia. Emerg. Infect. Dis. 2020, 26, 1221–1233. [Google Scholar] [CrossRef] [PubMed]
- Otranto, D.; Brianti, E.; Gaglio, G.; Dantas-Torres, F.; Azzaro, S.; Giannetto, S. Human ocular infection with Dirofilaria repens (Railliet and Henry, 1911) in an area endemic for canine dirofilariasis. Am. J. Trop. Med. Hyg. 2011, 84, 1002–1004. [Google Scholar] [CrossRef] [PubMed]
- Otranto, D.; Diniz, D.G.; Dantas-Torres, F.; Casiraghi, M.; Almeida, I.N.F.; Almeida, L.N.F.; Santos, J.N.; Furtado, A.P.; Sobrinho, E.F.A.; Bain, O. Human intraocular filariasis caused by Dirofilaria sp. nematode, Brazil. Emerg. Infect. Dis. 2011, 17, 863–866. [Google Scholar] [CrossRef] [PubMed]
- Capelli, G.; Genchi, C.; Baneth, G.; Bourdeau, P.; Brianti, E.; Cardoso, L.; Danesi, P.; Fuehrer, H.P.; Giannelli, A.; Ionică, A.M.; et al. Recent advances on Dirofilaria repens in dogs and humans in Europe. Parasit Vectors 2018, 11, 663. [Google Scholar] [CrossRef]
- Dantas-Torres, F.; Otranto, D. Overview on Dirofilaria immitis in the Americas, with notes on other filarial worms infecting dogs. Vet. Parasitol. 2020, 282, 109113. [Google Scholar] [CrossRef]
- Otranto, D.; Capelli, G.; Genchi, C. Changing distribution patterns of canine vector borne diseases in Italy: Leishmaniosis vs. dirofilariosis. Parasit Vectors 2009, 26, S1–S2. [Google Scholar] [CrossRef]
- Mendoza-Roldan, J.; Benelli, G.; Panarese, R.; Iatta, R.; Furlanello, T.; Beugnet, F.; Zatelli, A.; Otranto, D. Leishmania infantum and Dirofilaria immitis infections in Italy, 2009–2019: Changing distribution patterns. Parasit Vectors 2020, 13, 193. [Google Scholar] [CrossRef]
- Panarese, R.; Iatta, R.; Latrofa, M.S.; Zatelli, A.; Ćupina, A.I.; Montarsi, F.; Pombi, M.; Mendoza-Roldan, J.A.; Beugnet, F.; Otranto, D. Hyperendemic Dirofilaria immitis infection in a sheltered dog population: An expanding threat in the Mediterranean region. Int. J. Parasitol. 2020, S0020-7519(20), 30114-4. [Google Scholar]
- Diosdado, A.; Gómez, P.; González-Miguel, J.; Simón, F.; Morchón, R. Current status of canine dirofilariosis in an endemic area of western Spain. J. Helminthol. 2018, 92, 520–523. [Google Scholar] [CrossRef] [PubMed]
- Miterpáková, M.; Valentová, A.; Čabanová, V.; Berešíková, L. Heartworm on the rise—New insights into Dirofilaria immitis epidemiology. Parasitol. Res. 2018, 117, 2347–2350. [Google Scholar] [CrossRef] [PubMed]
- Stoyanova, H.; Carretón, E.; Montoya-Alonso, J.A. Stray dogs of Sofia (Bulgaria) could be an important reservoir of heartworm (Dirofilaria Immitis). Helminthologia 2019, 56, 329–333. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, Y.; Yang, C.H.; Tung, K.C.; Ooi, H.K. Comparison of microfilaria concentration method for Setaria digitata infection in cattle and for Dirofilaria immitis infection in dogs. J. Vet. Med. Sci. 2004, 66, 543–545. [Google Scholar] [CrossRef][Green Version]
- Venco, L.; Genchi, C.; Simón, F. La filariosis cardiopulmonar (Dirofilaria immitis) en el perro. In La Filariosis en las Especies Domésticas y en el Hombre; Simón, F., Genchi, C., Venco, L., Montoya, M.N., Eds.; Merial Laboratorios: Barcelona, Spain, 2011; pp. 19–60. [Google Scholar]
- Otto, G.F. The significance of microfilaremia in the diagnosis of heartworm infection. Proc. Heartworm Symp. 1978, 77, 22–30. [Google Scholar]
- Newton, W.L.; Wright, W.H. The occurrence of a dog filariid other than Dirofilaria immitis in the United States. J. Parasitol. 1956, 42, 246–258. [Google Scholar] [CrossRef]
- Lee, A.C.Y.; Bowman, D.D.; Lucio-Forster, A.; Beall, M.J.; Liotta, J.L.; Dillon, R. Evaluation of a new in-clinic method for the detection of canine heartworm antigen. Vet. Parasitol. 2011, 177, 387–391. [Google Scholar] [CrossRef]
- Venco, L.; Manzocchi, S.; Genchi, M.; Kramer, L.H. Heat treatment and false-positive heartworm antigen testing in ex vivo parasites and dogs naturally infected by Dirofilaria repens and Angiostrongylus vasorum. Parasit Vectors 2017, 10, 476. [Google Scholar] [CrossRef]
- Henry, L.G.; Brunson, K.J.; Walden, H.S.; Wenzlow, N.; Beachboard, S.E.; Barr, K.L.; Long, M.T. Comparison of six commercial antigen kits for detection of Dirofilaria immitis infections in canines with necropsy-confirmed heartworm status. Vet. Parasitol. 2018, 254, 178–182. [Google Scholar] [CrossRef]
- Weil, G.J.; Malane, M.S.; Powers, K.G.; Blair, L.S. Monoclonal antibodies to parasite antigens found in the serum of Dirofilaria immitis-infected dogs. J. Immunol. 1985, 134, 1185–1191. [Google Scholar]
- Little, S.E.; Munzing, C.; Heise, S.R.; Allen, K.E.; Starkey, L.A.; Johnson, E.M.; Meinkoth, J.; Reichard, M.V. Pretreatment with heat facilitates detection of antigen of Dirofilaria immitis in canine samples. Vet. Parasitol. 2014, 20, 250–252. [Google Scholar] [CrossRef] [PubMed]
- Beall, M.J.; Arguello-Marin, A.; Drexel, J.; Liu, J.; Chandrashekar, R.; Alleman, A.R. Validation of immune complex dissociation methods for use with heartworm antigen tests. Parasit Vectors 2017, 10, 481. [Google Scholar] [CrossRef] [PubMed]
- Courtney, C.H.; Zeng, Q.Y. Comparison of heartworm antigen test kit performance in dogs having low heartworm burdens. Vet. Parasitol. 2001, 96, 317–322. [Google Scholar] [CrossRef]
- Starkey, L.A.; Bowles, J.V.; Payton, M.E.; Blagburn, B.L. Comparative evaluation of commercially available point-of-care heartworm antigen tests using well-characterized canine plasma samples. Parasit Vectors 2017, 10, 475. [Google Scholar] [CrossRef]
- Velasquez, L.; Blagburn, B.L.; Duncan-Decoq, R.; Johnson, E.M.; Allen, K.E.; Meinkoth, J.; Gruntmeira, J.; Littlea, S.E. Increased prevalence of Dirofilaria immitis antigen in canine samples after heat treatment. Vet. Parasitol. 2014, 206, 67–70. [Google Scholar] [CrossRef]
- Drake, J.; Gruntmeir, J.; Merritt, H.; Allen, L.; Little, S.E. False negative antigen tests in dogs infected with heartworm and placed on macrocyclic lactone preventives. Parasit Vectors 2015, 8, 68. [Google Scholar] [CrossRef]
- Knott, J. A method for making microfilarial survey on day blood. Med. Hyg. 1939, 33, 191–196. [Google Scholar] [CrossRef]
- Otranto, D.; Testini, G.; Dantas-Torres, F.; Latrofa, M.S.; Diniz, P.P.; de Caprariis, D.; Lia, R.P.; Mencke, N.; Stanneck, D.; Capelli, G.; et al. Diagnosis of canine vector-borne diseases in young dogs: A longitudinal study. J. Clin. Microbiol. 2010, 48, 3316–3324. [Google Scholar] [CrossRef]
- Rawlings, C.A.; Dawe, D.L.; McCall, J.W.; Keith, J.C.; Prestwood, A.K. Four types of occult Dirofilaria immitis infection in dogs. J. Am. Vet. Med. Assoc. 1982, 180, 1323–1326. [Google Scholar]
- Church, E.M.; Georgi, J.R.; Robson, D.S. Analysis of the microfilarial periodicity of Dirofilaria immitis. Cornell Vet. 1976, 66, 333–346. [Google Scholar]
- Nafe, L. Prevalence of Dirofilaria immitis antigen in client-owned pet dogs before and after serum heat treatment. In Proceedings of the Annual ACVIM Forum, Denver, CO, USA, 9–11 June 2016; Volume 30, p. 1428. [Google Scholar]
- Trancoso, T.A.L.; Lima, N.C.; Barbosa, A.S.; Leles, D.; Fonseca, A.B.M.; Labarthe, N.V.; Bastos, O.M.P.; Uchôa, C.M.A. Detection of Dirofilaria immitis using microscopic, serological and molecular techniques among dogs in Cabo Frio, RJ, Brazil. Braz. J. Vet. Parasitol. 2020, 29, e017219. [Google Scholar] [CrossRef] [PubMed]
Knott’s Test Negative Samples (n = 184) | SNAP 4Dx Plus | HW Ag ELISA without Preheating | HW Ag ELISA with Preheating |
---|---|---|---|
50 | Positive | Positive | Positive |
9 | Negative | Positive | Positive |
56 | Negative | Negative | Positive |
2 | Negative | Positive | Negative |
67 | Negative | Negative | Negative |
Modified Knott’s Method | HW Ag ELISA without Preheating | HW Ag ELISA with Preheating | Increase in Positive Samples with vs. without Preheating (%) |
---|---|---|---|
Dirofilaria immitis and co-infected a | 137 | 159 | 16% |
Dirofilaria repens only | 7 | 15 | 114% |
No microfilaria observed | 59 | 115 | 95% |
Total | 205 | 289 | 42% |
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Panarese, R.; Iatta, R.; Mendoza-Roldan, J.A.; Szlosek, D.; Braff, J.; Liu, J.; Beugnet, F.; Dantas-Torres, F.; Beall, M.J.; Otranto, D. Comparison of Diagnostic Tools for the Detection of Dirofilaria immitis Infection in Dogs. Pathogens 2020, 9, 499. https://doi.org/10.3390/pathogens9060499
Panarese R, Iatta R, Mendoza-Roldan JA, Szlosek D, Braff J, Liu J, Beugnet F, Dantas-Torres F, Beall MJ, Otranto D. Comparison of Diagnostic Tools for the Detection of Dirofilaria immitis Infection in Dogs. Pathogens. 2020; 9(6):499. https://doi.org/10.3390/pathogens9060499
Chicago/Turabian StylePanarese, Rossella, Roberta Iatta, Jairo Alfonso Mendoza-Roldan, Donald Szlosek, Jennifer Braff, Joe Liu, Frédéric Beugnet, Filipe Dantas-Torres, Melissa J. Beall, and Domenico Otranto. 2020. "Comparison of Diagnostic Tools for the Detection of Dirofilaria immitis Infection in Dogs" Pathogens 9, no. 6: 499. https://doi.org/10.3390/pathogens9060499
APA StylePanarese, R., Iatta, R., Mendoza-Roldan, J. A., Szlosek, D., Braff, J., Liu, J., Beugnet, F., Dantas-Torres, F., Beall, M. J., & Otranto, D. (2020). Comparison of Diagnostic Tools for the Detection of Dirofilaria immitis Infection in Dogs. Pathogens, 9(6), 499. https://doi.org/10.3390/pathogens9060499