Anti-Wolbachia Surface Protein Antibodies Are Present in the Urine of Dogs Naturally Infected with Dirofilaria immitis with Circulating Microfilariae But Not in Dogs with Occult Infections
Open accessAbstract
Heartworm infection (Dirofilaria immitis) can cause kidney damage due to the presence of circulating microfilariae (mf) that contribute to the production and deposit of immune complexes. It has been shown that mf are a major source of Wolbachia antigen during active infection. Here the authors compared urine samples from 19 naturally infected dogs with (mf+) and 12 without (mf-) microfilariae for the presence of proteinuria and anti-Wolbachia Surface Protein (-WSP) IgG in ELISA. Kidneys from 6 mf+ and 3 mf- dogs were also examined by anti-WSP immuno-histochemistry. All infected dogs showed proteinuria, but mf+ dogs had significantly higher values compared to mf-dogs. Mf+ dogs had optical density values for anti-WSP IgG consistently higher than established cut-off values and were significantly higher than values for mf- dogs. Kidneys from mf+ dogs showed Wolbachia+ mf in glomerular capillaries. Results strongly suggest that Wolbachia associated with circulating mf may contribute to immune-mediated kidney disease in dogs with heartworm infection.
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Among dogs with glomerulonephritis and proteinuria linked to dirofilariasis, anti-WSP IgG levels in urine are higher in microfilaremic than amicrofilaremic animals.
“Among dogs with glomerulonephritis and proteinuria linked to dirofilariasis, higher levels of anti-WSP IgG antibodies were detected in the urine of microfilaremic animals than in amicrofilaremic animals (288).”
From Human and animal dirofilariasis: The emergence of a zoonotic mosaic (2012) · cites this paper as [288]
Wolbachia is present in multiple tissues and immune cells of dogs with heartworm disease, as shown by immunohistochemical staining.
“immunohistochemical staining with polyclonal antibodies against WSP has revealed the presence of Wolbachia in multiple tissues and immune cells of dogs with heartworm disease (215,216,288).”
From Human and animal dirofilariasis: The emergence of a zoonotic mosaic (2012) · cites this paper as [288]
Cites
Chapter 4 Heartworm Disease in Animals and Humans
McCall, J. W., Genchi, C., Kramer, L. H., Guerrero, J., & Venco, L. (2008) · Advances in Parasitology · doi:10.1016/s0065-308x(08)00204-2 · Cited by 609 · see citing works
Self-citationRenal Abnormalities in Microfilaremic Patients with Bancroftian Filariasis
Dreyer, G., Ottesen, E. A., Galdino, E., Andrade, L., Rocha, A., de Medeiros, Z. M., Moura, I. F., Casimiro, I., Béliz, F., & Coutinho, A. (1992) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1992.46.745 · Cited by 103 · see citing works
Wolbachia and its influence on the pathology and immunology of Dirofilaria immitis infection
Kramer, L., Grandi, G., Leoni, M., Passeri, B., McCall, J., Genchi, C., Mortarino, M., & Bazzocchi, C. (2008) · Veterinary Parasitology · doi:10.1016/j.vetpar.2008.09.014 · Cited by 94 · see citing works
Self-citationBazzocchi, C., Ceciliani, F., McCall, J. W., Ricci, I., Genchi, C., & Bandi, C. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1313 · Cited by 93 · see citing works
Self-citationKramer, L., Passeri, B., Corona, S., Simoncini, L., & Casiraghi, M. (2003) · Parasitology Research · doi:10.1007/s00436-002-0765-6 · Cited by 79 · see citing works
Self-citationMorchón, R., Ferreira, A. C., Martín-Pacho, J. R., Montoya, A., Mortarino, M., Genchi, C., & Simón, F. (2004) · Veterinary Parasitology · doi:10.1016/j.vetpar.2004.08.003 · Cited by 62 · see citing works
Self-citationLulıch, J. P., & Osborne, C. A. (1990) · Compendium on Continuing Education for The Practicing Veterinarian · Cited by 39 · see citing works
Grauer, G. F., Culham, C. A., Dubielzig, R. R., Longhofer, S. L., & Grieve, R. B. (1989) · Journal of Parasitology · doi:10.2307/3282910 · Cited by 39 · see citing works
Dirofilaria immitis. 5. Immunopathology of filarial nephropathy in dogs.
Abramowsky, C. R., Powers, K. G., Aikawa, M., & Swinehart, G. L. (1981) · PubMed Central · Cited by 38 · see citing works
Morchón, R., López-Belmonte, J., Bazzocchi, C., Grandi, G., Kramer, L., & Simón, F. (2007) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2006.10.004 · Cited by 34 · see citing works
Self-citationPaes-de-Almeida, E. C., Ferreira, A. M. R., Labarthe, N., Caldas, M., & McCall, J. W. (2003) · Veterinary Parasitology · doi:10.1016/s0304-4017(03)00020-7 · Cited by 33 · see citing works
Renal microcirculatory and correlated histologic changes associated with dirofilariasis in dogs
Ludders, J. W., Grauer, G. F., Dubielzig, R. R., Ribble, G. A., & Wilson, J. W. (1988) · American Journal of Veterinary Research · doi:10.2460/ajvr.1988.49.06.826 · Cited by 29 · see citing works
Solano‐Gallego, L., Rodríguez, A., Iniesta, L., Arboix, M., Portús, M., & Alberola, J. (2003) · Clinical and Vaccine Immunology · doi:10.1128/cdli.10.5.849-855.2003 · Cited by 28 · see citing works
Upregulation of Cardiac Cell Plasma Membrane Calcium Pump in a Canine Model of Chagas Disease
Barr, S. C., Pannabecker, T. L., Gilmour, R. F., & Chandler, J. S. (2003) · Journal of Parasitology · doi:10.1645/0022-3395(2003)089[0381:uoccpm]2.0.co;2 · Cited by 14 · see citing works
Grauer, G. F., Culham, C. A., Dubielzig, R. R., Presto, S., Oberley, T. D., Thomas, C. B., & Grieve, R. B. (1988) · Journal of Veterinary Internal Medicine · doi:10.1111/j.1939-1676.1988.tb00316.x · Cited by 11 · see citing works
Nakagaki, K., HAYASAKI, M., & OHISHI, I. (1990) · PubMed · Cited by 9 · see citing works
Wenk, P., Kellermann, E., & Seeger (1993) · PubMed · Cited by 4 · see citing works
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Human and animal dirofilariasis: The emergence of a zoonotic mosaic
Simón, F., Siles-Lucas, M., Morchón, R., González-Miguel, J., Mellado, I., Carretón, E., & Montoya-Alonso, J. A. (2012) · Clinical Microbiology Reviews · doi:10.1128/cmr.00012-12 · Cited by 834 · see citing works
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Ferreira, C., Afonso, A., Calado, M., Maurício, I., Alho, A. M., Meireles, J., Madeira de Carvalho, L., & Belo, S. (2017) · Parasites & Vectors · doi:10.1186/s13071-017-2180-y · Cited by 33 · see citing works
Carretón, E., Falcón-Cordón, Y., Rodón, J., Matos, J. I., Morchón, R., & Montoya-Alonso, J. A. (2020) · Veterinary Parasitology · doi:10.1016/j.vetpar.2020.109144 · Cited by 25 · see citing works
Self-citationProteomic analysis of the urine of Dirofilaria immitis infected dogs
Hormaeche, M., Carretón, E., González‐Miguel, J., Gussoni, S., Montoya-Alonso, J. A., Simón, F., & Morchón, R. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.01.025 · Cited by 22 · see citing works
Self-citationCiucă, L., Vismarra, A., Lebon, W., Beugnet, F., Morchón, R., Rinaldi, L., Cringoli, G., Kramer, L. H., & Genchi, M. (2020) · Veterinary Parasitology · doi:10.1016/j.vpoa.2020.100029 · Cited by 21 · see citing works
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Wysmołek, M. E., Dobrzyński, A., Długosz, E., Czopowicz, M., Wiśniewski, M., Jurka, P., & Klockiewicz, M. (2020) · Frontiers in Veterinary Science · doi:10.3389/fvets.2020.00590 · Cited by 14 · see citing works
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Hartmann, K., Pennisi, M. G., & Dorsch, R. (2020) · Advances in Small Animal Care · doi:10.1016/j.yasa.2020.07.013 · Cited by 12 · see citing works
Carretón, E., González‐Miguel, J., Montoya-Alonso, J. A., Morchón, R., Simón, F., Passeri, B., Cantoni, A. M., & Kramer, L. H. (2012) · Veterinary Parasitology · doi:10.1016/j.vetpar.2012.08.008 · Cited by 11 · see citing works
Self-citationSungpradit, S., & Sanprasert, V. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-821202-8.00004-9 · Cited by 5 · see citing works
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Vetter, C., Meindl, A. G., Lourenço, B. N., Coyne, M. J., Drake, C., Murphy, R. E., Roth, I. G., & Moorhead, A. R. (2023) · Parasites & Vectors · doi:10.1186/s13071-023-05779-0 · Cited by 4 · see citing works
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Preyß-Jägeler, C., Hartmann, K., & Dorsch, R. (2022) · Tierärztliche Praxis Ausgabe K Kleintiere / Heimtiere · doi:10.1055/a-1811-6186 · Cited by 3 · see citing works
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Falus, F. A., Szabo, K. J., Becker, Z., Müller, L., Fok, É., Balogh, N., & Manczur, F. (2023) · Journal of Veterinary Internal Medicine · doi:10.1111/jvim.16712 · Cited by 2 · see citing works
Collado-Cuadrado, M., la Puente, A. B., Rodríguez-Escolar, I., González-Mohino, E. I., Alarcón-Torrecillas, C., Pericacho, M., & Morchón, R. (2025) · Animals · doi:10.3390/ani15070964 · Cited by 2 · see citing works
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Wysmołek, M. E., Klockiewicz, M., Długosz, E., & Wiśniewski, M. (2022) · Comparative Immunology Microbiology and Infectious Diseases · doi:10.1016/j.cimid.2022.101818 · Cited by 2 · see citing works
Gamboa‐Suárez, B. A., González, A. D., Nova‐Chamorro, M. H., Brieva, C., & Matta, N. E. (2025) · Integrative Zoology · doi:10.1111/1749-4877.12993 · Cited by 1 · see citing works
Transient glomerular dysfunction in dogs caused by Dirofilaria immitis infection.
Rusenov, A. G., Lazarov, L., Kirkova, Z., Tonev, A., Rusenova, N., & Dilda, F. (2015) · Kafkas Universitesi Veteriner Fakultesi Dergisi · Cited by 1 · see citing works
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Brown, A. C., Saleh, M. N., Fudge, J. M., Nabity, M. B., & Verocai, G. G. (2022) · Research Square · doi:10.21203/rs.3.rs-2375264/v1 · Cited by 1 · see citing works
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Rusenov, A. G., Lazarov, L., Kirkova, Z., Tonev, A., Rusenova, N., & Dilda, F. (2014) · Kafkas Universitesi Veteriner Fakultesi Dergisi · doi:10.9775/kvfd.2014.11680
Diniz, P. P. V. D. P. (2020) · Clinical Small Animal Internal Medicine · doi:10.1002/9781119501237.ch95
ACVIM, D. J. C. D. D., & Schenck, P. A. (2023) · Wiley eBooks · doi:10.1002/9781119380443.ch7
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Tizard, I. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23681-5.00018-4
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Tizard, I. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-23681-5.00016-0
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Tizard, I. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-29178-4.00017-4
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Tizard, I. R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-29178-4.00020-4
Costa-Rodríguez, N., Vera-Rodríguez, D. J., Falcón-Cordón, S., Morales, B. R., Morchón, R., Montoya-Alonso, J. A., & Carretón, E. (2025) · Animals · doi:10.3390/ani15142003
Self-citation
- Authors
- Morchón, R., Carretón, E., Grandi, G., González-Miguel, J., Montoya-Alonso, J. A., Simón, F., Genchi, C., & Kramer, L. H.
- Affiliations
- University of Parma (IT)
- Universidad de Las Palmas de Gran Canaria (ES)
- Laboratory of Parasitology, Faculty of Pharmacy, University of Salamanca, Salamanca, Spain.
- Universidad de Salamanca (ES)
- University of Milan (IT)
- Corresponding author
- Kramer, Laura H.
- ORCID
- Venue
- Vector-Borne and Zoonotic Diseases
- Publisher
- SAGE Publications
- Published
- 2012-01
- Volume
- 12
- Issue
- 1
- Pages
- 17-20
- ISSN
- 1530-3667 (ISSN-L)
- 1557-7759
- PMC
- PMC3249894
- OpenAlex
- W2041208399
- Cited by
- 30
- References
- 17
- Citations by year
- 2025: 4 · 2024: 4 · 2023: 4 · 2022: 4 · 2020: 6 · 2019: 1 · 2017: 1 · 2015: 1 · 2014: 3 · 2012: 2
- FWCI
- 1.08
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Vector-Borne and Zoonotic Diseases (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Acceda (Universidad de Las Palmas de Gran Canaria) (submittedVersion)
- Topics
- Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
- Health Sciences › Veterinary › Small Animals › Helminth infection and control
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Keywords
- Dirofilaria immitis, canine heartworm disease, Wolbachia, occult infection, proteinuria, kidney injury, immune complexes, glomerular deposition
- MeSH terms
- Animals, Antibodies, Bacterial, Bacterial Outer Membrane Proteins, Dirofilaria immitis, Dirofilariasis, Dog Diseases, Dogs, Microfilariae, Wolbachia
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