Immunohistochemical/immunogold detection and distribution of the endosymbiont Wolbachia of Dirofilaria immitis and Brugia pahangi using a polyclonal antiserum raised against WSP (Wolbachia surface protein)
Abstract
Intracellular bacteria in filarial nematodes were described as early as the 1970s, yet it was only with the work on Dirofilaria immitis, the agent of canine and feline heartworm disease, that these microorganisms were identified as belonging to Wolbachia, a genus known for encompassing bacteria infecting insects and other arthropods. The implications for the presence of intracellular bacteria in filarial nematodes is now the subject of intense research, particularly regarding their role in the immunology and pathogenesis of disease in infected humans and animals and as a possible target for therapy. Here, the authors report results on the immunohistochemical and immunogold staining of Wolbachia in D. immitis and Brugia pahangi using polyclonal antibodies raised against the recombinant Wolbachia surface protein (WSP). The bacteria were present in the lateral hypodermal chords of both male and female worms and in the reproductive tract of adult females (oocytes, morulae, microfilariae). In D. immitis and B. pahangi from animals treated with tetracycline, positive staining was observed in the lateral chords of adult males and females, but was absent from the oocytes and morulae. These results indicate that Wolbachia endosymbionts can be identified immunohistochemically with anti-WSP polyclonal antibodies, that their distribution matches that already described for Wolbachia of other filarial worms, and that antibiotic treatment may impede the vertical transmission of these bacteria. Unequivocal detection of Wolbachia is essential for the study of this symbiont, in particular to monitor the effects of antibiotic treatment on worms. The use of a specific marker for bacteria in their nematode hosts represents an extremely useful tool in evaluating the pathogenic role and the effect of antibiotic treatment on these potential targets in the control of filarial disease.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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 [215]
Cites
Braig, H. R., Zhou, W., Dobson, S. L., & O’Neill, S. L. (1998) · Journal of Bacteriology · doi:10.1128/jb.180.9.2373-2378.1998 · Cited by 668 · see citing works
Phylogeny of Wolbachia in filarial nematodes
Bandi, C., Anderson, T., Genchi, C., & Blaxter, M. (1998) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.1998.0591 · Cited by 576 · see citing works
Hoerauf, A. M., Nissen-Pähle, K., Schmetz, C., Henkle-Dührsen, K., Blaxter, M., Büttner, D. W., Gallin, M. Y., Al-Qaoud, K. M., Lucius, R., & Fleischer, B. (1999) · Journal of Clinical Investigation · doi:10.1172/jci4768 · Cited by 336 · see citing works
Endosymbiotic bacteria in worms as targets for a novel chemotherapy in filariasis
Hoerauf, A. M., Volkmann, L., Hamelmann, C., Adjei, O., Autenrieth, I. B., Fleischer, B., & Büttner, D. W. (2000) · The Lancet · doi:10.1016/s0140-6736(00)02095-x · Cited by 310 · see citing works
Wolbachia Bacteria of Filarial Nematodes
Taylor, M. J., & Hoerauf, A. (1999) · Parasitology Today · doi:10.1016/s0169-4758(99)01533-1 · Cited by 309 · see citing works
Hoerauf, A. M., Mand, S., Adjei, O., Fleischer, B., & Büttner, D. W. (2001) · The Lancet · doi:10.1016/s0140-6736(00)04581-5 · Cited by 282 · see citing works
Molecular evidence for a close relative of the arthropod endosymbiont Wolbachia in a filarial worm
Sironi, M., Bandi, C., Sacchi, L., di Sacco, B., Damiani, G., & Genchi, C. (1995) · Molecular and Biochemical Parasitology · doi:10.1016/0166-6851(95)02494-8 · Cited by 251 · see citing works
Bandi, C., McCall, J. W., Genchi, C., Corona, S., Venco, L., & Sacchi, L. (1999) · International Journal for Parasitology · doi:10.1016/s0020-7519(98)00200-8 · Cited by 250 · see citing works
Self-citationBandi, C., Trees, A. J., & Brattig, N. W. (2001) · Veterinary Parasitology · doi:10.1016/s0304-4017(01)00432-0 · Cited by 233 · see citing works
Langworthy, N. G., Renz, A., Ute Mackenstedt, A., Henkle–Dührsen, K., Bronsvoort, M., Tanya, V. N., Donnelly, M. J., & Trees, A. J. (2000) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2000.1110 · Cited by 207 · see citing works
Neutrophil accumulation around worms and chemotaxis of neutrophils are dependent on endobacteria
Brattig, N. W., Büttner, D. W., & Hoerauf, A. M. (2001) · Microbes and Infection · doi:10.1016/s1286-4579(01)01399-5 · Cited by 182 · see citing works
A comparison of two immunoperoxidase staining methods based on the avidin-biotin interaction.
Giorno, R. C. (1984) · PubMed · Cited by 177 · see citing works
Micro-organisms in filarial larvae (Nematoda)
McLaren, D. J., Worms, M. J., Laurence, B. R., & Simpson, M. G. (1975) · Transactions of the Royal Society of Tropical Medicine and Hygiene · doi:10.1016/0035-9203(75)90110-8 · Cited by 151 · see citing works
Intracytoplasmic Bacteria in Onchocerca Volvulus
Kozek, W. J., & Marroquín, H. F. (1977) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.1977.26.663 · Cited by 131 · see citing works
Brattig, N. W., Rathjens, U., Ernst, M., Geisinger, F., Renz, A., & Tischendorf, F. W. (2000) · Microbes and Infection · doi:10.1016/s1286-4579(00)01269-7 · Cited by 113 · see citing works
Taylor, M. J., Bilo, K., Cross, H. F., Archer, J. P., & Underwood, A. P. (1999) · Experimental Parasitology · doi:10.1006/expr.1998.4383 · Cited by 106 · see citing works
Bosshardt, S. C., McCall, J. W., Coleman, S. U., Jones, K. L., Petit, T. A., & Klei, T. R. (1993) · Journal of Parasitology · doi:10.2307/3283620 · Cited by 98 · see citing works
Bazzocchi, 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
wsp Gene Sequences from the Wolbachia of Filarial Nematodes
Bazzocchi, C., Jamnongluk, W., O'Neill, S. L., Anderson, T. J. C., Genchi, C., & Bandi, C. (2000) · Current Microbiology · doi:10.1007/s002840010100 · Cited by 87 · see citing works
Molecular identification of Wolbachia from the filarial nematode Mansonella ozzardi
Casiraghi, M., Favia, G., Cancrini, G., Bartoloni, A., & Bandi, C. (2001) · Parasitology Research · doi:10.1007/s004360000368 · Cited by 69 · see citing works
Self-citationHenkle‐Dührsen, K., ECKELT, V. H. O., Wildenburg, G., Blaxter, M., & Walter, R. D. (1998) · Molecular and Biochemical Parasitology · doi:10.1016/s0166-6851(98)00109-1 · Cited by 62 · see citing works
Wolbachia and the antifilarial properties of tetracycline. An untold story
McCall, J. W., Jun, J. J., & Bandi, C. (1999) · The European Zoological Journal · doi:10.1080/11250009909356230 · Cited by 62 · see citing works
Real-time PCR for quantification of the bacterial endosymbionts (Wolbachia) of filarial nematodes.
Simoncini, L., Casiraghi, M., Bazzocchi, C., Sacchi, L., Bandi, C., & Genchi, C. (2001) · PubMed · Cited by 20 · see citing works
Self-citationThe Wolbachia endosymbionts of filarial nematodes.
Bandi, C., Anderson, T., Genchi, C., & Blaxter, M. (2001) · CABI Publishing eBooks · doi:10.1079/9780851994239.0025 · Cited by 11 · see citing works
Kamoshida, S., Satoh, Y., Kamiya, S., & Tsutsumi, Y. (1999) · Pathology International · doi:10.1046/j.1440-1827.1999.00828.x · Cited by 8 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
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
The Wolbachia genome of Brugia malayi: Endosymbiont evolution within a human pathogenic \nnematode
Foster, J. M., Ganatra, M. B., Kamal, I. H., Ware, J., Makarova, K. S., Ivanova, N., Bhattacharyya, A., Kapatral, V., Kumar, S., Pósfai, J., et al. (2005) · eScholarship (California Digital Library) · Cited by 626 · see citing works
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-citationWolbachia.Bacterial Endosymbionts of Filarial Nematodes
Taylor, M. J., Bandi, C., & Hoerauf, A. M. (2005) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(05)60004-8 · Cited by 425 · see citing works
Mobile DNA in obligate intracellular bacteria
Bordenstein, S. R., & Reznikoff, W. S. (2005) · Nature Reviews Microbiology · doi:10.1038/nrmicro1233 · Cited by 192 · see citing works
Ferri, E., Bain, O., Barbuto, M., Martin, C., Lo, N. C., Uni, S., Landmann, F., Baccei, S. G., Guerrero, R., Lima, S. D. S., et al. (2011) · PLoS ONE · doi:10.1371/journal.pone.0020843 · Cited by 179 · see citing works
Self-citationBazzocchi, C., Mortarino, M., Grandi, G., Kramer, L. H., Genchi, C., Bandi, C., Genchi, M., Sacchi, L., & McCall, J. W. (2008) · International Journal for Parasitology · doi:10.1016/j.ijpara.2008.03.002 · Cited by 170 · see citing works
Self-citationAn endosymbiotic bacterium in a plant-parasitic nematode: Member of a new Wolbachia supergroup
Haegeman, A., Vanholme, B., Jacob, J., Vandekerckhove, T. T. M., Claeys, M., Borgonie, G., & Gheysen, G. (2009) · International Journal for Parasitology · doi:10.1016/j.ijpara.2009.01.006 · Cited by 170 · see citing works
Heartworm and Wolbachia: Therapeutic implications
McCall, J. W., Genchi, C., Kramer, L. H., Guerrero, J., Dzimianski, M. T., Supakorndej, P., Mansour, A., McCall, S. D., Supakorndej, N., Grandi, G., et al. (2008) · Veterinary Parasitology · doi:10.1016/j.vetpar.2008.09.008 · Cited by 111 · see citing works
Self-citationCasiraghi, M., McCall, J. W., Simoncini, L., Kramer, L. H., Sacchi, L., Genchi, C., Werren, J. H., & Bandi, C. (2002) · International Journal for Parasitology · doi:10.1016/s0020-7519(02)00158-3 · Cited by 109 · see citing works
Self-citationBreakdown of coevolution between symbiotic bacteria Wolbachia and their filarial hosts
Lefoulon, E., Bain, O., Makepeace, B. L., D’Haese, C. A., Uni, S., Martin, C., & Gavotte, L. (2016) · PeerJ · doi:10.7717/peerj.1840 · Cited by 109 · 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-citationTissue and Stage-Specific Distribution of Wolbachia in Brugia malayi
Fischer, K., Beatty, W. L., Jiang, D., Weil, G. J., & Fischer, P. (2011) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0001174 · Cited by 84 · see citing works
Grandi, G., Quintavalla, C., Mavropoulou, A., Genchi, M., Gnudi, G., Bertoni, G., & Kramer, L. (2010) · Veterinary Parasitology · doi:10.1016/j.vetpar.2010.01.025 · Cited by 78 · see citing works
Self-citationGilbert, J., Nfon, C. K., Makepeace, B. L., Njongmeta, L. M., Hastings, I. M., Pfarr, K. M., Renz, A., Tanya, V. N., & Trees, A. J. (2005) · The Journal of Infectious Diseases · doi:10.1086/462426 · Cited by 76 · see citing works
What is new in the Wolbachia/Dirofilaria interaction?
Kozek, W. J. (2005) · Veterinary Parasitology · doi:10.1016/j.vetpar.2005.02.005 · Cited by 71 · see citing works
Bazzocchi, C., Genchi, C., Paltrinieri, S., Lecchi, C., Mortarino, M., & Bandi, C. (2003) · Veterinary Parasitology · doi:10.1016/j.vetpar.2003.07.013 · Cited by 70 · see citing works
Immunopathology of Dirofilaria immitis infection
Simón, F., Kramer, L. H., Román, A., Blasini, W., Morchón, R., Marcos-Atxutegi, C., Grandi, G., & Genchi, C. (2007) · Veterinary Research Communications · doi:10.1007/s11259-006-3387-0 · Cited by 66 · see citing works
The role of endosymbioticWolbachiabacteria in filarial disease
Hise, A. G., Gillette‐Ferguson, I., & Pearlman, E. M. (2004) · Cellular Microbiology · doi:10.1046/j.1462-5822.2003.00350.x · Cited by 66 · see citing works
Exploring the transcriptome of the burrowing nematode Radopholus similis
Jacob, J., Mitreva, M., Vanholme, B., & Gheysen, G. (2008) · Molecular Genetics and Genomics · doi:10.1007/s00438-008-0340-7 · Cited by 63 · see citing works
Morchón, 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
Wolbachia surface protein (WSP) inhibits apoptosis in human neutrophils
Bazzocchi, C., Comazzi, S., Santoni, R., Bandi, C., Genchi, C., & Mortarino, M. (2006) · Parasite Immunology · doi:10.1111/j.1365-3024.2006.00915.x · Cited by 62 · see citing works
Kramer, L. H., Tamarozzi, F., Morchón, R., López-Belmonte, J. L., Marcos-Atxutegi, C., Martín-Pacho, R., & Simón, F. (2005) · Veterinary Immunology and Immunopathology · doi:10.1016/j.vetimm.2005.03.011 · Cited by 60 · see citing works
Self-citationMcCall, J. W., Kramer, L. H., Genchi, C., Guerrero, J., Dzimianski, M. T., Mansour, A., McCall, S. D., & Carson, B. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.09.023 · Cited by 58 · see citing works
Self-citationLefoulon, E., Gavotte, L., Junker, K., Barbuto, M., Uni, S., Landmann, F., Laaksonen, S., Saari, S., Nikander, S., Lima, S. D. S., et al. (2012) · International Journal for Parasitology · doi:10.1016/j.ijpara.2012.09.004 · Cited by 52 · see citing works
Self-citationLefoulon, E., Giannelli, A., Makepeace, B. L., Mutafchiev, Y., Townson, S., Uni, S., Verocai, G. G., Otranto, D., & Martin, C. (2017) · International Journal for Parasitology · doi:10.1016/j.ijpara.2016.12.009 · Cited by 50 · see citing works
Wolbachia -Induced Neutrophil Activation in a Mouse Model of Ocular Onchocerciasis (River Blindness)
Gillette‐Ferguson, I., Hise, A. G., McGarry, H. F., Turner, J. D., Esposito, A., Sun, Y., Diaconu, E., Taylor, M. J., & Pearlman, E. M. (2004) · Infection and Immunity · doi:10.1128/iai.72.10.5687-5692.2004 · Cited by 50 · see citing works
Michalski, M. L., Bain, O., Fischer, K., Fischer, P., Kumar, S., & Foster, J. M. (2010) · Journal of Parasitology · doi:10.1645/ge-2208.1 · Cited by 49 · see citing works
Is Wolbachia complicating the pathological effects of Dirofilaria immitis infections?
Kramer, L., Simón, F., Tamarozzi, F., Genchi, M., & Bazzocchi, C. (2005) · Veterinary Parasitology · doi:10.1016/j.vetpar.2005.04.011 · Cited by 44 · see citing works
Self-citationFischer, P., Schmetz, C., Bandi, C., Bonow, I., Mand, S., Fischer, K., & Büttner, D. W. (2002) · Experimental Parasitology · doi:10.1016/s0014-4894(03)00058-4 · Cited by 44 · see citing works
High infection rate of Wolbachia endobacteria in the sand flea Tunga penetrans from Brazil
Heukelbach, J., Bonow, I., Witt, L., Feldmeier, H., & Fischer, P. (2004) · Acta Tropica · doi:10.1016/j.actatropica.2004.08.005 · Cited by 39 · see citing works
Advances in Antiwolbachial Drug Discovery for Treatment of Parasitic Filarial Worm Infections
Bakowski, M. A., & McNamara, C. W. (2019) · Tropical Medicine and Infectious Disease · doi:10.3390/tropicalmed4030108 · Cited by 36 · see citing works
Detection of Wolbachia DNA in Blood for Diagnosing Filaria-Associated Syndromes in Cats
Turba, M. E., Zambon, E., Zannoni, A., Russo, S., & Gentilini, F. (2012) · Journal of Clinical Microbiology · doi:10.1128/jcm.00528-12 · Cited by 35 · see citing works
Wolbachia in Dirofilaria repens, an Agent Causing Human Subcutaneous Dirofilariasis
Grandi, G., Morchon, R., Kramer, L., Kartashev, V., & Simon, F. (2008) · Journal of Parasitology · doi:10.1645/ge-1575.1 · Cited by 33 · see citing works
Self-citationMorchón, R., Carretón, E., Grandi, G., González-Miguel, J., Montoya-Alonso, J. A., Simón, F., Genchi, C., & Kramer, L. H. (2012) · Vector-Borne and Zoonotic Diseases · doi:10.1089/vbz.2010.0211 · Cited by 30 · see citing works
Self-citationAssociation of Wolbachia with heartworm disease in cats and dogs
Dingman, P. A., Levy, J. K., Kramer, L. H., Johnson, C. M., Lappin, M. R., Greiner, E. C., Courtney, C. H., Tucker, S. J., & Morchón, R. (2010) · Veterinary Parasitology · doi:10.1016/j.vetpar.2010.01.037 · Cited by 30 · see citing works
Self-citationEffects of doxycycline on early infections of Dirofilaria immitis in dogs
McCall, J. W., Kramer, L. H., Genchi, C., Guerrero, J., Dzimianski, M. T., Supakorndej, P., Mansour, A., McCall, S. D., Supakorndej, N., Grandi, G., et al. (2011) · Veterinary Parasitology · doi:10.1016/j.vetpar.2011.01.022 · Cited by 29 · see citing works
Self-citationGarcía-Guasch, L., Caro-Vadillo, A., Manubens-Grau, J., Carretón, E., Morchón, R., Simón, F., Kramer, L. H., & Montoya-Alonso, J. A. (2013) · Veterinary Parasitology · doi:10.1016/j.vetpar.2013.01.060 · Cited by 24 · see citing works
Self-citationThe Wolbachia Genome of Brugia malayi: Endosymbiont Evolution within a Human Pathogenic Nematode
Foster, J. M., Ganatra, M. B., Kamal, I. H., Ware, J., Makarova, K. S., Ivanova, N., Bhattacharyya, A., Kapatral, V., Kumar, S., Pósfai, J., et al. (2005) · PLoS Biology · doi:10.1371/journal.pbio.0030121 · Cited by 617 · see citing works
Rhyan, J. C., Garner, M., Spraker, T. R., Lambourn, D. M., & Cheville, N. F. (2018) · Diseases of Aquatic Organisms · doi:10.3354/dao03291 · Cited by 23 · see citing works
Endosymbiotic Wolbachia of parasitic filarial nematodes as drug targets.
Rao, R. U. (2005) · PubMed · Cited by 23 · see citing works
Attout, T., Martin, C., Babayan, S. A., Kozek, W. J., Bazzocchi, C., Oudet, F., Gallagher, I. J., Specht, S., & Bain, O. (2008) · Parasitology International · doi:10.1016/j.parint.2008.01.001 · Cited by 23 · see citing works
Hise, A. G., Gillette‐Ferguson, I., & Pearlman, E. M. (2003) · Journal of Endotoxin Research · doi:10.1177/09680519030090060101 · Cited by 22 · see citing works
Interaction of a Wolbachia WSP-like protein with a nuclear-encoded protein of Brugia malayi
Melnikow, E., Xu, S., Liu, J., Li, L., Oksov, Y., Ghedin, E., Unnasch, T. R., & Lustigman, S. (2011) · International Journal for Parasitology · doi:10.1016/j.ijpara.2011.05.008 · Cited by 19 · see citing works
Thengchaisri, N., Inpankaew, T., Arthitvong, S., Steiner, J. M., & Sattasathuchana, P. (2022) · Veterinary World · doi:10.14202/vetworld.2022.239-243 · Cited by 17 · see citing works
Cytological detection ofWolbachiain squashed and paraffin embedded insect tissues
Martínez-Rodríguez, P., Castillo, P. D., & Bella, J. L. (2010) · Biotechnic & Histochemistry · doi:10.3109/10520290902903381 · Cited by 17 · see citing works
Uni, S., Udin, A. S. M., Agatsuma, T., Junker, K., Saijuntha, W., Bunchom, N., Fukuda, M., Martin, C., Lefoulon, E., Labat, A., et al. (2020) · Parasites & Vectors · doi:10.1186/s13071-020-3907-8 · Cited by 16 · see citing works
Carretón, E., Morchón, R., Falcón-Cordón, Y., Falcón-Cordón, S., Matos, J. I., & Montoya-Alonso, J. A. (2020) · Veterinary Parasitology · doi:10.1016/j.vetpar.2020.109141 · Cited by 14 · see citing works
Pfarr, K. M., HEIDER, U., Schmetz, C., Büttner, D. W., & Hoerauf, A. M. (2008) · Parasitology · doi:10.1017/s003118200700409x · Cited by 14 · see citing works
Dirofilaria spp. infection in cats from the Mediterranean basin: diagnosis and epidemiology
Carbonara, M., Perles, L., Venco, L., Gabrielli, S., Barrs, V. R., Miró, G., Papadopoulos, E., Lima, C., Bouhsira, E., Baneth, G., et al. (2025) · International Journal for Parasitology · doi:10.1016/j.ijpara.2025.01.011 · Cited by 12 · see citing works
Lau, D. C.-W., Power, R. I., & Šlapeta, J. R. (2023) · Veterinary Parasitology · doi:10.1016/j.vetpar.2023.110097 · Cited by 12 · see citing works
Neary, J. M., Trees, A. J., Ekale, D. D., Tanya, V. N., Hetzel, U., & Makepeace, B. L. (2010) · Veterinary Parasitology · doi:10.1016/j.vetpar.2010.08.031 · Cited by 11 · see citing works
Wężyk, D., Romańczuk, K., Rodo, A., Kavalevich, D., & Bajer, A. (2023) · Scientific Reports · doi:10.1038/s41598-023-29011-2 · Cited by 10 · see citing works
The gonads of Zyginidia pullula males feminized by Wolbachia pipientis
Negri, I., Franchini, A., Mandrioli, M., Mazzoglio, P. J., & Alma, A. (2008) · IRIS UNIMORE (University of Modena and Reggio Emilia) · Cited by 10 · see citing works
The emerging role of Wolbachia species in heartworm disease.
Frank, K., & Heald, R. D. (2010) · PubMed · Cited by 10 · see citing works
Uni, S., Bain, O., Suzuki, K., Agatsuma, T., Harada, M., Motokawa, M., Martin, C., Lefoulon, E., Fukuda, M., & Takaoka, H. (2012) · Parasitology International · doi:10.1016/j.parint.2012.08.004 · Cited by 10 · see citing works
Li, Z., Galvin, B. D., Raverdy, S., & Carlow, C. K. S. (2011) · Veterinary Parasitology · doi:10.1016/j.vetpar.2011.01.020 · Cited by 11 · see citing works
Voronin, D., Abeykoon, A. M. L. L., Gunawardene, Y. I. N. S., & Dassanayake, R. S. (2014) · Veterinary Parasitology · doi:10.1016/j.vetpar.2014.12.024 · Cited by 10 · see citing works
The Wolbachia Symbiont: Here, There and Everywhere
Lefoulon, E., Foster, J. M., Truchon, A. R., Carlow, C. K. S., & Slatko, B. E. (2020) · Results and problems in cell differentiation · doi:10.1007/978-3-030-51849-3_16 · Cited by 9 · see citing works
Ultrastructural analysis of Wuchereria bancrofti (Nematoda: Filarioidea) body wall
Oliveira-Menezes, A., Norões, J., Dreyer, G., & Lanfredi, R. M. (2010) · Micron · doi:10.1016/j.micron.2010.01.007 · Cited by 8 · see citing works
Uni, S., Udin, A. S. M., Tan, P. E., Rodrigues, J., Martin, C., Junker, K., Agatsuma, T., Low, V. L., Lim, Y. A. L., Saijuntha, W., et al. (2022) · Current Research in Parasitology and Vector-Borne Diseases · doi:10.1016/j.crpvbd.2022.100078 · Cited by 7 · see citing works
Molecular detection of Wolbachia endosymbiont in reptiles and their ectoparasites
Manoj, R. R. S., Latrofa, M. S., Mendoza‐Roldan, J. A., & Otranto, D. (2021) · Parasitology Research · doi:10.1007/s00436-021-07237-1 · Cited by 5 · see citing works
Wolbachia and Its Importance in Veterinary Filariasis
Kramer, L. H., McCall, J. W., Grandi, G., & Genchi, C. (2007) · KARGER eBooks · doi:10.1159/000104403 · Cited by 5 · see citing works
Self-citationLefoulon, E., Kuzmin, Y., Plantard, O., Mutafchiev, Y., Otranto, D., Martin, C., & Bain, O. (2014) · Parasitology International · doi:10.1016/j.parint.2014.07.011 · Cited by 5 · see citing works
Prevalence of the endosymbiont Wolbachia in heartworms ( Dirofilaria immitis )
Lee, S., Lee, S. K., Choi, E., & Hyun, C. (2008) · Veterinary Record · doi:10.1136/vr.163.16.484 · Cited by 4 · see citing works
Dog heartworm disease is here to stay: The most important aspects of clinical relevance
Spasojević-Kosić, L., & Lalošević, V. (2020) · Veterinarski glasnik · doi:10.2298/vetgl200928012s · Cited by 4 · see citing works
Ciancio, A. (2016) · Springer eBooks · doi:10.1007/978-94-024-0884-3_3 · Cited by 4 · see citing works
Use of in situ Hybridization to Localize Wolbachia during embryogenesis in Brugia malayi
Jiang, D., Fischer, P., & Weil, G. J. (2011) · Journal of Bacteriology & Parasitology · doi:10.4172/2155-9597.1000112 · Cited by 3 · see citing works
Cárdenas, M. Q., & Lanfredi, R. M. (2008) · Parasitology Research · doi:10.1007/s00436-008-0881-z · Cited by 3 · see citing works
McCall, J. W., Kramer, L. H., Genchi, C., Guerrero, J., Dzimianski, M. T., Mansour, A., McCall, S. D., Carson, B., & Evans, C. C. (2025) · Veterinary Parasitology · doi:10.1016/j.vetpar.2025.110568 · Cited by 1 · see citing works
Self-citationΔιροφιλαρίωση του σκύλου: παθογένεια και διάγνωση ενός πολυδιάστατου νοσήματος
ΣΙNΑΝΗΣ), T. N. S. (. Ν., KOUTINAS, C. K., Diakou, Α., & Papadopoulou, P. L. (2017) · Journal of the Hellenic Veterinary Medical Society · doi:10.12681/jhvms.15443 · Cited by 1 · see citing works
[How to fight parasitic infectious diseases with bacteria. The case of Wolbachia pipientis].
March-Rosselló, G. A., & Eirós-Bouza, J. M. (2014) · PubMed
El-Ashram, S. A., Nasr, I., Mehmood, R., Hu, M., He, L., & Suo, X. (2017) · International Journal of Advanced Research · doi:10.21474/ijar01/3599
A Light in the Dark: Uncovering Wolbachia-Host Interactions Using Fluorescence Imaging
Serbus, L. R. (2023) · Methods in molecular biology · doi:10.1007/978-1-0716-3553-7_21
The history of Wolbachia and heartworm
Vismarra, A., Fozzer, M., McCall, J. W., Genchi, M., Venco, L., García, R. M., Bazzocchi, C., Genchi, C., Kramer, L., & Bandi, C. (2026) · Parasites & Vectors · doi:10.1186/s13071-026-07397-y
Self-citationMcCall, J. W., Mansour, A., DiCosty, U., Fricks, C., McCall, S. D., Carson, B., Dzimianski, M. T., Nelson, C. T., & Moorhead, A. R. (2026) · Parasites & Vectors · doi:10.1186/s13071-026-07383-4
- Authors
- Kramer, L., Passeri, B., Corona, S., Simoncini, L., & Casiraghi, M.
- Affiliations
- University of Parma (IT)
- University of Pavia (IT)
- University of Milan (IT)
- Corresponding author
- Kramer, L.
- Venue
- Parasitology Research
- Published
- 2003-03
- Volume
- 89
- Issue
- 5
- Pages
- 381-386
- ISSN
- 0044-3255 (ISSN-L)
- 0932-0113
- 1432-1955
- OpenAlex
- W245877667
- Cited by
- 79
- References
- 25
- Citations by year
- 2026: 2 · 2025: 2 · 2023: 3 · 2022: 2 · 2021: 1 · 2020: 5 · 2019: 1 · 2018: 1 · 2017: 3 · 2016: 2 · 2014: 4 · 2013: 1 · 2012: 4
- FWCI
- 3.30
- Type
- journal article
- Language
- en
- Open access
- closed
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Parasitology Research (publishedVersion)
- PubMed (publishedVersion)
- Funders
- Ministero dell’Istruzione, dell’Università e della Ricerca
- Topics
- Health Sciences › Medicine › Infectious Diseases › Parasitic Diseases Research and Treatment
- Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect symbiosis and bacterial influences
- Life Sciences › Immunology and Microbiology › Parasitology › Parasites and Host Interactions
- Keywords
- Wolbachia, Dirofilaria immitis, Brugia pahangi, Wolbachia surface protein, endosymbionts, filarial nematodes, intracellular bacteria, vertical transmission, tetracycline therapy, polyclonal antibodies, immunogold labeling, heartworm disease
- MeSH terms
- Animals, Antibodies, Bacterial, Antigens, Bacterial, Bacterial Outer Membrane Proteins, Dirofilaria immitis, Dirofilariasis, Dogs, Doxycycline, Female, Gerbillinae, Immunohistochemistry, Male, Symbiosis, Microscopy, Immunoelectron, Brugia pahangi, Wolbachia
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
