Assessment of the safety and efficacy of an oral probiotic-based vaccine against Aspergillus infection in captive-bred Humboldt penguins (Spheniscus humboldti)

Thorel, Milan; Mateos-Hernandez, Lourdes; Mulot, Baptiste; Azzouni, Mouna Naila; Hodžić, Adnan; Gaillot, Hugues; Ruel, Yannick; Desoubeaux, Guillaume; Delaye, Jean-Baptiste; Obregon, Dasiel; Wu-Chuang, Alejandra; de la Fuente, José; Bermúdez-Humarán, Luis G.; Risco-Castillo, Veronica; Leclerc, Antoine; Cabezas-Cruz, Alejandro

doi:10.3389/fimmu.2022.897223

Cited by 12Antifungal resistance and susceptibilityAquaculture disease management and microbiotaMicrobial infections and disease research

Assessment of the safety and efficacy of an oral probiotic-based vaccine against Aspergillus infection in captive-bred Humboldt penguins (Spheniscus humboldti)

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Thorel, Milan, Mateos-Hernandez, Lourdes, Mulot, Baptiste, Azzouni, Mouna Naila, Hodžić, Adnan, Gaillot, Hugues, Ruel, Yannick, Desoubeaux, Guillaume +8 more·2022·Frontiers in Immunology

DOI 10.3389/fimmu.2022.897223PMC PMC9137413

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Abstract

Aspergillosis is a fungal infection caused mainly by Aspergillus fumigatus that often results in respiratory disease in birds. Aspergillosis is a major cause of morbidity and mortality in captive-bred penguin species. Currently, there is no registered vaccine to prevent aspergillosis. Recent research demonstrated that oral administration of gram-negative bacteria expressing high levels of galactose-α-1,3-galactose (α-Gal) modulates anti-α-Gal immunity and protects turkeys from clinical aspergillosis caused by experimental A. fumigatus infection. The role of anti-α-Gal immunity in penguins has not been studied. Here, we tested the distribution of α-1,3-galactosyltransferase (α1,3GT) genes in the fecal microbiome of Humboldt penguins (Spheniscus humboldti). The occurrence of natural anti-α-Gal antibodies (Abs) in sera and eggs of healthy Humboldt penguins was also assessed. A trial was then conducted to test whether oral administration of Escherichia coli Nissle, expressing high α-Gal levels, modulates anti-α-Gal immunity in a colony of Humboldt penguins. Animals in the vaccination and placebo groups were evaluated before the trial and followed for one year for aspergillosis detection using a diagnostic panel including computed tomography scans, capillary zone electrophoresis, 3-hydroxybutyrate levels, and anti-A. fumigatus Abs. Anti-α-Gal Abs were detected in sera (IgM and IgY) and eggs (IgY) of healthy penguins. Microbiota analysis and functional predictions revealed the presence of α1,3GT genes in the microbiota of Humboldt penguins and other penguin species. A strong decrease in anti-α-Gal IgM levels was observed in all animals in the placebo group three months after vaccination protocol. This decrease was not observed in E. coli Nissle-treated penguins. After the vaccination protocol, we found a positive correlation between anti-E. coli IgY and anti-α-Gal IgY in the E. coli Nissle group, suggesting a correlation between the presence of the bacteria and these Abs. During the study period, three penguins exhibited respiratory signs consistent with aspergillosis. Two were from the placebo group whose symptoms resolved with specific treatments, while a single vaccinated individual developed fatal respiratory aspergillosis eight months after the trial. We conclude that E. coli Nissle represents a safe potential probiotic with a protective effect against aspergillosis in Humboldt penguins that deserves to be further explored for therapeutic uses in these animals.

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New technologies such as diagnosis with image analysis, plasma biomarkers, and probiotic-based vaccination might be useful in reducing the incidence of aspergillosis among penguins.
“New technologies, such as diagnosis with image analysis [25,27], plasma biomarkers [38], and probiotic-based vaccination [39], might be useful in reducing the incidence of aspergillosis among penguins.”
From Nationwide Survey about the Occurrence of Aspergillosis in Captive Penguins in Zoos and Aquariums in Japan (2023) · cites this paper as [39]

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KEGG: Kyoto Encyclopedia of Genes and Genomes
Kanehisa, M. (2000) · Nucleic Acids Research · doi:10.1093/nar/28.1.27 · Cited by 37,077 · see citing works
DADA2: High–resolution sample inference from Illumina amplicon data
Callahan, B. J., McMurdie, P. J., Rosen, M. J., Han, A. W., Johnson, A. J. A., & Holmes, S. P. (2016) · Nature Methods · doi:10.1038/nmeth.3869 · Cited by 35,698 · see citing works
KEGG: Kyoto Encyclopedia of Genes and Genomes
Ogata, H., Goto, S., Sato, K., Fujibuchi, W., Bono, H., & Kanehisa, M. (1999) · Nucleic Acids Research · doi:10.1093/nar/27.1.29 · Cited by 31,232 · see citing works
Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2
Bolyen, E., Rideout, J. R., Dillon, M. R., Bokulich, N. A., Abnet, C. C., Al-Ghalith, G. A., Alexander, H., Alm, E. J., Arumugam, M., Asnicar, F., et al. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0209-9 · Cited by 23,742 · see citing works
PICRUSt2 for prediction of metagenome functions
Douglas, G. M., Maffei, V. J., Zaneveld, J., Yurgel, S. N., Brown, J. R., Taylor, C. M., Huttenhower, C., & Langille, M. G. I. (2020) · Nature Biotechnology · doi:10.1038/s41587-020-0548-6 · Cited by 6,815 · see citing works
Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin
Bokulich, N. A., Kaehler, B. D., Rideout, J. R., Dillon, M. R., Bolyen, E. K., Knight, R. D., Huttley, G. A., & Caporaso, J. G. (2018) · Microbiome · doi:10.1186/s40168-018-0470-z · Cited by 5,873 · see citing works
circlize implements and enhances circular visualization in R
Gu, Z., Gu, L., Eils, R., Schlesner, M., & Brors, B. (2014) · Bioinformatics · doi:10.1093/bioinformatics/btu393 · Cited by 4,290 · see citing works
The Sequence Read Archive
Leinonen, R., Sugawara, H., & Shumway, M. F. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkq1019 · Cited by 2,760 · see citing works
Uniting the classification of cultured and uncultured bacteria and archaea using 16S rRNA gene sequences
Yarza, P., Yilmaz, P., Pruesse, E., Glöckner, F. O., Ludwig, W., SCHLEIFER, K. H., Whitman, W. B., Euzéby, J. P., Amann, R., & Rossello-Mora, R. A. (2014) · Nature Reviews Microbiology · doi:10.1038/nrmicro3330 · Cited by 2,563 · see citing works
Interaction between human natural anti-alpha-galactosyl immunoglobulin G and bacteria of the human flora
Galili, U., Mandrell, R. E., Hamadeh, R. M., Shohet, S., & Griffiss, J. M. (1988) · Infection and Immunity · doi:10.1128/iai.56.7.1730-1737.1988 · Cited by 549 · see citing works
Gut Microbiota Elicits a Protective Immune Response against Malaria Transmission
Yılmaz, B., Portugal, S., Tran, T. M., Gozzelino, R., Ramos, S., Gomes, J., Regalado, A. P., Cowan, P. J., d’Apice, A. J. F., Chong, A. S., et al. (2014) · Cell · doi:10.1016/j.cell.2014.10.053 · Cited by 352 · see citing works
Blood group isoantibody stimulation in man by feeding blood group-active bacteria
Springer, G. F., & Horton, R. E. (1969) · Journal of Clinical Investigation · doi:10.1172/jci106094 · Cited by 321 · see citing works
Maternal transfer of antibodies in vertebrates: trans-generational effects on offspring immunity
Hasselquist, D., & Nilsson, J. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2008.0137 · Cited by 315 · see citing works
Lytic anti- α -galactosyl antibodies from patients with chronic Chagas' disease recognize novel O -linked oligosaccharides on mucin-like glycosyl-phosphatidylinositol-anchored glycoproteins of Trypanosoma cruzi
de Almeida, I. C., Ferguson, M. A. J., Schenkman, S., & Travassos, L. R. (1994) · Biochemical Journal · doi:10.1042/bj3040793 · Cited by 230 · see citing works
Aspergillusinfections in birds: a review
Beernaert, L. A., Pasmans, F., Waeyenberghe, L. V., Haesebrouck, F., & Martel, A. (2010) · Avian Pathology · doi:10.1080/03079457.2010.506210 · Cited by 206 · see citing works
ORIGIN OF ANTI-HUMAN BLOOD GROUP B AGGLUTININS IN WHITE LEGHORN CHICKS
Springer, G. F., Horton, R. E., & Forbes, M. (1959) · The Journal of Experimental Medicine · doi:10.1084/jem.110.2.221 · Cited by 169 · see citing works
Complement-mediated lysis of Trypanosoma cruzi trypomastigotes by human anti-alpha-galactosyl antibodies
de Almeida, I. C., Milani, S. R., Gorin, P. A. J., & Travassos, L. R. (1991) · The Journal of Immunology · doi:10.4049/jimmunol.146.7.2394 · Cited by 157 · see citing works
Interspecific variations in the gastrointestinal microbiota in penguins
Dewar, M., Arnould, J. P. Y., Dann, P., Trathan, P. N., Groscolas, R., & Smith, S. (2013) · MicrobiologyOpen · doi:10.1002/mbo3.66 · Cited by 116 · see citing works
Intestinal immunity ofEscherichia coliNISSLE 1917: a safe carrier for therapeutic molecules
Westendorf, A. M., Gunzer, F., Deppenmeier, S., Tapadar, D., Hunger, J. K., Schmidt, M. A., Buer, J., & Bruder, D. (2004) · FEMS Immunology & Medical Microbiology · doi:10.1016/j.femsim.2004.10.023 · Cited by 94 · see citing works
Effect of blood type on anti-α-Gal immunity and the incidence of infectious diseases
Cabezas‐Cruz, A., Mateos‐Hernández, L., Alberdi, P., Villar, M., Riveau, G. J., Hermann, E., Schacht, A., Khalife, J., Correia‐Neves, M., Gortázar, C., et al. (2017) · Experimental & Molecular Medicine · doi:10.1038/emm.2016.164 · Cited by 92 · see citing works
Self-citation
The diagnosis of aspergillosis in birds
Jones, M. P., & Orosz, S. E. (2000) · Seminars in Avian and Exotic Pet Medicine · doi:10.1053/ax.2000.4619 · Cited by 82 · see citing works
Application of Galactomannan Analysis and Protein Electrophoresis in the Diagnosis of Aspergillosis in Avian Species
Cray, C., Watson, T., Rodriguez, M., & Arheart, K. L. (2009) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2007-0138.1 · Cited by 78 · see citing works
Induction of Cytolytic Anti-Gal Antibodies in α-1,3-Galactosyltransferase Gene Knockout Mice by Oral Inoculation withEscherichia coliO86:B7 Bacteria
Posekany, K. J., Pittman, H. K., Bradfield, J. F., Haisch, C. E., & Verbanac, K. M. (2002) · Infection and Immunity · doi:10.1128/iai.70.11.6215-6222.2002 · Cited by 77 · see citing works
Aspergillosis in Wild Birds
Arné, P., Risco‐Castillo, V., Jouvion, G., Barzic, C. L., & Guillot, J. (2021) · Journal of Fungi · doi:10.3390/jof7030241 · Cited by 77 · see citing works
Self-citation
Removal of bowel aerobic gram‐negative bacteria is more effective than immunosuppression with cyclophosphamide and steroids to decrease natural α‐Galactosyl IgG antibodies
Máñez, R., Blanco, F. J., Díaz, I., Centeno, A., López-Peláez, E., Hermida, M., DAVIES, H. F. S., & Katopodis, A. G. (2001) · Xenotransplantation · doi:10.1034/j.1399-3089.2001.00082.x · Cited by 76 · see citing works
Aspergillosis: a limiting factor during recovery of captive magellanic penguins
Xavier, M. O., Soares, M. P., Meinerz, A. R. M., Nobre, M. D. O., Osório, L. G., Filho, R. P. D. S., & Meireles, M. C. A. (2007) · Brazilian Journal of Microbiology · doi:10.1590/s1517-83822007000300018 · Cited by 71 · see citing works
Untitled work
(1990) · PubMed · Cited by 56 · see citing works
Distribution of Bacterial α1,3-Galactosyltransferase Genes in the Human Gut Microbiome
Montassier, E., Al‐Ghalith, G. A., Mathé, C., Bastard, Q. L., Douillard, V., Garnier, A., Guimon, R., Raimondeau, B., Touchefeu, Y., Duchalais, É., et al. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2019.03000 · Cited by 54 · see citing works
Galactomannan Assay and Plasma Protein Electrophoresis Findings in Psittacine Birds With Aspergillosis
Cray, C., Reavill, D. R., Romagnano, A., Sant, F. V., Champagne, D., Stevenson, R., Rolfe, V., Griffin, C., & Clubb, S. L. (2009) · Journal of Avian Medicine and Surgery · doi:10.1647/2007-041.1 · Cited by 54 · see citing works
Polyclonal Aspergillus fumigatus infection in captive penguins
Alvarez-Perez, S., Mateos, A., Dominguez, L., Martinez-Nevado, E., Blanco, J. L., & Garcia, M. E. (2010) · Veterinary Microbiology · doi:10.1016/j.vetmic.2010.02.026 · Cited by 52 · see citing works
An α-Gal-containing neoglycoprotein-based vaccine partially protects against murine cutaneous leishmaniasis caused by Leishmania major
Iniguez, E., Schocker, N. S., Subramaniam, K. S., Portillo, S., Montoya, A. L., Al-Salem, W. S., Torres, C. L., Rodriguez, F., Moreira, O. C., Acosta-Serrano, Á., et al. (2017) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0006039 · Cited by 51 · see citing works
Transthyretin: From Structural Stability to Osteoarticular and Cardiovascular Diseases
Wieczorek, E., & Ożyhar, A. (2021) · Cells · doi:10.3390/cells10071768 · Cited by 49 · see citing works
α-Gal-Based Vaccines: Advances, Opportunities, and Perspectives
Hodžić, A., Mateos‐Hernández, L., de la Fuente, J., & Cabezas‐Cruz, A. (2020) · Trends in Parasitology · doi:10.1016/j.pt.2020.08.001 · Cited by 48 · see citing works
Self-citation
Evaluation of Oral Itraconazole Administration in Captive Humboldt Penguins (Spheniscus humboldti)
Bunting, E. M., Abou‐Madi, N., COX, S. K., Martín‐Jiménez, T., Fox, H., & Kollias, G. V. (2009) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2009-0045.1 · Cited by 48 · see citing works
Serologic and Plasma Protein Electrophoretic Findings in 7 Psittacine Birds With Aspergillosis
Ivey, E. S. (2000) · Journal of Avian Medicine and Surgery · doi:10.1647/1082-6742(2000)014[0103:sappef]2.0.co;2 · Cited by 48 · see citing works
Serosurvey and Diagnostic Application of Antibody Titers to Aspergillus in Avian Species
Cray, C., Watson, T., & Arheart, K. L. (2009) · Avian Diseases · doi:10.1637/8673-030209-reg.1 · Cited by 47 · see citing works
Gut Microbiota Abrogates Anti-α-Gal IgA Response in Lungs and Protects against Experimental Aspergillus Infection in Poultry
Mateos-Hernández, L., Risco-Castillo, V., Torres-Maravilla, E., Bermúdez-Humarán, L. G., Alberdi, P., Hodžić, A., Hernández-Jarguin, A., Rakotobe, S., Galon, C., Devillers, E., et al. (2020) · Vaccines · doi:10.3390/vaccines8020285 · Cited by 46 · see citing works
Self-citation
The Formation of Glycan-Specific Natural Antibodies Repertoire in GalT-KO Mice Is Determined by Gut Microbiota
Bello‐Gil, D., Audebert, C., Olivera‐Ardid, S., Pérez-Cruz, M., Even, G., Khasbiullina, N. R., Gantois, N., Shilova, N. V., Merlin, S., Costa, C., et al. (2019) · Frontiers in Immunology · doi:10.3389/fimmu.2019.00342 · Cited by 45 · see citing works
Diagnostic Procedures and Available Techniques for the Diagnosis of Aspergillosis in Birds
Fischer, D., & Lierz, M. (2015) · Journal of Exotic Pet Medicine · doi:10.1053/j.jepm.2015.06.016 · Cited by 43 · see citing works
IgY antiporcine endothelial cell antibodies effectively block human antiporcine xenoantibody binding
FRYER, J. P., Firca, J. R., Leventhal, J. R., Blondie, B., Malcolm, A. J., Ivancic, D. Z., Gandhi, R. T., Shah, A. H., Pao, W. C., Abecassis, M. M., et al. (1999) · Xenotransplantation · doi:10.1034/j.1399-3089.1999.00015.x · Cited by 42 · see citing works
The Airway Pathobiome in Complex Respiratory Diseases: A Perspective in Domestic Animals
Mach, N., Baranowski, É., Nouvel, L., & Citti, C. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.583600 · Cited by 41 · see citing works
Immunity to α-Gal: Toward a Single-Antigen Pan-Vaccine To Control Major Infectious Diseases
Cabezas‐Cruz, A., & de la Fuente, J. (2017) · ACS Central Science · doi:10.1021/acscentsci.7b00517 · Cited by 39 · see citing works
Self-citation
Transthyretin Stimulates Tumor Growth through Regulation of Tumor, Immune, and Endothelial Cells
Lee, C., Ding, X., Zhao, T., Wu, L., Perkins, S. M., Du, H., & Yan, C. (2018) · The Journal of Immunology · doi:10.4049/jimmunol.1800736 · Cited by 38 · see citing works
Pharmacokinetics of Orally Administered Terbinafine in African Penguins (Spheniscus demersus) for Potential Treatment of Aspergillosis
Bechert, U. S., Christensen, J. M., Poppenga, R. H., Le, H., Wyatt, J., & Schmitt, T. L. (2010) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2009-0211r.1 · Cited by 37 · see citing works
VORICONAZOLE TOXICITY IN MULTIPLE PENGUIN SPECIES
Hyatt, M. W., Georoff, T. A., Nollens, H. H., Wells, R. L., Clauss, T. M., Ialeggio, D. M., Harms, C. A., & Wack, A. N. (2015) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2015-0128.1 · Cited by 36 · see citing works
Aspergillus spp. seropositivity in New Zealand penguins
Graczyk, T. K., & Cockrem, J. F. (1995) · Mycopathologia · doi:10.1007/bf01102898 · Cited by 36 · see citing works
Comparison of Diagnostic Tools for the Detection of Aspergillosis in Blood Samples of Experimentally Infected Falcons
Fischer, D., Waeyenberghe, L. V., Cray, C., Gross, M., Usleber, E., Pasmans, F., Martel, A., & Lierz, M. (2014) · Avian Diseases · doi:10.1637/10831-032714-reg · Cited by 35 · see citing works
Effects of Adjuvant-Augmented Germling Vaccines in Turkey Poults Challenged with Aspergillus fumigatus
Richard, J. L., Peden, W. M., & Sacks, J. M. (1991) · Avian Diseases · doi:10.2307/1591300 · Cited by 34 · see citing works
Effects of Compounding on Pharmacokinetics of Itraconazole in Black-Footed Penguins (Spheniscus demersus)
Smith, J. A. J., Papich, M. G., Russell, G., & Mitchell, M. A. (2010) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2010-0019.1 · Cited by 33 · see citing works
Probiotic Bacteria with High Alpha-Gal Content Protect Zebrafish against Mycobacteriosis
Pacheco, I., Sanchez, S. D., Contreras, M., Villar, M., Cabezas‐Cruz, A., Gortázar, C., & de la Fuente, J. (2021) · Pharmaceuticals · doi:10.3390/ph14070635 · Cited by 33 · see citing works
Self-citation
Development of an indirect ELISA for the detection of serum antibodies to Aspergillus fumigatus in captive penguins
German, A. J., Flach, E. J., Shankland, G. S., & Edwards, J. (2002) · Veterinary Record · doi:10.1136/vr.150.16.513 · Cited by 30 · see citing works
Prealbumin as a Predictor of Prognosis in Patients With Coronavirus Disease 2019
Luo, Y., Xue, Y., Mao, L., Xu, Y., Lin, Q., Tang, G., Song, H., Wang, F., & Sun, Z. (2020) · Frontiers in Medicine · doi:10.3389/fmed.2020.00374 · Cited by 29 · see citing works
Transthyretin is an inhibitor of monocyte and endothelial cell interleukin-1 production
Borish, L., King, M. S., Mascali, J. J., Johnson, S. M., Coll, B., & Rosenwasser, L. J. (1992) · Inflammation · doi:10.1007/bf00918973 · Cited by 28 · see citing works
Fluorescence immunoassay of E. coli using anti-lipopolysaccharide antibodies isolated from human serum
Bong, J.-H., Kim, J., Lee, G.-Y., Park, J.-H., Kim, T., Kang, M., & Pyun, J. (2018) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2018.10.036 · Cited by 28 · see citing works
Immunity to α-Gal: The Opportunity for Malaria and Tuberculosis Control
Cabezas‐Cruz, A., & de la Fuente, J. (2017) · Frontiers in Immunology · doi:10.3389/fimmu.2017.01733 · Cited by 27 · see citing works
Self-citation
APPLICATION OF 3-HYDROXYBUTYRATE MEASUREMENT AND PLASMA PROTEIN ELECTROPHORESIS IN THE DIAGNOSIS OF ASPERGILLOSIS IN AFRICAN PENGUINS ( <i>SPHENISCUS DEMERSUS</i> )
Desoubeaux, G., Rodriguez, M., Bronson, E., Sirpenski, G., & Cray, C. (2018) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2017-0172.1 · Cited by 27 · see citing works
A standardized quantitative method for detecting remnant alpha-Gal antigen in animal tissues or animal tissue-derived biomaterials and its application
Lu, Y., Shao, A., Shan, Y., Zhao, H.-N., Leiguo, M., Zhang, Y., Tang, Y., Zhang, W., Jin, Y. J., & Xu, L. (2018) · Scientific Reports · doi:10.1038/s41598-018-32959-1 · Cited by 27 · see citing works
Serum Protein Electrophoresis by Using High-resolution Agarose Gel in Clinically Healthy andAspergillusSpecies-infected Falcons
Kummrow, M., Silvanose, C., Somma, A., Bailey, T. A., & Vorbrüggen, S. (2012) · Journal of Avian Medicine and Surgery · doi:10.1647/2011-006r1.1 · Cited by 24 · see citing works
INCIDENCE DENSITY, PROPORTIONATE MORTALITY, AND RISK FACTORS OF ASPERGILLOSIS IN MAGELLANIC PENGUINS IN A REHABILITATION CENTER FROM BRAZIL
Filho, R. P. D. S., Xavier, M. O., Martins, A. M., Ruoppolo, V., Mendoza-Sassi, R. A., Adornes, A. C., Cabana, Â. L., & Meireles, M. C. A. (2015) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2013-0092.1 · Cited by 23 · see citing works
Sphenisciformes (Penguins)
Wallace, R. S. (2014) · Elsevier eBooks · doi:10.1016/b978-1-4557-7397-8.00010-4 · Cited by 23 · see citing works
Comparison of air sac volume, lung volume, and lung densities determined by use of computed tomography in conscious and anesthetized Humboldt penguins (Spheniscus humboldti) positioned in ventral, dorsal, and right lateral recumbency
Nevitt, B. N., Langan, J. N., Adkesson, M. J., Mitchell, M. A., Henzler, M. A., & Drees, R. (2014) · American Journal of Veterinary Research · doi:10.2460/ajvr.75.8.739 · Cited by 22 · see citing works
Control of vector-borne infectious diseases by human immunity against α-Gal
Cabezas‐Cruz, A., Valdés, J. J., & de la Fuente, J. (2016) · Expert Review of Vaccines · doi:10.1080/14760584.2016.1181547 · Cited by 19 · see citing works
Self-citation
Exploring the Ecological Implications of Microbiota Diversity in Birds: Natural Barriers Against Avian Malaria
Palinauskas, V., Mateos‐Hernández, L., Chuang, A. W., de la Fuente, J., Aželytė, J., Obregón, D., & Cabezas‐Cruz, A. (2022) · Frontiers in Immunology · doi:10.3389/fimmu.2022.807682 · Cited by 19 · see citing works
Self-citation
Sphenisciformes, Gaviiformes, Podicipediformes, Procellariiformes, and Pelecaniformes
Stidworthy, M. F., & Denk, D. (2018) · Elsevier eBooks · doi:10.1016/b978-0-12-805306-5.00027-4 · Cited by 19 · see citing works
Plasma protein electrophoresis as a prognostic indicator in Aspergillus species‐infected Gentoo penguins (Pygoscelis papua papua)
Naylor, A. D., Girling, S. J., Brown, D., Crompton, C. G., & Pizzi, R. (2017) · Veterinary Clinical Pathology · doi:10.1111/vcp.12527 · Cited by 18 · see citing works
Simple purification methods for an αgalactose-specific antibody from chicken eggs
Cook, C. L., Pao, W. C., Firca, J. R., Anderson, B., & Fryer, J. P. (2001) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(01)80139-0 · Cited by 18 · see citing works
ENVIRONMENTAL FUNGAL LOADS IN AN INDOOR–OUTDOOR AFRICAN PENGUIN (SPHENISCUS DEMERSUS) EXHIBIT
Rivas, A. E., Dykstra, M. J., Kranz, K. R., & Bronson, E. (2018) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2017-0119.1 · Cited by 17 · see citing works
Characterization of a polyclonal anti-Galα1-3Gal antibody from chicken
Bouhours, J., Richard, C., Ruvoën‐Clouet, N., Barreau, N., Naulet, J., & Bouhours, D. (1998) · Glycoconjugate Journal · doi:10.1023/a:1006903919461 · Cited by 17 · see citing works
Low rate of azole resistance in cases of avian aspergillosis in Germany
Barber, A. E., Scheufen, S., Walther, G., Kurzai, O., & Schmidt, V. (2020) · Medical Mycology · doi:10.1093/mmy/myaa045 · Cited by 16 · see citing works
A retrospective analysis of mortality in captive Magellanic penguins (Spheniscus magellanicus) in the United States, 2008–2018
Krol, L., Moore, R. P., Mutlow, A. G., Brady, S. M., & Dorsa, D. (2020) · Zoo Biology · doi:10.1002/zoo.21561 · Cited by 14 · see citing works
Autopsy imaging for aspergillosis in King Penguin, an economically valuable zoo animal
YAMADA, K., Toyotome, T., Matsumoto, N., & Itoh, M. (2020) · Journal of Veterinary Medical Science · doi:10.1292/jvms.19-0431 · Cited by 13 · see citing works
RETROSPECTIVE STUDY OF MORBIDITY AND MORTALITY OF AFRICAN PENGUINS (SPHENISCUS DEMERSUS) UNDER MANAGED CARE IN NORTH AMERICA: 2007–2018
Trumpp, K. M., Sander, S. J., Sander, W., Zimmerman, D. M., & Bronson, E. (2021) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2020-0224 · Cited by 11 · see citing works
THE ISOLATION AND ANTIMICROBIAL SENSITIVITY OF ASPERGILLUS FUMIGATUS FROM FROZEN RESPIRATORY TISSUES OF PENGUINS FROM ZOOLOGICAL COLLECTIONS IN THE UNITED KINGDOM, 2007–2018
Reed, K., Macgregor, S. K., Stidworthy, M. F., Denk, D., & Guthrie, A. L. (2020) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2019-0160 · Cited by 11 · see citing works
Aspergillosis in the Peruvian Penguin (Spheniscus humboldti)
Nakeeb, S. M., Babus, B., & Clifton, A. Y. (1981) · The Journal of Zoo Animal Medicine · doi:10.2307/20094516 · Cited by 11 · see citing works
Distribution of, and immune response to, chicken anti‐αGal immunoglobulin Y antibodies in wild‐type and αGal knockout mice
Walsh, W. E., Anderson, B. E., Ivancic, D. Z., Zhang, Z., Piccini, J. P., Rodgers, T., Pao, W. C., & Fryer, J. P. (2000) · Immunology · doi:10.1046/j.1365-2567.2000.00136.x · Cited by 10 · see citing works
Molecular epidemiology of aspergillosis in Magellanic penguins and susceptibility patterns of clinical isolates
Melo, A. M., Poester, V. R., Canabarro, P. L., Sampaio, D. A., Stevens, D. A., Veríssimo, C., Sabino, R., & Xavier, M. O. (2021) · Medical Mycology · doi:10.1093/mmy/myab040 · Cited by 10 · see citing works
STANDING COMPUTED TOMOGRAPHY IN NONANESTHETIZED LITTLE PENGUINS (EUDYPTULA MINOR) TO ASSESS RESPIRATORY SYSTEM ANATOMY AND MONITOR DISEASE
Rivas, A. E., Fischetti, A. J., Roux, A. B. L., & Hollinger, C. (2019) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2018-0189 · Cited by 9 · see citing works
Characteristic imaging findings of the respiratory system in penguins with suspected aspergillosis in an aquarium
ITOH, M., TOYOTOME, T., MATSUMOTO, N., OKAMOTO, M., WATANABE, K.-I., & YAMADA, K. (2020) · Journal of Veterinary Medical Science · doi:10.1292/jvms.20-0129 · Cited by 9 · see citing works
Human prealbumin fraction: Effects on cell-mediated immunity and tumor rejection
Leung, K. H., Ehrke, M. J., Bercsenyi, K., & Mihich, E. (1982) · Immunopharmacology · doi:10.1016/0162-3109(82)90025-x · Cited by 9 · see citing works
Capillary Electrophoresis Assessment of Plasma Protein Changes in an African Penguin ( Spheniscus demersus ) With Aspergillosis
Valdivia, A. O., Ortega, K. J., Bhattacharya, S. K., & Cray, C. (2020) · ACS Omega · doi:10.1021/acsomega.0c04983 · Cited by 8 · see citing works
Applicability of the Platelia EIA® Aspergillus test for the diagnosis of aspergilosis in penguins
Cabana, Â. L., Xavier, M. O., Mendes, J. F., Teles, A. J., Martins, A. M., da Silva-Filho, R. P., & Meireles, M. C. A. (2018) · Brazilian Journal of Biology · doi:10.1590/1519-6984.171140 · Cited by 8 · see citing works
Preliminary Pilot Study of Itraconazole After a Single Oral Dose of a Veterinary Formulation Solution in African Penguins (Spheniscus demersus)
Zalesak, S. M., Sánchez, C. R., Pich, A. A., & Papich, M. G. (2020) · Journal of Avian Medicine and Surgery · doi:10.1647/1082-6742-34.1.52 · Cited by 8 · see citing works
APPLICATION OF A NOVEL ASPERGILLUS LATERAL-FLOW DEVICE IN THE DIAGNOSIS OF ASPERGILLOSIS IN CAPTIVE GENTOO PENGUINS (PYGOSCELIS PAPUA PAPUA)
Mota, S. M., Girling, S. J., Cole, G. C., Brown, D., Johnson, G. L., & Naylor, A. D. (2023) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2021-0158 · Cited by 6 · see citing works
DIAGNOSIS AND MANAGEMENT OF MYCOBACTERIOSIS IN A COLONY OF LITTLE PENGUINS (EUDYPTULA MINOR)
Rivas, A. E., & Hollinger, C. (2019) · Journal of Zoo and Wildlife Medicine · doi:10.1638/2018-0190 · Cited by 6 · see citing works
Simple Purification Methods for an .ALPHA.Galactose-Specific Antibody from Chicken Eggs.
COOK, C. L., Pao, W. C., Firca, J. R., Anderson, B., & FRYER, J. P. (2001) · Journal of Bioscience and Bioengineering · doi:10.1263/jbb.91.305 · Cited by 5 · see citing works
Serological monitoring of antibodies for an early diagnosis ofaspergillosis in captive penguins
Cabana, Â. L., Xavier, M. O., Poester, V. R., Klafke, G. B., B.Filho, P. L., Martins, A. M., Filho, R. P. S., & Meireles, M. C. A. (2015) · Pesquisa Veterinária Brasileira · doi:10.1590/s0100-736x2015000600015 · Cited by 4 · see citing works
[Levels of anti-Gal antibodies in persons infected and non-infected with Trypanosoma cruzi. Probably induced by bacteria and by the parasite].
González, J., Ramírez, C., Seguel, X., Gutiérrez, B., Manque, P., Porcile, P., Neira, I., & Sagua, H. (1995) · PubMed · Cited by 3 · see citing works
Avian Medicine, 3rd edition
Howse, S. (2017) · Europe PMC (PubMed Central) · Cited by 1 · see citing works

Flagged first, then by citations

Research works printed but not linked: 4

[4]Redig PT. Avian Aspergillosis. In: Fowler ME, editor. Zoo and Wild Animal Medicine Current Therapy 3 in Philadelphia. PA, USA: WB Saunders (1993). p. 178– 218.
[10]Thompson R Wolf T Rasmussen J. Aspergillosis in African Penguins (Spheniscus demersus). In: Understanding Diagnostic Criteria, Treatment, and Prophylaxis. In Proceedings of the IAAAM Conference. San Francisco, USA (2013).
[59]Meredith A. Prophylactic Administration of Itraconazole for the Control of Aspergillosis in Gentoo Penguins (Pygoscelis Papua)s. In: The 4th Conference of the European Committee of the Association of Avian Veterinarians. London, UK (1997) p. 227s.
[86]Kostka V Janeczek F. Diagnostic of Protein Electrophoresis in Large Psittacines - A Review of 30 Cases. In: Proceedings of the 1st ICARE Conference. Wiesbaden, Germany (2013).

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Authors: Thorel, M., Mateos-Hernandez, L., Mulot, B., Azzouni, M. N., Hodžić, A., Gaillot, H., Ruel, Y., Desoubeaux, G., Delaye, J.-B., Obregon, D., Wu-Chuang, A., de la Fuente, J., Bermúdez-Humarán, L. G., Risco-Castillo, V., Leclerc, A., & Cabezas-Cruz, A.
Affiliations: École Nationale Vétérinaire d'Alfort (FR)
University of Veterinary Medicine Vienna (AT)
Centre Hospitalier Universitaire de Tours (FR)
Corresponding author: Thorel, Milan
ORCID: Thorel, Milan
Mulot, Baptiste
Hodžić, Adnan
Gaillot, Hugues
Ruel, Yannick
Delaye, Jean-Baptiste
Leclerc, Antoine
Venue: Frontiers in Immunology
Publisher: Frontiers Media SA
Published: 2022-05-13
Volume: 13
Pages: 897223-897223
ISSN: 1664-3224 (ISSN-L)
DOI: 10.3389/fimmu.2022.897223
PMC: PMC9137413
OpenAlex: W4280504666
Cited by: 11
References: 88
Citations by year: 2026: 1 · 2025: 2 · 2024: 3 · 2023: 5
FWCI: 1.22
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Frontiers in Immunology (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
HAL (submittedVersion, other-oa)
DIGITAL.CSIC (Spanish National Research Council (CSIC)) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
RUIdeRA - Institutional University Repository (University of Castilla-La Mancha) (submittedVersion, other-oa)
Funders: Agence Nationale de la Recherche
Topics: Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
Life Sciences › Immunology and Microbiology › Immunology › Aquaculture disease management and microbiota
Life Sciences › Immunology and Microbiology › Microbiology › Microbial infections and disease research
Keywords: aspergillosis, Aspergillus fumigatus, Humboldt penguin, galactose-alpha-1,3-galactose, Escherichia coli Nissle, fecal microbiota, captive-bred birds, respiratory diseases, vaccine safety and efficacy, anti-Aspergillus antibodies
MeSH terms: Animals, Aspergillosis, Escherichia coli, Galactose, Immunoglobulin M, Vaccines, Probiotics, Spheniscidae

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Assessment of the safety and efficacy of an oral probiotic-based vaccine against Aspergillus infection in captive-bred Humboldt penguins (Spheniscus humboldti)

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