Abstract
In this study, it was aimed to present the results of microbiological, cytological, histopathological, and immunohistochemical analyses of ocular samples from an Antarctic (Ardley Island, King George Island) Gentoo penguin chick (Pygoscelis papua) with a pyogranulomatous lesion in the right eye. Samples were taken from both the healthy left eye and the lesion in the right eye. Conventional culture methods and phenotypic and molecular tests were used for bacterial isolation and identification, respectively. None of the isolates could be identified phenotypically. As a result, four of the five isolates obtained from the right eye were considered to belong to putative novel bacterial species and taxa as their similarity to GenBank data was below 98.75%. The isolates were considered to be Pasteurellaceae bacterium, Corynebacterium ciconiae, Cardiobacteriaceae bacterium, Actinomyces sp., and Dermabacteraceae bacterium. The only isolate from the left eye was identified as Psychrobacter pygoscelis. The cytological analysis demonstrated cell infiltrates composed mostly of degenerate heterophils, reactive macrophages, plasma cells, lymphocytes, and eosinophils. Based on histopathological findings, the lesion was defined as a typical pyogranulomatous lesion. Immunohistochemistry demonstrated that the granuloma was positive for TNF-α, IL-4, MMP-9, IL-1β, and IL-6. This is the first documented report of the unilateral pyogranulomatous ocular lesion in a Gentoo penguin chick, living in its natural habitat in Antarctica. This report also describes the isolation of four bacteria from the infected eye, which are considered to belong to novel Genus, species, or taxa. The primary bacterial pathogen that caused the ocular lesion was not able to be detected and remains unclear.
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The data that support the findings of this study are available from the corresponding author upon reasonable request.
References
Adhikari P, Cosby DE, Cox NA, Franca MS, Williams SM, Gogal RM, Ritz CW, Kim WK (2018) Effect of dietary fructooligosaccharide supplementation on internal organs Salmonella colonization, immune response, ileal morphology, and ileal immunohistochemistry in laying hens challenged with Salmonella enteritidis. Poult Sci 97:2525–2533. https://doi.org/10.3382/ps/pey101
Athanasiou LV, Psemmas DE, Papaioannou N (2018) Conjunctival cytology assessment in dogs and cats. Sampling, diagnostic techniques and findings. J Hell Vet Med Soc 69:701–710. https://doi.org/10.12681/jhvms.16382
Balouria A, Deshmukh S, Banga HS, Ahmad A, Brar RS, Sodhi S (2019) Early migration pattern of Avibacterium paragallinarum in the nasal passage of experimentally infected chicken and Japanese quail by immunohistochemistry. Avian Pathol 48:168–177. https://doi.org/10.1080/03079457.2018.1562153
Barbosa A, Palacios MJ (2009) Health of Antarctic birds: a review of their parasites, pathogens and diseases. Polar Biol 32:1095. https://doi.org/10.1007/s00300-009-0640-3
Barnes LD, Grahn BH (2007) Actinomyces endophthalmitis and pneumonia in a dog. Can Vet J 48:1155–1158
Bayram LC, Gurbulak K, Gumussoy KS, Kutsal O (2019) The role of centrifuged liquid-based cytology in the evaluation of the endometrium in mares. Vet Arh 89:743–770. https://doi.org/10.24099/vet.arhiv.0653
Beckman BJ, Howe CW, Trampel DW, DeBey MC, Richard JL, Niyo Y (1994) Aspergillus fumigatus keratitis with intraocular invasion in 15-day-old chicks. Avian Dis 38:660–665. https://doi.org/10.2307/1592095
Bisgaard M (1993) Ecology and significance of pasteurellaceae in animals. Zentralblatt Fur Bakteriol 279:7–26. https://doi.org/10.1016/S0934-8840(11)80487-1
Bisgaard M, Mutter R (1986) A new facultatively anaerobic gram-negative fermentative rod obtained from different pathological lesions in poultry and tentatively designated taxon 14. Avian Pathol 15:117–127. https://doi.org/10.1080/03079458608436271
Bliss CD, Aquino S, Woodhouse S (2015) Ocular findings and reference values for selected ophthalmic diagnostic tests in the macaroni penguin (Eudyptes chrysolophus) and southern rockhopper penguin (Eudyptes chrysocome). Vet Ophthalmol 18:86–93. https://doi.org/10.1111/vop.12123
Bolzan AA, Brunelli ATJ, Castro MB, Souza MA, Souza JL, Laus JL (2005) Conjunctival impression cytology in dogs. Vet Ophthalmol 8:401–405. https://doi.org/10.1111/j.1463-5224.2005.00414.x
Bonelli F, Barsotti G, Attili AR, Mugnaini L, Cuteri V, Preziuso S, Corazza M, Preziuso G, Sgorbini M (2014) Conjunctival bacterial and fungal flora in clinically normal sheep. Vet Rec Open 1:e000017. https://doi.org/10.1136/vropen-2013-000017
Bonnedahl J, Olsen B, Waldenström J, Broman T, Jalava J, Huovinen P, Österblad M (2008) Antibiotic susceptibility of faecal bacteria in Antarctic penguins. Polar Biol 31:759–763. https://doi.org/10.1007/s00300-008-0430-3
Cakir L, Gumussoy K, Kutsal O, Tunc A (2014) Evaluation of brush cytology (cytospin technique) and cultural results in the diagnosis of keratoconjunctivitis in a goat herd. Ankara Üniversitesi Vet Fakültesi Derg 61:35–41. https://doi.org/10.1501/vetfak_0000002602
CCAMLR (2004) Protocols for collection of samples for pathological analysis in the event of disease being suspected among monitored species of birds. Part IV. In: CCAMLR ecosystem monitoring program-standard methods. Commission for the Conservation of Antarctic Marine. Cuervo
Cerdà-Cuéllar M, Moré E, Ayats T, Aguilera M, Muñoz-González S, Antilles N, Ryan PG, González-Solís J (2019) Do humans spread zoonotic enteric bacteria in Antarctica? Sci Total Environ 654:190–196. https://doi.org/10.1016/j.scitotenv.2018.10.272
Christensen H, Foster G, Christensen JP, Pennycott T, Olsen JE, Bisgaard M (2003) Phylogenetic analysis by 16S rDNA gene sequence comparison of avian taxa of Bisgaard and characterization and description of two new taxa of Pasteurellaceae. J Appl Microbiol 95:354–363. https://doi.org/10.1046/j.1365-2672.2003.01986.x
Chun J, Oren A, Ventosa A, Christensen H, Arahal DR, da Costa MS, Rooney AP, Yi H, Xu XW, De Meyer S, Trujillo ME (2018) Proposed minimal standards for the use of genome data for the taxonomy of prokaryotes. Int J Syst Evol Microbiol 68:461–466. https://doi.org/10.1099/ijsem.0.002516
Church ML, Priehs DR, Denis H, Croft L, DiRocco S, Davis M (2018) Technique, postoperative complications, and visual outcomes of phacoemulsification cataract surgery in 21 penguins (27 eyes): 2011–2015. Vet Ophthalmol 21:612–621. https://doi.org/10.1111/vop.12555
CLSI, Clinical Laboratory and Standards Institute (2018a) Interpretive Criteria for Identification of Bacteria and Fungi by Targeted DNA Sequencing, MM18. Wayne, PA: Clinical and Laboratory Standards Institute, MM18, 2nd ed. Replaces MM18‐A
CLSI, Clinical and Laboratory Standards Institute (2018b) Performance Standards for Antimicrobial Disk and Dilution Susceptibility Tests for Bacteria Isolated from Animals. 4th ed. CLSI, supplement VET08. Wayne, PA
CLSI, Clinical and Laboratory Standards Institute (2019) Performance Standards for Antimicrobial Susceptibility Testing; 20th Informational Supplement. CLSI document M100-S19. Replace. M100, 28th ed., Wayne, Pennsylvania, USA. 282
Cole N, Hume E, Khan S, Madigan M, Husband AJ, Garthwaite L, Willcox M (2005) Contribution of the cornea to cytokine levels in the whole eye induced during the early phase of Pseudomonas aeruginosa challenge. Immunol Cell Biol 83:301–306. https://doi.org/10.1111/j.1440-1711.2005.01324.x
Cullen CL (2003) Normal ocular features, conjunctival microflora and intraocular pressure in the Canadian beaver (Castor canadensis). Vet Ophthalmol 6:279–284. https://doi.org/10.1111/j.1463-5224.2003.00307.x
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32:1792–1797. https://doi.org/10.1093/nar/gkh340
Fedchenko N, Reifenrath J (2014) Different approaches for interpretation and reporting of immunohistochemistry analysis results in the bone tissue - a review. Diagn Pathol 9(221):1–12. https://doi.org/10.1186/s13000-014-0221-9
Goloboff PA, Farris JS, Nixon KC (2008) TNT, a free program for phylogenetic analysis. Cladistics 24:774–786. https://doi.org/10.1111/j.1096-0031.2008.00217.x
González-Acuña D, Hernández J, Moreno L, Herrmann B, Palma R, Latorre A, Medina-Vogel G, Kinsella MJ, Martín N, Araya K, Torres I, Fernandez N, Olsen B (2013) Health evaluation of wild gentoo penguins (Pygoscelis papua) in the antarctic peninsula. Polar Biol 36:1749–1760. https://doi.org/10.1007/s00300-013-1394-5
Gonzalez-Alonso-Alegre EM, Martinez-Nevado E, Caro-Vadillo A, Rodriguez-Alvaro A (2015) Central corneal thickness and intraocular pressure in captive black-footed penguins (Spheniscus dermersus). Vet Ophthalmol 18:94–97. https://doi.org/10.1111/vop.12206
Griggs A (2019) Ocular surface disease in birds. Vet Clin North Am - Exot Anim Pract 22:53–68. https://doi.org/10.1016/j.cvex.2018.08.005
Günther R, Haider W, Hotzel H, Ryll M (2006) Blepharoconjunctivitis in turkeys -the possible role of Bisgaard Taxon 14. 16th Int Symp Turkey Dis 129–133. ISBN3–939902–04–07
Holt DW, Layne EA (2008) Eye injuries in long-eared owls (Asio otus): prevalence and survival. J Raptor Res 42:243–247. https://doi.org/10.3356/JRR-07-42.1
Jara D, Bello-Toledo H, Domínguez M, Cigarroa C, Fernández P, Vergara L, Quezada-Aguiluz M, Opazo-Capurro A, Lima CA, González-Rocha G (2020) Antibiotic resistance in bacterial isolates from freshwater samples in Fildes Peninsula, King George Island. Antarctica Sci Rep 10:3145. https://doi.org/10.1038/s41598-020-60035-0
Jencek JE, Beaufrère H, Tully TN, Garner MM, Dunker FH, Baszler TV (2012) An outbreak of Chlamydophila psittaci in an outdoor colony of Magellanic penguins (Spheniscus magellanicus). J Avian Med Surg 26:225–231. https://doi.org/10.1647/2010-046R1.1
Kaiser P, Stäheli P (2013) Avian Cytokines and Chemokines. In: Schat KA, Kaspers B, Kaiser PBT-AI (Second E. (Eds.) Avian Immunology: Second Edition. Academic Press, Boston, pp. 189–204. https://doi.org/10.1016/B978-0-12-396965-1.00010-8
Labelle AL, Whittington JK, Breaux CB, Labelle P, Mitchell MA, Zarfoss MK, Schmidt SA, Hamor RE (2012) Clinical utility of a complete diagnostic protocol for the ocular evaluation of free-living raptors. Vet Ophthalmol 15:5–17. https://doi.org/10.1111/j.1463-5224.2011.00899.x
Leigue L, Montiani-Ferreira F, Moore BA (2016) Antimicrobial susceptibility and minimal inhibitory concentration of Pseudomonas aeruginosa isolated from septic ocular surface disease in different animal species. Open Vet J 6:215–222. https://doi.org/10.4314/ovj.v6i3.9
Martin GR (1999) Eye structure and foraging in King Penguins Aptenodytes patagonicus. Ibis (Lond. 1859) 141:444–450. https://doi.org/10.1111/j.1474-919x.1999.tb04413.x
Meekins JM, Stuckey JA, Carpenter JW, Armbrust L, Higbie C, Rankin AJ (2015) Ophthalmic diagnostic tests and ocular findings in a flock of captive American flamingos (Phoenicopterus ruber ruber). J Avian Med Surg 29:95–105. https://doi.org/10.1647/2014-021
Meier-Kolthoff JP, Auch AF, Klenk HP, Göker M (2013a) Genome sequence-based species delimitation with confidence intervals and improved distance functions. BMC Bioinformatics 14:60. https://doi.org/10.1186/1471-2105-14-60
Meier-Kolthoff JP, Göker M, Spröer C, Klenk HP (2013b) When should a DDH experiment be mandatory in microbial taxonomy? Arch Microbiol 195:413–418. https://doi.org/10.1007/s00203-013-0888-4
Meier-Kolthoff JP, Hahnke RL, Petersen J, Scheuner C, Michael V, Fiebig A, Rohde C, Rohde M, Fartmann B, Goodwin LA, Chertkov O, Reddy T, Pati A, Ivanova N, Markowitz V, Kyrpides NC, Woyke T, Göker M, Klenk HP (2014) Complete genome sequence of DSM 30083T, the type strain (U5/41T) of Escherichia coli, and a proposal for delineating subspecies in microbial taxonomy. Stand Genomic Sci 10(2):2014. https://doi.org/10.1186/1944-3277-9-2
Michalle Willis A, Wilkie DA (1999a) Avian ophthalmology part 1: Anatomy, examination, and diagnostic techniques. J Avian Med Surg 13:160–166. https://doi.org/10.2307/30130679
Michalle Willis A, Wilkie DA (1999b) Avian ophthalmology, part 2: Review of ophthalmic diseases. J Avian Med Surg 13:245–251. https://doi.org/10.2307/30135227
Miller RV, Gammon K, Day MJ (2009) Antibiotic resistance among bacteria isolated from seawater and penguin fecal samples collected near Palmer Station, Antarctica Can J Microbiol 55(1):37–45. https://doi.org/10.1139/W08-119
Moore BA, Teixeira LBC, Sponsel WE, Dubielzig RR (2017) The consequences of avian ocular trauma: histopathological evidence and implications of acute and chronic disease. Vet Ophthalmol 20(6):496–504. https://doi.org/10.1111/vop.12453
Moore BA, Paul-Murphy JR, Adamson KL, Dubielzig RR, Kern T, Gonzales BJ, Wolff P, Murphy CJ (2018) Lipoidal corneal degeneration in aged falcons. Vet Ophthalmol 21:332–338. https://doi.org/10.1111/vop.12508
Murphy CJ, Kern TJ, McKeever K, McKeever L, MacCoy D (1982) Ocular lesions in free-living raptors. J Am Vet Med Assoc 181(11):1302–1304
Nelson JD, Havener VR, Cameron JD (1983) Impressions of the Ocular Surface. Arch Ophthalmol 101:1869–1872
Nesterova AP, Le Bohec C, Beaune D, Pettex E, Le Maho Y, Bonadonna F (2010) Do penguins dare to walk at night? Visual cues influence king penguin colony arrivals and departures. Behav Ecol Sociobiol 64:1145–1156. https://doi.org/10.1007/s00265-010-0930-3
Nievas VF, Leotta GA, Vigo GB (2007) Subcutaneous clostridial infection in Adelie penguins in Hope Bay, Antarctica. Polar Biol 30:249–252. https://doi.org/10.1007/s00300-006-0179-5
Ott L (2018) Adhesion properties of toxigenic corynebacteria. AIMS Microbiol 4:85–103. https://doi.org/10.3934/microbiol.2018.1.85
Park FJ, Jaensch S (2009) Unusual multifocal granulomatous disease caused by actinomycetous bacteria in a nestling Derbyan parrot (Psittacula derbiana). Aust Vet J 87:63–65. https://doi.org/10.1111/j.1751-0813.2008.00378.x
Pattengale ND, Alipour M, Bininda-Emonds ORP, Moret BME, Stamatakis A (2010) How many bootstrap replicates are necessary? J Comput Biol 17:337–354. https://doi.org/10.1089/cmb.2009.0179
Perazzi A, Bonsembiante F, Gelain ME, Patruno M, Di Iorio E, Migliorati A, Iacopetti I (2017) Cytology of the healthy canine and feline ocular surface: comparison between cytobrush and impression technique. Vet Clin Pathol 46:164–171. https://doi.org/10.1111/vcp.12450
Petznick A, Madigan MC, Garrett Q, Sweeney DF, Evans MDM (2013) Contributions of ocular surface components to matrix-metalloproteinases (MMP)-2 and MMP-9 in feline tears following corneal epithelial wounding. PLoS One 8:13–18. https://doi.org/10.1371/journal.pone.0071948
Pritt B, Mount SL, Cooper K, Blaszyk H (2006) Pseudoactinomycotic radiate granules of the gynaecological tract: Review of a diagnostic pitfall. J Clin Pathol 59:17–20. https://doi.org/10.1136/jcp.2005.028977
Proietto L, Beatty SS, Plummer CE (2019) Comparison of 3 corneal cytology collection methods for evaluating equine ulcerative keratitis: Cytobrush, kimura platinum spatula, and handle edge of scalpel blade. Vet Ophthalmol 22:153–160. https://doi.org/10.1111/vop.12574
Qin QL, Xie BB, Zhang XY, Chen XL, Zhou BC, Zhou J, Oren A, Zhang YZ (2014) A proposed genus boundary for the prokaryotes based on genomic insights. J Bacteriol 196(12):2210–2215. https://doi.org/10.1128/JB.01688-14
Quinn PJ, Markey BK, Leonard FC, Hartigan P, Fanning S, Fitzpatrick ES (2011) Veterinary microbiology and microbial disease, Second. Wiley, West Sussex
Rabbia V, Bello-Toledo H, Jiménez S, Quezada M, Domínguez M, Vergara L, Gómez-Fuentes C, Calisto-Ulloa N, González-Acuña D, López J, González-Rocha G (2016) Antibiotic resistance in Escherichia coli strains isolated from Antarctic bird feces, water from inside a wastewater treatment plant, and seawater samples collected in the Antarctic Treaty area. Polar Sci 10:123–131. https://doi.org/10.1016/j.polar.2016.04.002
Sala A, Taddei S, Santospirito D, Sandri C, Magnone W, Cabassi CS (2016) Antibiotic resistance in conjunctival and enteric bacterial flora in raptors housed in a zoological garden. Vet Med Sci 2:239–245. https://doi.org/10.1002/vms3.38
Scott PR, Penny CD (1993) A field study of meningoencephalitis in calves with particular reference to analysis of cerebrospinal fluid. Vet Rec 133:119–121. https://doi.org/10.1136/vr.133.5.119
Sheldon JD, Adkesson MJ, Allender MC, Jankowski G, Langan J, Cardeña M, Cárdenas-Alayza S (2017) Determination of Tear Production and Intraocular Pressure with Rebound Tonometry in Wild Humboldt Penguins (Spheniscus humboldti). J Avian Med Surg 31:16–23. https://doi.org/10.1647/2015-134
Shoshani Y, Pe’er J, Doviner V, Frucht-Pery J, Solomon A (2005) Increased expression of inflammatory cytokines and matrix metalloproteinases in pseudophakic corneal edema. Investig Ophthalmol vis Sci 46:1940–1947. https://doi.org/10.1167/iovs.04-1203
Shyu LY, Chen KM, Lai SC (2019) Matrix metalloproteinase-2 and matrix metalloproteinase-9 in mice with ocular toxocariasis. Parasitol Res 118:483–491. https://doi.org/10.1007/s00436-018-06196-4
Sila G, Aquino S, Fuller G, Allard S, Woodhouse S (2015) Initial Clinical Experiences with Bilateral Phacoemulsification in Captive Macaroni (Eudyptes chrysolophus) and Southern Rockhopper (Eudyptes chrysocome) Penguins (abstract)., in: 46th Annual Conference of the American College of Veterinary Ophthalmologists
Silvanose CD, Bailey TA, Naldo JL, Howlett JC (2001) Bacterial flora of the conjunctiva and nasal cavity in normal and diseased captive bustards. Avian Dis 45:447–451. https://doi.org/10.2307/1592986
Singh R, Joseph A, Umapathy T, Tint NL, Dua HS (2005) Impression cytology of the ocular surface. Br J Ophthalmol 9:1655–1659. https://doi.org/10.1136/bjo.2005.073916
Stamatakis A (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313. https://doi.org/10.1093/bioinformatics/btu033
Suburo AM, Marcantoni M, Scolaro JA (1988) The structure of the eye in Spheniscus magellanicus: dimensions of the cornea and lens in different age groups. Colon Waterbirds 11:227. https://doi.org/10.2307/1521004
Swinger RL, Langan JN, Hamor R (2009) Ocular bacterial flora, tear production, and intraocular pressure in a captive flock of humboldt penguins (Spheniscus humboldti). J Zoo Wildl Med 40:430–436. https://doi.org/10.1638/2007-0126.1
Swofford DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods), Version 4.0 b10. Sinauer Associates, Sunderland
Wang HK, Sheng WH, Hung CC, Chen YC, Liew PL, Hsiao CH, Chang SC (2012) Hepatosplenic actinomycosis in an immunocompetent patient. J Formos Med Assoc 111:228–231. https://doi.org/10.1016/j.jfma.2012.03.001
Williams GT, Williams WJ (1983) Granulomatous inflammation - A review. J Clin Pathol 36:723–733. https://doi.org/10.1136/jcp.36.7.723
Wright AM, Mody DR, Anton RC, Schwartz MR (2017) Aberrant staining with Grocott’s methenamine silver: utility beyond fungal organisms. J Am Soc Cytopathol 6:223–227. https://doi.org/10.1016/j.jasc.2017.05.004
Xu ZY, Yu Y, Liu Y, Ou CB, Zhang YH, Liu TY, Wang QX, Ma JY (2019) Differential expression of pro-inflammatory and anti-inflammatory genes of layer chicken bursa after experimental infection with infectious bursal disease virus. Poult Sci 98:5307–5314. https://doi.org/10.3382/ps/pez312
Yoon SH, Ha SM, Kwon S, Lim J, Kim Y, Seo H, Chun J (2017) Introducing EzBioCloud: a taxonomically united database of 16S rRNA gene sequences and whole-genome assemblies. Int J Syst Evol Microbiol 67:1613–1617. https://doi.org/10.1099/ijsem.0.001755
Acknowledgements
This study was carried out under the auspices of the Presidency of The Republic of Turkey, supported by the Ministry of Industry and Technology, and coordinated by the Polar Research Centre (PolReC) of Istanbul Technical University (ITU). The authors would like to thank the Chilean Antarctic Institute (INACH-Instituto Antártico Chileno) and Chilean officials, specifically the INACH Project team led by Dr Rafael Medina, also including Dr Victor Neira Ramírez, Ph.D. student Gonzalo Barriga, and graduate student Felipe Berrios, for their valuable assistance during the fieldwork. The authors extend their special thanks to Dr José Retamales for enabling access to the excellent working facilities in Chile and Antarctica. We also thank the staff of the Chilean Antarctic bases, namely, the Chilean Army Bernardo O’Higgins Base, Yelchoo Base, Professor Julio Escudero Base, the Chilean Navy Stations Arturo Prat, AP-41 Aquiles and Karpuj for their logistic support. We are greatly indebted to the penguin groups of the Chilean Antarctic Expedition for their help in the fieldwork. Furthermore, we acknowledge Res. Assist. Capt. Sinan Yirmibesoglu of Istanbul Technical University, Maritime Faculty, for his map arrangement based on the processing of Copernicus Sentinel data [2020] included in the Norwegian Polar Institute’s Quantarctica package, using the Sentinel Hub (Fig. 1). We thank Professor Dr. Ayhan Duzler for his assistance in taking electron microscope pictures of bacteria.
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Some parts of this study including bacteriological, cytological, histopathological, and immunohistochemical analyses of the ocular samples examined were financially supported by Rectorate of Erciyes University, Kayseri, Turkey and other part of this study including the 16S rRNA gene sequence analyses of the bacteria isolated was financially supported by Scientific and Technological Research Council of Turkey (TUBITAK; project number: 119Z847).
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Latife Cakir Bayram: designed the research and collected the samples from the field; Secil Abay and Fuat Aydin: performed the bacteriological analysis of the samples and PCR for the identification of bacteria and 16S rRNA gene sequencing and analysed antibacterial susceptibility of the isolates; Tolga Guvenc and Gorkem Ekebas: performed immunohistochemical staining of cytospin preparations and tissue sections; Latife Cakır Bayram: prepared cytospin slides, stained tissue sections and cytospin smears with special staining methods and interpreted the results; Izzet Burcin Saticioglu: prepared and evaluated the phylogenetic trees; Latife Cakir Bayram, Secil Abay and Fuat Aydin: discussed the results and wrote the manuscript.
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Çakır Bayram, L., Abay, S., Satıcıoğlu, İ.B. et al. The ocular pyogranulomatous lesion in a Gentoo penguin (Pygoscelis papua) from the Antarctic Peninsula: evaluation of microbiological and histopathological analysis outcomes. Vet Res Commun 45, 143–158 (2021). https://doi.org/10.1007/s11259-021-09796-1
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DOI: https://doi.org/10.1007/s11259-021-09796-1