{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,1]],"date-time":"2026-09-01T02:42:41Z","timestamp":1788230561510,"version":"build-2803163510"},"reference-count":86,"publisher":"MDPI AG","issue":"14","license":[{"start":{"date-parts":[[2023,7,18]],"date-time":"2023-07-18T00:00:00Z","timestamp":1689638400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"Environment Research and Technology Development Fund","award":["JPMEERF18S20100"],"award-info":[{"award-number":["JPMEERF18S20100"]}]},{"name":"Environment Research and Technology Development Fund","award":["2019\u20134062"],"award-info":[{"award-number":["2019\u20134062"]}]},{"name":"The Japan Science Society","award":["JPMEERF18S20100"],"award-info":[{"award-number":["JPMEERF18S20100"]}]},{"name":"The Japan Science Society","award":["2019\u20134062"],"award-info":[{"award-number":["2019\u20134062"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>Lead (Pb), an environmental pollutant, has been widely reported to have contaminated mammals, including humans and birds. This study focuses on the effects of Pb pollution on avian influenza virus (AIV) antibody production. A total of 170 black-headed gulls (Chroicocephalus ridibundus) were captured in Tokyo Bay (TBP) from January 2019 to April 2020 and in Mikawa Bay (MBP) from November 2019 to April 2021. The gulls were weighed, subjected to blood sampling, and released with a ring band on their tarsus. The samples were used to measure blood Pb levels (BLL) and AIV-specific antibodies. The BLL were compared using the Wilcoxon two-sample test between the period when black-headed gulls arrived and the wintering period, defined by the number of gulls counted in each area. A significant increase was found in the TBP. A decrease in BLL significantly increased antibody titer during wintering in TBP and MBP. Pb pollution had a negative effect on the production of AIV antibodies. These findings suggest that wild birds that were contaminated by Pb in the environment may facilitate the spread of zoonotic diseases, further increasing the possibility that environmental pollutants may threaten human health.<\/jats:p>","DOI":"10.3390\/ani13142338","type":"journal-article","created":{"date-parts":[[2023,7,18]],"date-time":"2023-07-18T01:35:16Z","timestamp":1689644116000},"page":"2338","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":9,"title":["Evaluation of the Effect of Pb Pollution on Avian Influenza Virus-Specific Antibody Production in Black-Headed Gulls (Chroicocephalus ridibundus)"],"prefix":"10.3390","volume":"13","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-2232-786X","authenticated-orcid":false,"given":"Nana","family":"Ushine","sequence":"first","affiliation":[{"name":"Laboratory of Wildlife Medicine, Department of Veterinary Medicine, Nippon Veterinary and Life Science University, Musashino 180-0023, Japan"},{"name":"Laboratory of Animal Welfare, Department of Animal Health Technology, Yamazaki University of Animal Health Technology, Hachioji 192-0364, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-7731-5321","authenticated-orcid":false,"given":"Makoto","family":"Ozawa","sequence":"additional","affiliation":[{"name":"Joint Faculty of Veterinary Medicine, Kagoshima University, Kagoshima 890-0065, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-1635-2898","authenticated-orcid":false,"given":"Shouta M. M.","family":"Nakayama","sequence":"additional","affiliation":[{"name":"School of Veterinary Medicine, The University of Zambia, Lusaka P.O. Box 32379, Zambia"},{"name":"Laboratory of Toxicology, Department of Environmental Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo 060-0808, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mayumi","family":"Ishizuka","sequence":"additional","affiliation":[{"name":"Laboratory of Toxicology, Department of Environmental Veterinary Sciences, Faculty of Veterinary Medicine, Hokkaido University, Sapporo 060-0808, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-5614-3380","authenticated-orcid":false,"given":"Takuya","family":"Kato","sequence":"additional","affiliation":[{"name":"Laboratory of Wildlife Medicine, Department of Veterinary Medicine, Nippon Veterinary and Life Science University, Musashino 180-0023, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-4882-7969","authenticated-orcid":false,"given":"Shin-ichi","family":"Hayama","sequence":"additional","affiliation":[{"name":"Laboratory of Wildlife Medicine, Department of Veterinary Medicine, Nippon Veterinary and Life Science University, Musashino 180-0023, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2023,7,18]]},"reference":[{"key":"ref_1","first-page":"10","article-title":"Zoonotic diseases of poultry: A threat to profitable poultry production. a review","volume":"4","author":"Elenwo","year":"2014","journal-title":"J. Nat. Sci. Res."},{"key":"ref_2","doi-asserted-by":"crossref","unstructured":"Kim, W.-H., Bae, S.H., and Cho, S. (2021). Spatiotemporal dynamics of highly pathogenic avian influenza subtype H5N8 in poultry farms, South Korea. Viruses, 13.","DOI":"10.3390\/v13020274"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"121","DOI":"10.1146\/annurev-animal-030117-014628","article-title":"Detection of emerging zoonotic pathogens: An integrated one health approach","volume":"6","author":"Bird","year":"2018","journal-title":"Annu. Rev. Anim. Biosci."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1111\/zph.12617","article-title":"Chinese poultry farmers\u2019 decision-making for avian influenza prevention: A qualitative analysis","volume":"66","author":"Cui","year":"2019","journal-title":"Zoonoses Public Health"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"541","DOI":"10.1099\/vir.0.037572-0","article-title":"Reintroduction of H5N1 highly pathogenic avian influenza virus by migratory water birds, causing poultry outbreaks in the 2010\u20132011 winter season in Japan","volume":"93","author":"Sakoda","year":"2012","journal-title":"J. Gen. Virol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"21132","DOI":"10.2807\/1560-7917.ES2015.20.20.21132","article-title":"Genetic diversity of highly pathogenic H5N8 avian influenza viruses at a single overwintering site of migratory birds in Japan, 2014\/15","volume":"20","author":"Ozawa","year":"2015","journal-title":"Eurosurveillance"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"691","DOI":"10.3201\/eid2304.161957","article-title":"Characterization of highly pathogenic avian influenza virus A (H5N6), Japan, November 2016","volume":"23","author":"Okamatsu","year":"2017","journal-title":"Emerg. Infect. Dis."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1234957","DOI":"10.1080\/23312025.2016.1234957","article-title":"Analysis of influenza A viruses from gulls: An evaluation of inter-regional movements and interactions with other avian and mammalian influenza A viruses","volume":"2","author":"Benkaroun","year":"2016","journal-title":"Cogent. Biol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1754","DOI":"10.1016\/S0264-410X(03)00067-7","article-title":"Animal influenza virus surveillance","volume":"21","author":"Fouchier","year":"2003","journal-title":"Vaccine"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/S1573-5214(06)80021-7","article-title":"Outdoor ranging of poultry: A major risk factor for the introduction and development of High-Pathogenicity Avian Influenza","volume":"54","author":"Koch","year":"2006","journal-title":"NJAS-Wagen. J. Life Sci."},{"key":"ref_11","first-page":"490","article-title":"Within-host model of respiratory virus shedding and antibody response to H9N2 avian influenza virus vaccination and infection in chickens","volume":"6","author":"Xie","year":"2021","journal-title":"Infect. Dis. Model."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"939","DOI":"10.1007\/s00705-009-0385-x","article-title":"Field assessment of an H5N1 inactivated vaccine in chickens and ducks in Lao PDR","volume":"154","author":"Boltz","year":"2009","journal-title":"Arch. Virol."},{"key":"ref_13","first-page":"89","article-title":"Accumulation of heavy metals (Ni, Cu, Cd, Cr, Pb, Zn, Fe) in the soil, water and plants and analysis of physico-chemical parameters of soil and water collected from Tanda Dam Kohat","volume":"7","author":"Nazir","year":"2015","journal-title":"J. Pharm. Sci."},{"key":"ref_14","unstructured":"Delahay, R.J., and Spray, C.J. (2014). Lead Ammunition: Understanding and Minimising the Risks to Human and Environmental Health, Edward Grey Institute, University of Oxford. The Oxford Lead Symposium."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1080\/0307945021000070660","article-title":"Lead and lead toxicity in domestic and free-living birds","volume":"32","author":"Troya","year":"2003","journal-title":"Avian Pathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"935","DOI":"10.1007\/s13280-019-01159-0","article-title":"Effects of lead from ammunition on birds and other wildlife: A review and update","volume":"48","author":"Pain","year":"2019","journal-title":"Ambio"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"238","DOI":"10.2307\/3801228","article-title":"Environmental contaminants in California condors","volume":"52","author":"Wiemeyer","year":"1988","journal-title":"J. Wildl. Manag."},{"key":"ref_18","unstructured":"Watson, R.T., Fuller, M., Pokras, M., and Hunt, W.G. (2009). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans, The Peregrine Fund."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1515\/mgmc-2017-0023","article-title":"Lead acetate toxicity on human lymphocytes at non-cytotoxic concentrations detected in human blood","volume":"40","author":"Zarei","year":"2017","journal-title":"Main Group Met. Chem."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1080\/109374000281096","article-title":"Effects of lead on birds (Laridae): A review of laboratory and field studies","volume":"3","author":"Burger","year":"2000","journal-title":"J. Toxicol. Environ. Health B Crit. Rev."},{"key":"ref_21","first-page":"729","article-title":"Heavy metal contamination of soil and sediment in Zambia","volume":"4","author":"Ikenaka","year":"2010","journal-title":"Afr. J. Environ. Sci. Technol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1006\/taap.2001.9307","article-title":"Low level lead exposure in vitro stimulates the proliferation and expansion of alloantigen-reactive CD4 high T cells","volume":"177","author":"McCabe","year":"2001","journal-title":"Toxicol. Appl. Pharmacol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"477","DOI":"10.1006\/brbi.2001.0641","article-title":"Neonatal lead exposure potentiates sickness behavior induced by Listeria monocytogenes infection of mice","volume":"16","author":"Dyatlov","year":"2002","journal-title":"Brain Behav. Immun."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1038\/250148a0","article-title":"Decreased antibody formation in mice exposed to lead","volume":"250","author":"Koller","year":"1974","journal-title":"Nature"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"74","DOI":"10.1016\/j.ecoenv.2019.03.036","article-title":"Effect of selenium antagonist lead-induced damage on Th1\/Th2 imbalance in the peripheral blood lymphocytes of chickens","volume":"175","author":"Fu","year":"2019","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_26","first-page":"669","article-title":"Acute lead poisoning from a fishing sinker","volume":"7","author":"Yanagawa","year":"1996","journal-title":"Acute Med. Surg."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"272","DOI":"10.1016\/j.taap.2012.10.001","article-title":"Pb exposure attenuates hypersensitivity in vivo by increasing regulatory T cells","volume":"265","author":"Fang","year":"2012","journal-title":"Toxicol. Appl. Pharmacol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1016\/j.fsi.2020.08.015","article-title":"Pb exposure triggers MAPK-dependent inflammation by activating oxidative stress and miRNA-155 expression in carp head kidney","volume":"106","author":"Jing","year":"2020","journal-title":"Fish Shellfish Immunol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"1","DOI":"10.21743\/pjaec\/2017.06.01","article-title":"Perilous effects of heavy metals contamination on human health","volume":"18","author":"Zahra","year":"2017","journal-title":"Pak. J. Anal. Environ. Chem."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"492","DOI":"10.1080\/03079450400003601","article-title":"Investigation of outbreaks of highly pathogenic H5N1 avian influenza in waterfowl and wild birds in Hong Kong in late 2002","volume":"33","author":"Ellis","year":"2004","journal-title":"Avian Pathol."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2814","DOI":"10.1128\/JVI.79.5.2814-2822.2005","article-title":"Characterization of a novel influenza A virus hemagglutinin subtype (H16) obtained from Black-headed gulls","volume":"79","author":"Fouchier","year":"2005","journal-title":"J. Virol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"349","DOI":"10.3201\/eid1602.090974","article-title":"Avian influenza (H5N1) outbreak among wild birds, Russia, 2009","volume":"16","author":"Sharshov","year":"2010","journal-title":"Emerg. Infect. Dis."},{"key":"ref_33","first-page":"521","article-title":"Virological and serological investigation of avian influenza in Black headed gulls captured on a rubbish dump in Zagreb, Croatia","volume":"84","year":"2014","journal-title":"Vet. Arh."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"138","DOI":"10.3201\/eid2001.130984","article-title":"Epidemiology of influenza A virus among black headed gulls, the Netherlands, 2006\u20132010","volume":"20","author":"Verhagen","year":"2014","journal-title":"Emerg. Infect. Dis."},{"key":"ref_35","unstructured":"(2020, June 11). Status of Occurrence and Detection of Highly Pathogenic Avian Influenza in Japan, Available online: https:\/\/www.env.go.jp\/nature\/dobutsu\/bird_flu\/wildbird_past.html."},{"key":"ref_36","unstructured":"Baker, K. (1993). Identification Guide to European Non-Passerines, British Trust for Ornithology."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"37","DOI":"10.1016\/j.virol.2018.07.004","article-title":"Receptor-binding properties of influenza viruses isolated from gulls","volume":"522","author":"Gambaryan","year":"2018","journal-title":"Virology"},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Postnikova, Y., Treshchalina, A., Boravleva, E., Gambaryan, A., Ishmukhametov, A., Matrosovich, M., Fouchier, R.A.M., Sadykova, G., Prilipov, A., and Lomakina, N. (2021). Diversity and reassorment rate of influenza A viruses in wild ducks and gulls. Viruses, 13.","DOI":"10.20944\/preprints202105.0050.v1"},{"key":"ref_39","unstructured":"Kloubec, B., and \u0160vecov\u00e1, Z. (1989, January 25\u201326). Changes in the South Bohemian population of Black-headed Gull (Larus ridibundus) and their possible causes (in Czech). Proceedings of the II South Bohemian Ornithological Conference, \u010cesk\u00e9 Bud\u011bjovice, Czech Republic."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"726","DOI":"10.1006\/jmsc.1997.0243","article-title":"Seabirds as monitors of the marine environment","volume":"54","author":"Furness","year":"1997","journal-title":"ICES Mar. Sci. Symp."},{"key":"ref_41","unstructured":"Pickard, K. (2010). Heavy Metal Pollution and Black Headed Gull (Larus ridibundus L.) Breeding Ecology. [Ph.D. Thesis, School of Civil Engineering and the Environment, University of Southampton]."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1515\/eko-2016-0028","article-title":"Long-term decline in breeding abundance of Black-headed Gull (Chroicocephalus ridibundus) in the Czech Republic: A case study of a population trend at the Chomoutov lake","volume":"35","author":"Poprach","year":"2016","journal-title":"Ekol\u00f3gia Bratisl."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"159","DOI":"10.3161\/068.035.0209","article-title":"Heavy metals, resting metabolism rates and breeding parameters in two populations of Black-headed gull Larus ridibundus from the industrially polluted areas of Upper Silesia, Poland","volume":"35","author":"Migula","year":"2000","journal-title":"Acta Ornithol."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"80","DOI":"10.1007\/s00265-003-0681-5","article-title":"Inter-sexual differences in T-cell-mediated immunity of black-headed gull chicks (Larus ridibundus) depend on the hatching order","volume":"55","author":"Muller","year":"2003","journal-title":"Behav. Ecol. Sociobiol."},{"key":"ref_45","first-page":"783","article-title":"Heavy metal concentrations in the tissues of the Black-headed gull Larus ridibundus L. nesting in the dam reservoir in south-western Poland","volume":"55","author":"Orlowski","year":"2007","journal-title":"Pol. J. Ecol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"825","DOI":"10.1007\/s13280-017-0929-3","article-title":"Concentrations of lead and other elements in the liver of the White-tailed eagle (Haliaeetus albicilla), a European flagship species, wintering in Eastern Poland","volume":"46","author":"Kitowski","year":"2017","journal-title":"Ambio"},{"key":"ref_47","unstructured":"Bird Banding Society of Japan (2022, June 01). Available online: https:\/\/birdbanding-assn.jp\/J05_color_ring\/color.htm."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1177\/1040638716675197","article-title":"Comparison of three different primer sets for sexing birds","volume":"29","author":"Bilgin","year":"2017","journal-title":"J. Vet. Diagn. Investig."},{"key":"ref_49","first-page":"51","article-title":"Sex identification in Japanese birds using droppings as a source of DNA","volume":"28","author":"Ushine","year":"2016","journal-title":"J. Jpn. Bird Band. Assoc."},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"1124","DOI":"10.1292\/jvms.20-0246","article-title":"Relationship between blood test values and blood lead (Pb) levels in Black-headed gull (Chroicocephalus ridibundus: Laridae)","volume":"82","author":"Ushine","year":"2020","journal-title":"J. Vet. Med. Sci."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"84","DOI":"10.1186\/1751-0147-55-84","article-title":"An enzyme-linked immunosorbent assay for detection of avian influenza virus subtypes H5 and H7 antibodies","volume":"55","author":"Jensen","year":"2013","journal-title":"Acta Vet. Scand."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1146\/annurev.ecolsys.32.081501.114006","article-title":"The physiology of life history trade-offs in animals","volume":"32","author":"Zera","year":"2001","journal-title":"Annu. Rev. Ecol. Evol. Syst."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"748","DOI":"10.1111\/j.1600-0706.2010.18961.x","article-title":"Reconstructing an annual cycle of interaction: Natural infection and antibody dynamics to avian influenza along a migratory flyway","volume":"120","author":"Hoye","year":"2011","journal-title":"Oikos"},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"2","DOI":"10.1016\/j.virusres.2021.198331","article-title":"Establishment of a safe and convenient assay for detection of HA subtype-specific antibodies with PB2 gene-knockout influenza viruses","volume":"295","author":"Ito","year":"2021","journal-title":"Virus Res."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"e00282-19","DOI":"10.1128\/JVI.00282-19","article-title":"Aerosol transmission of gull-origin Iceland subtype H10N7 influenza A virus in ferrets","volume":"93","author":"Guan","year":"2019","journal-title":"J. Virol."},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"He, F., Prabakaran, M., Tan, Y., Indira, K., Kumar, S.R., and Kwang, J. (2013). Development of dual-function ELISA for effective antigen and antibody detection against H7 avian influenza virus. BMC Microbiol., 13.","DOI":"10.1186\/1471-2180-13-219"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"154","DOI":"10.3201\/eid0802.010148","article-title":"Lack of evidence for human-to-human transmission of avian influenza A (H9N2) viruses in Houng Kong, China, 1999","volume":"8","author":"Uyeki","year":"2002","journal-title":"Emerg. Infect. Dis."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"1471","DOI":"10.1007\/s10096-021-04174-w","article-title":"The impact of obesity on seasonal influenza: A single-center, retrospective study conducted in Israel","volume":"40","author":"Atamna","year":"2021","journal-title":"Eur. J. Clin. Microbiol. Infect. Dis."},{"key":"ref_59","doi-asserted-by":"crossref","unstructured":"Hammouda, A., Selmi, S., Pearce-Duvet, J., Chokri, M.A., Arnal, A., Gauthier-Clerc, M., and Boulinier, T. (2012). Maternal antibody transmission in relation to mother fluctuating asymmetry in a long-lived colonial seabird: The Yellow-legged gull Larus michahellis. PLoS ONE, 7.","DOI":"10.1371\/journal.pone.0034966"},{"key":"ref_60","doi-asserted-by":"crossref","first-page":"708","DOI":"10.1016\/S0022-3476(81)80829-3","article-title":"Risk of respiratory syncytial virus infection for infants from low-income families in relationship to age, sex, ethnic group, and maternal antibody level","volume":"98","author":"Glezen","year":"1981","journal-title":"J. Pediatr."},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"671","DOI":"10.1002\/jez.1402320336","article-title":"Interrelation of the avian immune and neuroendocrine systems","volume":"232","author":"Glick","year":"1984","journal-title":"J. Exp. Zool."},{"key":"ref_62","first-page":"150","article-title":"Gender Medicine and Autoimmune Disorders; Why our Ladies Get Sick?","volume":"72","author":"Hayakawa","year":"2013","journal-title":"J. Nihon Univ. Med. Assoc."},{"key":"ref_63","doi-asserted-by":"crossref","unstructured":"Beyer, W.N., and Meador, J.P. (2011). Environmental Contaminants in Biota, Interpreting Tissue Concentrations, Taylor & Francis Group LLC. [2nd ed.].","DOI":"10.1201\/b10598"},{"key":"ref_64","first-page":"126","article-title":"Toxicological effects of lead in birds","volume":"Volume 237","year":"2016","journal-title":"Reviews of Environmental Contamination and Toxicology"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"20221312","DOI":"10.1098\/rspb.2022.1312","article-title":"Avian influenza antibody titer increases with mercury contamination in wild waterfowl","volume":"289","author":"Teitelbaum","year":"2022","journal-title":"Proc. R. Soc. B"},{"key":"ref_66","unstructured":"Geological Survey of Japan (2021, September 06). Available online: https:\/\/gbank.gsj.jp\/geochemmap\/gmaps\/map.htm."},{"key":"ref_67","first-page":"25","article-title":"Estimation of the relationship between Pb contamination and feeding history of black-headed gulls (Chroicocephalus ridibundus) using stable isotopes","volume":"26","author":"Ushine","year":"2023","journal-title":"Jpn. J. Environ. Toxicol."},{"key":"ref_68","doi-asserted-by":"crossref","unstructured":"Ellis, J.W., Root, J.J., McCurdy, L.M., Bentler, K.T., Barrett, N.L., VanDalen, K.K., Dirsmith, K.L., and Shriner, S.A. (2021). Avian influenza A virus susceptibility, infection, transmission, and antibody kinetics in European starlings. PLoS Pathog., 17.","DOI":"10.1371\/journal.ppat.1009879"},{"key":"ref_69","unstructured":"Watson, R.T., Fuller., M., Pokras, M., and Hunt, W.G. (2009). Ingestion of Lead from Spent Ammunition: Implications for Wildlife and Humans, The Peregrine Fund."},{"key":"ref_70","doi-asserted-by":"crossref","first-page":"350","DOI":"10.1016\/j.envpol.2015.06.014","article-title":"Altered immune response in mallard ducklings exposed to lead through maternal transfer in the wild","volume":"205","author":"Mateo","year":"2015","journal-title":"Environ. Pollut."},{"key":"ref_71","unstructured":"(2021, March 24). USEPA Regional Screening Level (RSL) Summary Table, Available online: https:\/\/www.epa.gov\/risk\/regional-screening-levels-rsls-generic-tables."},{"key":"ref_72","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1016\/j.ecoenv.2012.09.025","article-title":"Tracheal responsiveness to methacholine and ovalbumin; and lung inflammation in guinea pigs exposed to inhaled lead after sensitization","volume":"86","author":"Boskabady","year":"2012","journal-title":"Ecotoxicol. Environ. Saf."},{"key":"ref_73","doi-asserted-by":"crossref","first-page":"162","DOI":"10.1007\/s12011-017-1200-2","article-title":"The antagonistic effect of selenium on lead-induced immune dysfunction via recovery of cytokine and heat shock protein expression in chicken neutrophils","volume":"185","author":"Xing","year":"2018","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_74","doi-asserted-by":"crossref","first-page":"1060","DOI":"10.1002\/etc.4702","article-title":"Modulatory effects of Pb2+ on virally challenged chicken macrophage (HD-11) and B-lymphocyte (DT40) cell lines in vitro","volume":"39","author":"Han","year":"2020","journal-title":"Environ. Toxicol. Chem."},{"key":"ref_75","doi-asserted-by":"crossref","first-page":"111809","DOI":"10.1016\/j.fct.2020.111809","article-title":"Toxic metal exposure as a possible risk factor for COVID-19 and other respiratory infectious diseases","volume":"146","author":"Skalny","year":"2020","journal-title":"Food Chem. Toxicol."},{"key":"ref_76","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1177\/1721727X221122719","article-title":"Potential mechanisms of some selected heavy metals in the induction of inflammation and autoimmunity","volume":"20","author":"Anka","year":"2022","journal-title":"Eur. J. Inflamm."},{"key":"ref_77","doi-asserted-by":"crossref","first-page":"13","DOI":"10.1007\/BF02783306","article-title":"Lead disrupts eicosanoid metabolism, macrophage function, and disease resistance in birds","volume":"60","author":"Knowles","year":"1997","journal-title":"Biol. Trace Elem. Res."},{"key":"ref_78","doi-asserted-by":"crossref","first-page":"404","DOI":"10.1016\/j.envint.2018.08.013","article-title":"The effect of environmental lead exposure on human health and the contribution of inflammatory mechanisms, a review","volume":"120","author":"Boskabady","year":"2018","journal-title":"Environ. Int."},{"key":"ref_79","doi-asserted-by":"crossref","first-page":"A178","DOI":"10.1289\/ehp.1306945","article-title":"Health risks from lead-based ammunition in the environment","volume":"121","author":"Bellinger","year":"2013","journal-title":"Environ. Health Perspect."},{"key":"ref_80","doi-asserted-by":"crossref","first-page":"367","DOI":"10.1016\/j.chemosphere.2017.07.143","article-title":"Lead exposure in raptors from Japan and source identification using Pb stable isotope ratios","volume":"186","author":"Ishii","year":"2017","journal-title":"Chemosphere"},{"key":"ref_81","doi-asserted-by":"crossref","first-page":"36237","DOI":"10.1038\/srep36237","article-title":"Surveillance for highly pathogenic H5 avian influenza virus in synanthropic wildlife associated with poultry farms during an acute outbreak","volume":"6","author":"Shriner","year":"2016","journal-title":"Sci. Rep."},{"key":"ref_82","doi-asserted-by":"crossref","first-page":"717","DOI":"10.3201\/eid2304.161886","article-title":"Novel reassortant highly pathogenic avian influenza (H5N8) virus in zoos, India","volume":"23","author":"Nagarajan","year":"2017","journal-title":"Emerg. Infect. Dis."},{"key":"ref_83","doi-asserted-by":"crossref","first-page":"915","DOI":"10.1089\/vbz.2009.0107","article-title":"Multiple introduction of Asian H5N1 avian influenza virus in Croatia by wild birds during 2005\u20132006 and isolation of the virus from apparently healthy Black-headed gulls (Larus ridibundus)","volume":"10","author":"Savic","year":"2010","journal-title":"Vector Borne Zoonotic Dis."},{"key":"ref_84","unstructured":"Yamashina Institute for Ornithology (2002). Atlas of Japanese Migratory Birds from 1961 to 1995, Yamashina Institute for Ornithology. (In Japanese)."},{"key":"ref_85","doi-asserted-by":"crossref","first-page":"1","DOI":"10.7589\/2014-01-004","article-title":"The role of one health in wildlife conservation: A challenge and opportunity","volume":"51","author":"Buttke","year":"2015","journal-title":"J. Wildl. Dis."},{"key":"ref_86","doi-asserted-by":"crossref","first-page":"1827","DOI":"10.3201\/eid1612.100589","article-title":"Surveillance of wild birds for avian influenza virus","volume":"16","author":"Hoye","year":"2010","journal-title":"Emerg. Infect. Dis."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/14\/2338\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T20:13:44Z","timestamp":1760127224000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/13\/14\/2338"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,7,18]]},"references-count":86,"journal-issue":{"issue":"14","published-online":{"date-parts":[[2023,7]]}},"alternative-id":["ani13142338"],"URL":"https:\/\/doi.org\/10.3390\/ani13142338","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,7,18]]}}}