{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,13]],"date-time":"2026-10-13T18:24:50Z","timestamp":1791915890896,"version":"4.3.4"},"reference-count":56,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2015,9,3]],"date-time":"2015-09-03T00:00:00Z","timestamp":1441238400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Animals"],"abstract":"<jats:p>The EU ban on conventional barren cages for laying hens from 2012 has improved many aspects of laying hen welfare. The new housing systems allow for the expression of highly-motivated behaviors. However, the systems available for intensive large-scale egg production (e.g., aviaries, floor housing systems, furnished cages) may cause other welfare challenges. We have reviewed the literature regarding the health, behavior, production characteristics, and welfare of laying hens when exposed to ammonia in their housing environment. Concentrations of ammonia gas are commonly high in aviaries and floor housing systems in which manure is not regularly removed, whereas they are usually lower in furnished cages. High levels are found during the cold season when ventilation flow is often reduced. Ammonia is a pungent gas, and behavioral studies indicate chickens are averse to the gas. High concentrations of gaseous ammonia can have adverse health effects and, when very high, even influence production performance. The most profound effects seen are the occurrence of lesions in the respiratory tract and keratoconjunctivitis. There is also evidence that high ammonia concentrations predispose poultry to respiratory disease and secondary infections. We conclude that there are animal welfare challenges related to high ammonia levels, and that immediate actions are needed. Development of improved systems and management routines for manure removal and ventilation will be important for the reduction of ammonia levels and hence will contribute to safeguarding hen welfare.<\/jats:p>","DOI":"10.3390\/ani5030389","type":"journal-article","created":{"date-parts":[[2015,9,3]],"date-time":"2015-09-03T10:57:07Z","timestamp":1441277827000},"page":"886-896","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":102,"title":["Air Quality in Alternative Housing Systems may have an Impact on Laying Hen Welfare. Part II\u2014Ammonia"],"prefix":"10.3390","volume":"5","author":[{"given":"Bruce","family":"David","sequence":"first","affiliation":[{"name":"Norwegian Veterinary Institute, P.O. Box 750 Sentrum, 0106 Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Cecilie","family":"Mejdell","sequence":"additional","affiliation":[{"name":"Norwegian Veterinary Institute, P.O. Box 750 Sentrum, 0106 Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Virginie","family":"Michel","sequence":"additional","affiliation":[{"name":"French Agency for Food, Environmental and Occupational Health Safety (Anses), BP 53, 22440 Ploufragan, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vonne","family":"Lund","sequence":"additional","affiliation":[{"name":"Norwegian Veterinary Institute, P.O. Box 750 Sentrum, 0106 Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Randi","family":"Moe","sequence":"additional","affiliation":[{"name":"Norwegian University of Life Sciences, Pb 8146 Dep, 0033 Oslo, Norway"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2015,9,3]]},"reference":[{"key":"ref_1","unstructured":"European Food Safety Authority (2005). Opinion of the Scientific Panel on Animal Health and Welfare (AHAW) on a Request from the Commission Related to the Welfare Aspects of Various Systems of Keeping Laying Hens, European Food Safety Authority."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"495","DOI":"10.3390\/ani5030368","article-title":"Air quality in alternative housing systems may have an impact on laying hen welfare. Part I\u2014Dust","volume":"5","author":"David","year":"2015","journal-title":"Animals"},{"key":"ref_3","first-page":"554","article-title":"Ventilation, air hygiene and animal health","volume":"113","author":"Wathes","year":"1983","journal-title":"Vet. Rec."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"891","DOI":"10.1177\/074823379801400609","article-title":"Ammonia exposure: A common cause for sinusitis. A case report and review of the literature","volume":"14","author":"Brautbar","year":"1998","journal-title":"Toxicol. Ind. Health"},{"key":"ref_5","first-page":"427","article-title":"Effects of small nitrogen compound concentrations on the upper respiratory tract","volume":"28","author":"Laciak","year":"1977","journal-title":"Med. Pracy"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"211","DOI":"10.13031\/2013.13686","article-title":"The relationship between agricultural environments and olfactory dysfunction","volume":"9","author":"Snyder","year":"2003","journal-title":"J. Agric. Saf. Health"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"379","DOI":"10.1080\/00071669888935","article-title":"Effect of type of aviary, manure and litter handling on the emission kinetics of ammonia from layer houses","volume":"39","author":"Bleijenberg","year":"1998","journal-title":"Br. Poult. Sci."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"412","DOI":"10.1111\/j.1365-2672.1965.tb02171.x","article-title":"The decomposition of uric acid in built up poultry litter","volume":"28","author":"Schefferle","year":"1965","journal-title":"J. Appl. Bacteriol."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"399","DOI":"10.1080\/00071660701473865","article-title":"Ammonia emissions from broiler litter: Response to bedding materials and acidifiers","volume":"48","author":"Tasistro","year":"2007","journal-title":"Br. Poult. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"14","DOI":"10.1080\/00071669708417936","article-title":"Concentrations and emission rates of aerial ammonia, nitrous oxide, methane, carbon dioxide, dust and endotoxin in UK broiler and layer houses","volume":"38","author":"Wathes","year":"1997","journal-title":"Br. Poult. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"518","DOI":"10.3382\/ps\/peu076","article-title":"Environmental assessment of three egg production systems\u2014Part I: Monitoring system and indoor air quality","volume":"94","author":"Zhao","year":"2015","journal-title":"Poult. Sci."},{"key":"ref_12","unstructured":"Von Wachenfelt, E., Od\u00e9n, K., and Gunnarsson, S. (2002). V\u00e4rph\u00f6ns i l\u00e5gbel\u00e4ggningssystem, Swedish University of Agricultural Sciences, Department of Agricultural Biosystems and Technology. (In Swedish)."},{"key":"ref_13","first-page":"103","article-title":"Ammonia, dust and bacteria in welfare-oriented systems for laying hens","volume":"16","author":"Nimmermark","year":"2009","journal-title":"Ann. Agric. Environ. Med."},{"key":"ref_14","unstructured":"Nimmermark, S., and Gustafsson, G. (2005). Influence of Temperature, Humidity and Ventilation Rate on the Release of Odor and Ammonia in a Floor Housing System for Laying Hens, International Commission of Agricultural Engineering."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1080\/00071668908417122","article-title":"Air hygiene in a broiler house: Comparison of deep litter with raised netting floors","volume":"30","author":"Madelin","year":"1989","journal-title":"Br. Poult. Sci."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"534","DOI":"10.3382\/ps.2010-01037","article-title":"Characterization of gas emissions from a mediterranean broiler farm","volume":"90","author":"Calvet","year":"2011","journal-title":"Poult. Sci."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1397","DOI":"10.3382\/ps.2010-01114","article-title":"High litter moisture content suppresses litter ammonia volatilization","volume":"90","author":"Miles","year":"2011","journal-title":"Poult. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"369","DOI":"10.2307\/1587967","article-title":"The adverse effects of ammonia on chickens including resistence to infection with Newcastle disease virus","volume":"8","author":"Anderson","year":"1964","journal-title":"Avian Res."},{"key":"ref_19","unstructured":"Reuvekamp, B.F.J., and van Niekerk, T.G.C.M. (1996). Ammoniakemissie bij Scharrelhennen: Traditioneel en Geperforeerde Schijnvloer, Praktijkonderzoek Pluimveehouderij \u201cHet Spelderholt\u201d. (In Dutch)."},{"key":"ref_20","unstructured":"Tauson, R., and Holm, K.E. (2001, January 1\u20134). First Furnished Small Group Cages in Evaluation Program on Commercial Farms in Sweden. Proceedings of the 6th European Symposium on Poultry Welfare, Zollikofen, Switzerland."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1927","DOI":"10.13031\/2013.20002","article-title":"Ammonia emissions from U.S. Laying hen houses in Iowa and Pennsylvania","volume":"48","author":"Liang","year":"2005","journal-title":"Trans. ASAE"},{"key":"ref_22","first-page":"139","article-title":"Luftfremde stoffe in und aus verschiedenen haltungssystemen f\u00fcr legehennen\u2014Teil 1: Ammoniak","volume":"60","author":"Hinz","year":"2010","journal-title":"Landbauforschung"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1071\/AN11352","article-title":"Yearly emission factors of ammonia and particulate matter from three laying-hen housing systems","volume":"52","author":"Costa","year":"2012","journal-title":"Anim. Prod. Sci."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"286","DOI":"10.3168\/jds.S0022-0302(68)86976-0","article-title":"Some aspects of ammonia toxicity in animal cells","volume":"51","author":"Visek","year":"1968","journal-title":"J. Dairy Sci."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"481","DOI":"10.3168\/jds.S0022-0302(84)81331-4","article-title":"Ammonia: Its effects on biological systems, metabolic hormones, and reproduction","volume":"67","author":"Visek","year":"1984","journal-title":"J. Dairy Sci."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"762","DOI":"10.3923\/ijps.2007.762.769","article-title":"Interactive effects of ammonia and light intensity on ocular, fear and leg health in broiler chickens","volume":"6","author":"Olanrewaju","year":"2007","journal-title":"Int. J. Poult. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1637\/7386-052405R.1","article-title":"Ocular responses to ammonia in broiler chickens","volume":"50","author":"Miles","year":"2006","journal-title":"Avian Dis."},{"key":"ref_28","unstructured":"Marthedal, H.E. (1980). Fjerkraesygdomme, DSR Forlag. (In Danish)."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"386","DOI":"10.3382\/ps.0290386","article-title":"A keratoconjunctivitis in chickens","volume":"29","author":"Bullis","year":"1950","journal-title":"Poult. Sci."},{"key":"ref_30","first-page":"1","article-title":"Mucous flow and ciliary activity in the trachea of healthy rats and rats exposed to respiratory irritant gases (SO2, H3N, HCHO): A functional and morphologic (light microscopic and electron microscopic) study, with special reference to technique","volume":"36","author":"Dalhamn","year":"1956","journal-title":"Acta Physiol. Scand. Suppl."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"177","DOI":"10.2307\/1588348","article-title":"Influence of poultry house dust, ammonia, and carbon dioxide on the resistance of chickens to Newcastle disease virus","volume":"10","author":"Anderson","year":"1966","journal-title":"Avian Dis."},{"key":"ref_32","first-page":"1049","article-title":"Influence of dust and ammonia on the development of air sac lesions in turkeys","volume":"29","author":"Anderson","year":"1968","journal-title":"Am. J. Vet. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.2460\/ajvr.1983.44.08.1530","article-title":"Scanning electron microscopic studies of adverse effects of ammonia on tracheal tissues of turkeys","volume":"44","author":"Nagaraja","year":"1983","journal-title":"Am. J. Vet. Res."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"392","DOI":"10.2460\/ajvr.1984.45.02.392","article-title":"Effect of ammonia on the quantitative clearance of escherichia coli from lungs, air sacs, and livers of turkeys aerosol vaccinated against Escherichia coli","volume":"45","author":"Nagaraja","year":"1984","journal-title":"Am. J. Vet. Res."},{"key":"ref_35","first-page":"187","article-title":"Aerosol exposure of ammonia, dust and Escherichia coli in broiler chickens","volume":"19","author":"Oyetunde","year":"1978","journal-title":"Can. Vet. J."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"149","DOI":"10.1080\/00071666408415526","article-title":"A study of the effect of different ventilation rates on the ammonia concentrations in the atmosphere of broiler houses","volume":"5","author":"Valentine","year":"1964","journal-title":"Br. Poult. Sci."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1592","DOI":"10.3382\/ps.0531592","article-title":"Evaluation of ammonia and infectious bronchitis vaccination stress on broiler performance and carcase quality","volume":"53","author":"Quarles","year":"1974","journal-title":"Poult. Sci."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"543","DOI":"10.3382\/ps.0580543","article-title":"Effect of air contaminants on performance and quality of broilers","volume":"58","author":"Quarles","year":"1979","journal-title":"Poult. Sci."},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1605","DOI":"10.13031\/2013.11067","article-title":"Aversion of pigs and domestic fowl to atmospheric ammonia","volume":"45","author":"Wathes","year":"2002","journal-title":"Trans. ASAE"},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"293","DOI":"10.1016\/j.applanim.2004.08.009","article-title":"Avoidance of atmospheric ammonia by domestic fowl and the effect of early experience","volume":"90","author":"Jones","year":"2005","journal-title":"Appl. Anim. Behav. Sci."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"263","DOI":"10.3382\/ps.2010-00877","article-title":"Environmental impacts and sustainability of egg production systems","volume":"90","author":"Xin","year":"2011","journal-title":"Poult. Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1080\/00071668608415623","article-title":"The influence of graded levels of atmospheric ammonia on chickens. II. Effects on the performance of laying hens","volume":"7","author":"Charles","year":"1966","journal-title":"Br. Poult. Sci."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1815","DOI":"10.3382\/ps.0611815","article-title":"Effect of atmospheric ammonia on laying hen performance","volume":"61","author":"Deaton","year":"1982","journal-title":"Poult. Sci."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"384","DOI":"10.3382\/ps.0630384","article-title":"Effect of atmospheric ammonia on pullets at point of lay","volume":"63","author":"Deaton","year":"1984","journal-title":"Poult. Sci."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"513","DOI":"10.3382\/ps.0600513","article-title":"Atmospheric ammonia and broiler cockerel performance","volume":"60","author":"Caveny","year":"1981","journal-title":"Poult. Sci."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"1161","DOI":"10.3382\/ps.0531161","article-title":"Effect of atmospheric ammonia and the stress of infectious bronchitis vaccination on leghorn males","volume":"53","author":"Kling","year":"1974","journal-title":"Poult. Sci."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"605","DOI":"10.3382\/japr.2007-00086","article-title":"Air quality and bird health status in three types of commercial egg layer houses","volume":"18","author":"Green","year":"2009","journal-title":"J. Appl. Poult. Res."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"421","DOI":"10.3382\/japr.2007-00076","article-title":"Reduction of ammonia emissions from stored laying hen manure through topical application of zeolite, Al + Clear, ferix-3, or poultry litter treatment","volume":"17","author":"Li","year":"2008","journal-title":"J. Appl. Poult. Res."},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.13031\/2013.37101","article-title":"Particulate matter concentrations and emissions of a high-rise layer house in Iowa","volume":"54","author":"Li","year":"2011","journal-title":"Trans. ASABE"},{"key":"ref_50","doi-asserted-by":"crossref","first-page":"73","DOI":"10.1006\/jaer.1994.1065","article-title":"Review on emissions of ammonia from housing systems for laying hens in relation to sources, processes, building design and manure handling","volume":"59","year":"1994","journal-title":"J. Agric. Eng. Res."},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"1115","DOI":"10.1071\/AN12367","article-title":"Bentonite can decrease ammonia volatilisation losses from poultry litter: Laboratory studies","volume":"53","author":"Redding","year":"2013","journal-title":"Anim. Prod. Sci."},{"key":"ref_52","first-page":"89","article-title":"Emission of harmful gases from poultry farms and possibilities of their reduction","volume":"34","year":"2015","journal-title":"Ekologia"},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"57","DOI":"10.1300\/J096v08n02_09","article-title":"Synergistic effects of dust and ammonia on the occupational health effects of poultry production workers","volume":"8","author":"Donham","year":"2002","journal-title":"J. Agromed."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"260","DOI":"10.1097\/00043764-200003000-00006","article-title":"Dose-response relationships between occupational aerosol exposures and cross-shift declines of lung function in poultry workers: Recommendations for exposure limits","volume":"42","author":"Donham","year":"2000","journal-title":"J. Occup. Environ. Med."},{"key":"ref_55","doi-asserted-by":"crossref","first-page":"699","DOI":"10.1080\/00071669208417510","article-title":"Fear of humans and its relationships with productivity in laying hens at commercial farms","volume":"33","author":"Barnett","year":"1992","journal-title":"Br. Poult. Sci."},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"87","DOI":"10.1016\/0168-1591(94)90054-X","article-title":"The effects of modifying the amount of human contact on behavioural, physiological and production responses of laying hens","volume":"41","author":"Barnett","year":"1994","journal-title":"Appl. Anim. Behav. Sci."}],"container-title":["Animals"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2615\/5\/3\/389\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T20:48:00Z","timestamp":1760215680000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2615\/5\/3\/389"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2015,9,3]]},"references-count":56,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2015,9]]}},"alternative-id":["ani5030389"],"URL":"https:\/\/doi.org\/10.3390\/ani5030389","relation":{},"ISSN":["2076-2615"],"issn-type":[{"value":"2076-2615","type":"electronic"}],"subject":[],"published":{"date-parts":[[2015,9,3]]}}}