Skeletal health of layers across all housing systems and future research directions for Australia
D. L. M. Campbell
+ Author Affiliations
- Author Affiliations
CSIRO, Agriculture and Food, New England Highway, Armidale, NSW 2350, Australia. Email: dana.campbell@csiro.au
Animal Production Science 61(10) 883-892 https://doi.org/10.1071/AN19578
Submitted: 1 October 2019 Accepted: 30 June 2020 Published: 20 August 2020
Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND
Abstract
Modern laying hens have been selected for an astounding rate of egg production, but the physiological calcium demand takes a significant toll on their skeletal health. Bones can be assessed both in vivo and ex vivo, using a combination of different structural and mechanical analysis methods. Typically, the properties of leg, wing and keel bones are measured. Conventional caged layers are restricted in movement, which imbalances structural bone resorption and new bone formation, resulting in osteoporosis. Hens within alternative housing systems have opportunities to exercise for strengthening bones, but they can also suffer from higher rates of keel fractures and/or deviations that are likely to have resulted from collisions or pressure force. Limited research has been conducted within Australian commercial housing systems to assess hen skeletal health, including prevalence of keel damage across different system types. Research conducted on both brown and white hen strains approximately within the past decade internationally (2009 onward) has shown that skeletal health is impaired across all housing systems. Keel-bone damage is of specific concern as it occurs at high rates, particularly in multi-tiered systems, is painful, can alter hen behaviour, and reduce both production and egg quality. Management strategies such as the provision of ramps to access perches and tiers can reduce the incidence of keel-bone damage to a degree. Bone strength can be improved through exercise opportunities, particularly when available during pullet rearing. Genetic selection for high bone strength may be necessary for hens to adequately adapt to loose-housed systems, but the best strategy for improving skeletal health is likely to be multifactorial.
Additional keywords: damage, density, fracture, humerus, keel, tibia, welfare.
References
Aguado E, Pascaretti-Grizon F, Goyenvalle E, Audran M, Chappard D (2015) Bone mass and bone quality are altered by hypoactivity in the chicken. PLoS One 10, e0116763| Bone mass and bone quality are altered by hypoactivity in the chicken.Crossref | GoogleScholarGoogle Scholar | 25635404PubMed |
Ali ABA, Campbell DLM, Karcher DM, Siegford JM (2016) Influence of genetic strain and access to litter on spatial distribution of 4 strains of laying hens in an aviary system. Poultry Science 95, 2489–2502.
| Influence of genetic strain and access to litter on spatial distribution of 4 strains of laying hens in an aviary system.Crossref | GoogleScholarGoogle Scholar |
Armstrong EA, Rufener C, Toscano MJ, Eastham JE, Guy JH, Sandilands V, Boswell T, Smulders TV (2020) Keel bone fractures induce a depressive-like state in laying hens. Scientific Reports 10, 3007
| Keel bone fractures induce a depressive-like state in laying hens.Crossref | GoogleScholarGoogle Scholar | 32080271PubMed |
Baker S, Robison CI, Karcher DM, Toscano MJ, Makagon MM (2020) Keel impacts and associated behaviors in laying hens. Applied Animal Behaviour Science 222, 104886
| Keel impacts and associated behaviors in laying hens.Crossref | GoogleScholarGoogle Scholar |
Baur S, Rufener C, Toscano MJ, Geissbühler U (2020) Radiographic evaluation of keel bone damage in laying hens: morphologic and temporal observations in a longitudinal study. Frontiers in Veterinary Science 7, 129
| Radiographic evaluation of keel bone damage in laying hens: morphologic and temporal observations in a longitudinal study.Crossref | GoogleScholarGoogle Scholar | 32226794PubMed |
Blatchford RA, Fulton RM, Mench JA (2016) The utilization of the Welfare Quality® assessment for determining laying hen condition across three housing systems. Poultry Science 95, 154–163.
| The utilization of the Welfare Quality® assessment for determining laying hen condition across three housing systems.Crossref | GoogleScholarGoogle Scholar | 26240396PubMed |
Buijs S, Heerkens JLT, Ampe B, Delezie E, Rodenburg TB, Tuyttens FAM (2019) Assessing keel bone damage in laying hens by palpation: effects of assessor experience on accuracy, inter-rater agreement and intra-rater consistency. Poultry Science 98, 514–521.
| Assessing keel bone damage in laying hens by palpation: effects of assessor experience on accuracy, inter-rater agreement and intra-rater consistency.Crossref | GoogleScholarGoogle Scholar | 30768146PubMed |
Burr DB, Robling AG, Turner CH (2002) Effects of biomechanical stress on bones in animals. Bone 30, 781–786.
| Effects of biomechanical stress on bones in animals.Crossref | GoogleScholarGoogle Scholar | 11996920PubMed |
Campbell DLM, Goodwin SL, Makagon MM, Swanson JC, Siegford JM (2016) Failed landings after laying hen flight in a commercial aviary over two flock cycles. Poultry Science 95, 188–197.
| Failed landings after laying hen flight in a commercial aviary over two flock cycles.Crossref | GoogleScholarGoogle Scholar |
Candelotto L, Stratmann A, Gebhardt-Henrich SG, Rufener C, van de Braak T, Toscano MJ (2017) Susceptibility to keel bone fractures in laying hens and the role of genetic variation. Poultry Science 96, 3517–3528.
| Susceptibility to keel bone fractures in laying hens and the role of genetic variation.Crossref | GoogleScholarGoogle Scholar | 28938772PubMed |
Casey-Trott TM, Widowski TM (2016) Behavioral differences of laying hens with fractured keel bones within furnished cages. Frontiers in Veterinary Science 3, 42
| Behavioral differences of laying hens with fractured keel bones within furnished cages.Crossref | GoogleScholarGoogle Scholar | 27303674PubMed |
Casey-Trott TM, Widowski TM (2018) Validation of an accelerometer to quantify inactivity in laying hens with or without keel-bone fractures. Animal Welfare 27, 103–114.
| Validation of an accelerometer to quantify inactivity in laying hens with or without keel-bone fractures.Crossref | GoogleScholarGoogle Scholar |
Casey-Trott TM, Guerin MT, Sandilands V, Torrey S, Widowski TM (2017a) Rearing system affects prevalence of keel-bone damage in laying hens: a longitudinal study of four consecutive flocks. Poultry Science 96, 2029–2039.
| Rearing system affects prevalence of keel-bone damage in laying hens: a longitudinal study of four consecutive flocks.Crossref | GoogleScholarGoogle Scholar | 28371938PubMed |
Casey-Trott TM, Korver DR, Guerin MT, Sandilands V, Torrey S, Widowski TM (2017b) Opportunities for exercise during pullet rearing. Part 1: effect on the musculoskeletal characteristics of pullets. Poultry Science 96, 2509–2517.
| Opportunities for exercise during pullet rearing. Part 1: effect on the musculoskeletal characteristics of pullets.Crossref | GoogleScholarGoogle Scholar | 28379533PubMed |
Casey-Trott TM, Korver DR, Guerin MT, Sandilands V, Torrey S, Widowski TM (2017c) Opportunities for exercise during pullet rearing. Part II: long-term effects on bone characteristics of adult laying hens at the end-of-lay. Poultry Science 96, 2518–2527.
| Opportunities for exercise during pullet rearing. Part II: long-term effects on bone characteristics of adult laying hens at the end-of-lay.Crossref | GoogleScholarGoogle Scholar | 28431174PubMed |
Chargo NJ, Robison CI, Baker SL, Toscano MJ, Makagon MM, Karcher DM (2019a) Keel bone damage assessment: consistency in enriched colony laying hens. Poultry Science 98, 1017–1022.
| Keel bone damage assessment: consistency in enriched colony laying hens.Crossref | GoogleScholarGoogle Scholar | 30165387PubMed |
Chargo NJ, Robison CI, Okaeze HO, Baker SL, Toscano MJ, Makagon MM, Karcher DM (2019b) Keel bone differences in laying hens housed in enriched colony cages. Poultry Science 98, 1031–1036.
| Keel bone differences in laying hens housed in enriched colony cages.Crossref | GoogleScholarGoogle Scholar | 30239903PubMed |
Donaldson CJ, Ball MEE, O’Connell NE (2012) Aerial perches and free-range laying hens: the effect of access to aerial perches and of individual bird parameters on keel one injuries in commercial free-range laying hens. Poultry Science 91, 304–315.
| Aerial perches and free-range laying hens: the effect of access to aerial perches and of individual bird parameters on keel one injuries in commercial free-range laying hens.Crossref | GoogleScholarGoogle Scholar | 22252341PubMed |
Donnelly E (2011) Methods for assessing bone quality: a review. Clinical Orthopaedics and Related Research 469, 2128–2138.
| Methods for assessing bone quality: a review.Crossref | GoogleScholarGoogle Scholar | 21116752PubMed |
Enneking SA, Cheng HW, Jefferson-Moore KY, Einstein ME, Rubin DA, Hester PY (2012) Early access to perches in caged White Leghorn pullets. Poultry Science 91, 2114–2120.
| Early access to perches in caged White Leghorn pullets.Crossref | GoogleScholarGoogle Scholar | 22912444PubMed |
Eusemann BK, Baulain U, Schrader L, Thöne-Reineke C, Patt A, Petow S (2018) Radiographic examination of keel bone damage in living laying hens of different strains kept in two housing systems. PLoS ONE 13, e0194974
| Radiographic examination of keel bone damage in living laying hens of different strains kept in two housing systems.Crossref | GoogleScholarGoogle Scholar | 29742164PubMed |
Eusemann BK, Patt A, Schrader L, Weigend S, Thöne-Reineke C, Petow S (2020) The role of egg production in the etiology of keel bone damage in laying hens. Frontiers in Veterinary Science 7, 81
| The role of egg production in the etiology of keel bone damage in laying hens.Crossref | GoogleScholarGoogle Scholar | 32154276PubMed |
Gebhardt-Henrich SG, Fröhlich EKF (2015) Early onset of laying and bumblefoot favour keel bone fractures. Animals 5, 1192–1206.
| Early onset of laying and bumblefoot favour keel bone fractures.Crossref | GoogleScholarGoogle Scholar | 26633520PubMed |
Gebhardt-Henrich SG, Pflug A, Fröhlich EKF, Käppeli S, Guggisberg D, Liesegang A, Stoffel MH (2017) Limited associations between keel bone damage and bone properties measured with computer tomography, three-point bending test, and analysis of minerals in Swiss laying hens. Frontiers in Veterinary Science 4, 128
| Limited associations between keel bone damage and bone properties measured with computer tomography, three-point bending test, and analysis of minerals in Swiss laying hens.Crossref | GoogleScholarGoogle Scholar | 28848740PubMed |
Grafl B, Polster S, Sulejmanovic B, Pürrer B, Guggenberger B, Hess M (2017) Assessment of health and welfare of Austrian laying hens at slaughter demonstrates influence of husbandry system and season. British Poultry Science 58, 209–215.
| Assessment of health and welfare of Austrian laying hens at slaughter demonstrates influence of husbandry system and season.Crossref | GoogleScholarGoogle Scholar | 28084805PubMed |
Gunnarsson S, Yngvesson J, Keeling LJ, Forkman B (2000) Rearing without early access to perches impairs the spatial skills of laying hens. Applied Animal Behaviour Science 67, 217–228.
| Rearing without early access to perches impairs the spatial skills of laying hens.Crossref | GoogleScholarGoogle Scholar | 10736530PubMed |
Habig C, Distl O (2013) Evaluation of bone strength, keel bone status, plumage condition and egg quality of two layer lines kept in small group housing systems. British Poultry Science 54, 413–424.
| Evaluation of bone strength, keel bone status, plumage condition and egg quality of two layer lines kept in small group housing systems.Crossref | GoogleScholarGoogle Scholar | 23906215PubMed |
Habig C, Baulain U, Hanning M, Scholz AM, Sharifi AR, Janisch S, Simianer H, Weigend S (2017) How bone stability in laying hens is affected by phylogenetic background and performance level. Archiv für Geflügelkunde 81, 1–17.
| How bone stability in laying hens is affected by phylogenetic background and performance level.Crossref | GoogleScholarGoogle Scholar |
Hardin E, Castro FLS, Kim WK (2019) Keel bone injury in laying hens: the prevalence of injuries in relation to different housing systems, implications, and potential solutions. World’s Poultry Science Journal 75, 285–292.
| Keel bone injury in laying hens: the prevalence of injuries in relation to different housing systems, implications, and potential solutions.Crossref | GoogleScholarGoogle Scholar |
Harlander-Matauschek A, Rodenburg TB, Sandilands V, Tobalske BW, Toscano MJ (2015) Causes of keel bone damage and their solutions in laying hens. World’s Poultry Science Journal 71, 461–472.
| Causes of keel bone damage and their solutions in laying hens.Crossref | GoogleScholarGoogle Scholar |
Heerkens JLT, Delezie E, Ampe B, Rodenburg TB, Tuyttens FAM (2016a) Ramps and hybrid effects on keel bone and foot pad disorders in modified aviaries for laying hens. Poultry Science 95, 2479–2488.
| Ramps and hybrid effects on keel bone and foot pad disorders in modified aviaries for laying hens.Crossref | GoogleScholarGoogle Scholar |
Heerkens JLF, Delezie E, Rodenburg TB, Kempen I, Zoons J, Ampe B, Tuyttens FAM (2016b) Risk factors associated with keel bone and footpad disorders in laying hens housed in aviary systems. Poultry Science 95, 482–488.
| Risk factors associated with keel bone and footpad disorders in laying hens housed in aviary systems.Crossref | GoogleScholarGoogle Scholar |
Heikkilä M, Wichman A, Gunnarsson S, Valros A (2006) Development of perching behaviour in chicks reared in enriched environment. Applied Animal Behaviour Science 99, 145–156.
| Development of perching behaviour in chicks reared in enriched environment.Crossref | GoogleScholarGoogle Scholar |
Hester PY (2014) The effect of perches installed in cages on laying hens. World’s Poultry Science Journal 70, 247–264.
| The effect of perches installed in cages on laying hens.Crossref | GoogleScholarGoogle Scholar |
Hester PY, Enneking SA, Haley BK, Cheng HW, Einstein ME, Rubin DA (2013) The effect of perch availability during pullet rearing and egg laying on musculoskeletal health of caged White Leghorn hens. Poultry Science 92, 1972–1980.
| The effect of perch availability during pullet rearing and egg laying on musculoskeletal health of caged White Leghorn hens.Crossref | GoogleScholarGoogle Scholar | 23873543PubMed |
Jung L, Niebuhr K, Hinrichsen LK, Gunnarsson S, Brenninkmeyer C, Bestman M, Heerkens J, Ferrari P, Knierim U (2019) Possible risk factors for keel bone damage in organic laying hens. Animal 13, 2356–2364.
| Possible risk factors for keel bone damage in organic laying hens.Crossref | GoogleScholarGoogle Scholar | 30808429PubMed |
Käppeli S, Gebhardt-Henrich SG, Fröhlich E, Pfulg A, Stoffel MH (2011a) Prevalence of keel bone deformities in Swiss laying hens. British Poultry Science 52, 531–536.
| Prevalence of keel bone deformities in Swiss laying hens.Crossref | GoogleScholarGoogle Scholar | 22029778PubMed |
Käppeli S, Gebhardt-Henrich SG, Fröhlich E, Pfulg A, Schäublin H, Stoffel MH (2011b) Effects of housing, perches, genetics, and 25-hydroxycholecalciferol on keel bone deformities in laying hens. Poultry Science 90, 1637–1644.
| Effects of housing, perches, genetics, and 25-hydroxycholecalciferol on keel bone deformities in laying hens.Crossref | GoogleScholarGoogle Scholar | 21753197PubMed |
Kerschnitzki M, Zander T, Zaslansky P, Fratzl P, Shahar R, Wagermaier W (2014) Rapid alterations of avian medullary bone material during the daily egg-laying cycle. Bone 69, 109–117.
| Rapid alterations of avian medullary bone material during the daily egg-laying cycle.Crossref | GoogleScholarGoogle Scholar | 25204794PubMed |
Kolakshyapati M, Flavel RJ, Sibanda TZ, Schneider D, Welch MC, Ruhnke I (2019) Various bone parameters are positively correlated with hen body weight while range access has no beneficial effect on tibia health of free-range layers. Poultry Science 98, 6241–6250.
| Various bone parameters are positively correlated with hen body weight while range access has no beneficial effect on tibia health of free-range layers.Crossref | GoogleScholarGoogle Scholar | 31504903PubMed |
Korver DR, Saunders-Blades JL, Nadeau KL (2004) Assessing bone mineral density in vivo: quantitative computed tomography. Poultry Science 83, 222–229.
| Assessing bone mineral density in vivo: quantitative computed tomography.Crossref | GoogleScholarGoogle Scholar | 14979573PubMed |
Kozak M, Tobalske B, Martins C, Bowley S, Wuerbel H, Harlander-Matauschek A (2016) Use of space by domestic chicks housed in complex aviaries. Applied Animal Behaviour Science 181, 115–121.
| Use of space by domestic chicks housed in complex aviaries.Crossref | GoogleScholarGoogle Scholar |
LeBlanc C, Tobalske B, Bowley S, Harlander-Matauschek A (2018) Development of locomotion over inclined surfaces in laying hens. Animal 12, 585–596.
| Development of locomotion over inclined surfaces in laying hens.Crossref | GoogleScholarGoogle Scholar | 28780926PubMed |
Li Z, Li Q, Wang S-J, Zhang L, Qiu J-Y, Wu Y, Zhou Z-L (2016) Rapid increase in carbonate in cortical bones of hens during laying period. Poultry Science 95, 2889–2894.
| Rapid increase in carbonate in cortical bones of hens during laying period.Crossref | GoogleScholarGoogle Scholar | 27287385PubMed |
Li X, Zhang D, Bryden WL (2017) Calcium and phosphorus metabolism and nutrition of poultry: are current diets formulated in excess? Animal Production Science 57, 2304–2310.
| Calcium and phosphorus metabolism and nutrition of poultry: are current diets formulated in excess?Crossref | GoogleScholarGoogle Scholar |
Meng F, Chen D, Li X, Li J, Bao J (2017) The effect of large or small furnished cages on behaviors and tibia bone of laying hens. Journal of Veterinary Behavior 17, 69–73.
| The effect of large or small furnished cages on behaviors and tibia bone of laying hens.Crossref | GoogleScholarGoogle Scholar |
Moinard C, Statham P, Green PR (2004) Control of landing flight by laying hens: implications for the design of extensive housing systems. British Poultry Science 45, 578–584.
| Control of landing flight by laying hens: implications for the design of extensive housing systems.Crossref | GoogleScholarGoogle Scholar | 15623208PubMed |
Nasr MAF, Nicol CJ, Murrell JC (2012a) Do laying hens with keel bone fractures experience pain? PLoS One 7, e42420
| Do laying hens with keel bone fractures experience pain?Crossref | GoogleScholarGoogle Scholar |
Nasr MAF, Murrell J, Wilkins LJ, Nicol CJ (2012b) The effect of keel fractures on egg-production parameters, mobility and behaviour in individual laying hens. Animal Welfare 21, 127–135.
| The effect of keel fractures on egg-production parameters, mobility and behaviour in individual laying hens.Crossref | GoogleScholarGoogle Scholar |
Nasr MAF, Browne WJ, Caplen G, Hothersall B, Murrell JC, Nicol CJ (2013a) Positive affective state induced by opioid analgesia in laying hens with bone fractures. Applied Animal Behaviour Science 147, 127–131.
| Positive affective state induced by opioid analgesia in laying hens with bone fractures.Crossref | GoogleScholarGoogle Scholar |
Nasr MAF, Murrell J, Nicol CJ (2013b) The effect of keel fractures on egg production, feed and water consumption in individual laying hens. British Poultry Science 54, 165–170.
| The effect of keel fractures on egg production, feed and water consumption in individual laying hens.Crossref | GoogleScholarGoogle Scholar |
Norman KI, Weeks CA, Pettersson IC, Nicol CJ (2018) The effect of experience of ramps at rear on the subsequent ability of layer pullets to negotiate a ramp transition. Applied Animal Behaviour Science 208, 92–99.
| The effect of experience of ramps at rear on the subsequent ability of layer pullets to negotiate a ramp transition.Crossref | GoogleScholarGoogle Scholar |
Olgun O, Aygun A (2016) Nutritional factors affecting the breaking strength of bone in laying hens. World’s Poultry Science Journal 72, 821–832.
| Nutritional factors affecting the breaking strength of bone in laying hens.Crossref | GoogleScholarGoogle Scholar |
Onbaşılar EE, Erdem E, Ünal N, Tunç AS, Kocakaya A, Yaranoğlu B (2016) Comparison of liver and bone health of two laying hen strains kept in different cage systems. Archiv für Geflügelkunde 80, 1–9.
| Comparison of liver and bone health of two laying hen strains kept in different cage systems.Crossref | GoogleScholarGoogle Scholar |
Petrik MT, Guerin MT, Widowski TM (2013) Keel fracture assessment of laying hens by palpation: inter-observer reliability and accuracy. Veterinary Record 173, 500
| Keel fracture assessment of laying hens by palpation: inter-observer reliability and accuracy.Crossref | GoogleScholarGoogle Scholar | 24162507PubMed |
Petrik MT, Guerin MT, Widowski TM (2015) On-farm comparison of keel fracture prevalence and other welfare indicators in conventional cage and floor-housed laying hens in Ontario, Canada. Poultry Science 94, 579–585.
| On-farm comparison of keel fracture prevalence and other welfare indicators in conventional cage and floor-housed laying hens in Ontario, Canada.Crossref | GoogleScholarGoogle Scholar | 25713398PubMed |
Pettersson IC, Weeks CA, Norman KI, Nicol CJ (2017) The ability of laying pullets to negotiate two ramp designs as measured by bird preference and behaviour. PeerJ 5, e4069
| The ability of laying pullets to negotiate two ramp designs as measured by bird preference and behaviour.Crossref | GoogleScholarGoogle Scholar | 29177116PubMed |
Pickel T, Schrader L, Scholz R (2011) Pressure load on keel bone and foot pads in perching laying hens in relation to perch design. Poultry Science 90, 715–724.
| Pressure load on keel bone and foot pads in perching laying hens in relation to perch design.Crossref | GoogleScholarGoogle Scholar | 21406354PubMed |
Regmi P, Deland TS, Steibel JP, Robison CI, Haut RC, Orth MW, Karcher DM (2015) Effect of rearing environment on bone growth of pullets. Poultry Science 94, 502–511.
| Effect of rearing environment on bone growth of pullets.Crossref | GoogleScholarGoogle Scholar | 25638471PubMed |
Regmi P, Smith N, Nelson N, Haut RC, Orth MW, Karcher DM (2016) Housing conditions alter properties of the tibia and humerus during the laying phase in Lohmann white Leghorn hens. Poultry Science 95, 198–206.
| Housing conditions alter properties of the tibia and humerus during the laying phase in Lohmann white Leghorn hens.Crossref | GoogleScholarGoogle Scholar | 26467011PubMed |
Regmi P, Nelson N, Haut RC, Orth MW, Karcher DM (2017a) Influence of age and housing systems on properties of tibia and humerus of Lohmann White hens: bone properties of laying hens in commercial housing systems. Poultry Science 96, 3755–3762.
| Influence of age and housing systems on properties of tibia and humerus of Lohmann White hens: bone properties of laying hens in commercial housing systems.Crossref | GoogleScholarGoogle Scholar | 28938787PubMed |
Regmi P, Cox G, Robison CI, Karcher DM (2017b) Correlation analysis of cortical geometry of tibia and humerus of white leghorns using clinical quantitative computed tomography and microcomputed tomography scans. Poultry Science 96, 2950–2955.
| Correlation analysis of cortical geometry of tibia and humerus of white leghorns using clinical quantitative computed tomography and microcomputed tomography scans.Crossref | GoogleScholarGoogle Scholar | 28371842PubMed |
Riber AB, Hinrichsen LK (2016) Keel-bone damage and foot injuries in commercial laying hens in Denmark. Animal Welfare 25, 179–184.
| Keel-bone damage and foot injuries in commercial laying hens in Denmark.Crossref | GoogleScholarGoogle Scholar |
Riber AB, Casey-Trott TM, Herskin MS (2018) The influence of keel bone damage on welfare of laying hens. Frontiers in Veterinary Science 5, 6
| The influence of keel bone damage on welfare of laying hens.Crossref | GoogleScholarGoogle Scholar | 29541640PubMed |
Richards GJ, Nasr MA, Brown SN, Szamocki EMG, Murrell J, Barr F, Wilkins LJ (2011) Use of radiography to identify keel bone fractures in laying hens and assess healing in live birds. Veterinary Record 169, 279
| Use of radiography to identify keel bone fractures in laying hens and assess healing in live birds.Crossref | GoogleScholarGoogle Scholar | 21831998PubMed |
Richards GJ, Wilkins LJ, Knowles TG, Booth F, Toscano MJ, Nicol CJ, Brown SN (2012) Pop hole use by hens with different keel fracture status monitored throughout the laying period. Veterinary Record 170, 494
| Pop hole use by hens with different keel fracture status monitored throughout the laying period.Crossref | GoogleScholarGoogle Scholar | 22447459PubMed |
Robison CI, Karcher DM (2019) Analytical bone calcium and bone ash from mature laying hens correlates to bone mineral content calculated from quantitative computed tomography scans. Poultry Science 98, 3611–3616.
| Analytical bone calcium and bone ash from mature laying hens correlates to bone mineral content calculated from quantitative computed tomography scans.Crossref | GoogleScholarGoogle Scholar | 31321433PubMed |
Rufener C, Baur S, Stratmann A, Toscano MJ (2018) A reliable method to assess keel bone fractures in laying hens from radiographs using a tagged visual analogue scale. Frontiers in Veterinary Science 5, 124
| A reliable method to assess keel bone fractures in laying hens from radiographs using a tagged visual analogue scale.Crossref | GoogleScholarGoogle Scholar | 29930948PubMed |
Rufener C, Baur S, Stratmann A, Toscano MJ (2019a) Keel bone fractures affect egg laying performance but not egg quality in laying hens housed in a commercial aviary system. Poultry Science 98, 1589–1600.
| Keel bone fractures affect egg laying performance but not egg quality in laying hens housed in a commercial aviary system.Crossref | GoogleScholarGoogle Scholar | 30481360PubMed |
Rufener C, Abreu Y, Asher L, Berezowski JA, Maximiano Sousa F, Stratmann A, Toscano MJ (2019b) Keel bone fractures are associated with individual mobility of laying hens in an aviary system. Applied Animal Behaviour Science 217, 48–56.
| Keel bone fractures are associated with individual mobility of laying hens in an aviary system.Crossref | GoogleScholarGoogle Scholar |
Sandilands V, Moinard C, Sparks NHC (2009) Providing laying hens with perches: fulfilling behavioural needs but causing injury? British Poultry Science 50, 395–406.
| Providing laying hens with perches: fulfilling behavioural needs but causing injury?Crossref | GoogleScholarGoogle Scholar | 19735008PubMed |
Scholz B, Rönchen S, Hamann H, Hewicker-Trautwein M, Distl O (2008) Keel bone condition in laying hens: a histological evaluation of macroscopically assessed keel bones. Berliner und Munchener Tierarztliche Wochenschrift 121, 89–94.
Scholz B, Rönchen S, Hamann H, Dist O (2009) Bone strength and keel bone status of two layer strains kept in small group housing systems with different perch configurations and group sizes. Berliner und Munchener Tierarztliche Wochenschrift 122, 249–256.
Shimmura T, Hirahara S, Azuma T, Suzuki T, Eguchi Y, Uetake K, Tanaka T (2010) Multifactorial investigation of various housing systems for laying hens. British Poultry Science 51, 31–42.
| Multifactorial investigation of various housing systems for laying hens.Crossref | GoogleScholarGoogle Scholar | 20390567PubMed |
Shipov A, Sharir A, Zelzer E, Milgram J, Monsonego-Ornan E, Shahar R (2010) The influence of severe prolonged exercise restriction on the mechanical and structural properties of bone in an avian model. The Veterinary Journal 183, 153–160.
| The influence of severe prolonged exercise restriction on the mechanical and structural properties of bone in an avian model.Crossref | GoogleScholarGoogle Scholar | 19135394PubMed |
Silversides FG, Singh R, Cheng KM, Korver DR (2012) Comparison of bones of 4 strains of laying hens kept in conventional cages and floor pens. Poultry Science 91, 1–7.
| Comparison of bones of 4 strains of laying hens kept in conventional cages and floor pens.Crossref | GoogleScholarGoogle Scholar | 22184423PubMed |
Stratmann A, Fröhlich EKF, Harlander-Matauschek A, Schrader L, Toscano MJ, Würbel H, Gebhardt-Henrich SG (2015a) Soft perches in an aviary system reduce incidence of keel bone damage in laying hens. PLoS One 10, e0122568
| Soft perches in an aviary system reduce incidence of keel bone damage in laying hens.Crossref | GoogleScholarGoogle Scholar | 25811980PubMed |
Stratmann A, Fröhlich EKF, Gebhardt-Henrich SG, Harlander-Matauschek A, Würbel H, Toscano MJ (2015b) Modification of aviary design reduces incidence of falls, collisions and keel bone damage in laying hens. Applied Animal Behaviour Science 165, 112–123.
| Modification of aviary design reduces incidence of falls, collisions and keel bone damage in laying hens.Crossref | GoogleScholarGoogle Scholar |
Stratmann A, Fröhlich EKF, Gebhardt-Henrich SG, Harlander-Matauschek A, Würbel H, Toscano MJ (2016) Genetic selection to increase bone strength affects prevalence of keel bone damage and egg parameters in commercially housed laying hens. Poultry Science 95, 975–984.
| Genetic selection to increase bone strength affects prevalence of keel bone damage and egg parameters in commercially housed laying hens.Crossref | GoogleScholarGoogle Scholar | 26944960PubMed |
Świątkiewicz S, Arczewska-Włosek A (2012) Prebiotic fructans and organic acids as feed additives improving mineral availability. World’s Poultry Science Journal 68, 269–279.
| Prebiotic fructans and organic acids as feed additives improving mineral availability.Crossref | GoogleScholarGoogle Scholar |
Świątkiewicz S, Arczewska-Włosek A, Szczurek W, Calik J, Krawczyk J, Józefiak D (2018) The influence of selected feed additives on mineral utilisation and bone characteristics in laying hens. Annals of Animal Science 18, 781–793.
| The influence of selected feed additives on mineral utilisation and bone characteristics in laying hens.Crossref | GoogleScholarGoogle Scholar |
Taylor AC, Horvat-Gordon M, Moore A, Bartell PA (2013) The effects of melatonin on the physical properties of bones and egg shells in the laying hen. PLoS One 8, e55663
| The effects of melatonin on the physical properties of bones and egg shells in the laying hen.Crossref | GoogleScholarGoogle Scholar | 24386079PubMed |
Thøfner I, Hougen HP, Villa C, Lynnerup N, Christensen JP (2020) Pathological characterization of keel bone fractures in laying hens does not support external trauma as the underlying cause. PLoS One 15, e0229735
| Pathological characterization of keel bone fractures in laying hens does not support external trauma as the underlying cause.Crossref | GoogleScholarGoogle Scholar | 32150551PubMed |
Toscano MJ, Booth F, Wilkins LJ, Avery NC, Brown SB, Richards G, Tarlton JF (2015) The effects of long (C20/22) and short (C18) chain omega-3 fatty acids on keel bone fractures, bone biomechanics, behavior, and egg production in free-range laying hens. Poultry Science 94, 823–835.
| The effects of long (C20/22) and short (C18) chain omega-3 fatty acids on keel bone fractures, bone biomechanics, behavior, and egg production in free-range laying hens.Crossref | GoogleScholarGoogle Scholar | 25771533PubMed |
Toscano M, Booth F, Richards G, Brown S, Karcher D, Tarlton J (2018) Modelling collisions in laying hens as a tool to identify causative factors for keel bone fractures and means to reduce their occurrence and severity. PLoS One 13, e0200025
| Modelling collisions in laying hens as a tool to identify causative factors for keel bone fractures and means to reduce their occurrence and severity.Crossref | GoogleScholarGoogle Scholar | 29990363PubMed |
Vaughan PE, Orth MW, Haut RC, Karcher DM (2016) A method of determining bending properties of poultry long bones using beam analysis and micro-CT data. Poultry Science 95, 207–212.
| A method of determining bending properties of poultry long bones using beam analysis and micro-CT data.Crossref | GoogleScholarGoogle Scholar | 26794840PubMed |
Webster AB (2004) Welfare implications of avian osteoporosis. Poultry Science 83, 184–192.
| Welfare implications of avian osteoporosis.Crossref | GoogleScholarGoogle Scholar | 14979568PubMed |
Wei H, Li C, Xin H, Li S, Bi Y, Li X, Li J, Zhang R, Bao J (2019) Keel fracture causes stress and inflammatory responses and inhibits the expression of the orexin system in laying hens. Animals 9, 804
| Keel fracture causes stress and inflammatory responses and inhibits the expression of the orexin system in laying hens.Crossref | GoogleScholarGoogle Scholar |
Whitehead CC (2004) Overview of bone biology in the egg-laying hen. Poultry Science 83, 193–199.
| Overview of bone biology in the egg-laying hen.Crossref | GoogleScholarGoogle Scholar | 14979569PubMed |
Whitehead CC, Fleming RH (2000) Osteoporosis in cage layers. Poultry Science 79, 1033–1041.
| Osteoporosis in cage layers.Crossref | GoogleScholarGoogle Scholar | 10901207PubMed |
Wilkins LJ, McKinstry JL, Avery NC, Knowles TG, Brown SN, Tarlton J, Nicol CJ (2011) Influence of housing system and design on bone strength and keel bone fractures in laying hens. Veterinary Record 169, 414
| Influence of housing system and design on bone strength and keel bone fractures in laying hens.Crossref | GoogleScholarGoogle Scholar | 21862469PubMed |
Yan FF, Hester PY, Cheng HW (2014) The effect of perch access during pullet rearing and egg laying on physiological measures of stress in White Leghorns at 71 weeks of age. Poultry Science 93, 1318–1326.
| The effect of perch access during pullet rearing and egg laying on physiological measures of stress in White Leghorns at 71 weeks of age.Crossref | GoogleScholarGoogle Scholar | 24879681PubMed |
