Infectious and non-infectious factors associated with leg disorders in poultry – a review

Open access

Abstract

Broiler chicken welfare, health and performance are strictly linked with skeleton development. Lameness compromises welfare of broiler chickens and causes considerable economic loss since lame birds have difficulty accessing feed and water, become dehydrated and eventually die. Leg disorders are therefore considered to be one of the main factors associated with in-field mortalities between 21-42 d in broiler rearing at European poultry farms. In chickens and other farm animals, bone development is strictly correlated with dietary content of inositol hexaphosphate (IP6), as well as calcium and phosphorus availability. However, lameness is also associated with many other factors, such as diseases, genetics, species, gender, growth, aging, as well as physical loading, rearing period and management. Therefore, the aim of the current paper is to review selected noninfectious and infectious factors, which contribute to bone quality in poultry.

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  • Abdelqader A. Al - Fataftah A.-R. Daş G. (2013). Effects of dietary Bacillus subtilis and inulin supplementation on performance eggshell quality intestinal morphology and microflora composition of laying hens in the late phase of production. Anim. Feed Sci. Tech. 179: 103-111.

  • Abrahamsson P. Tauson R. Appleby M. (1996). Behaviour health and integument of four hybrids of laying hens in modified and conventional cages. Brit. Poultry Sci. 37: 521-540.

  • Ajakaiye A. Atteh J. Leeson S. (2003). Biological availability of calcium in broiler chicks from different calcium sources found in Nigeria. Anim. Feed Sci. Tech. 104: 209-214.

  • Almeida Paz I. Garcia R. Bernardi R. Nääs I. Caldara F.R. Freitas L. Seno L. Ferreira V. Pereira D. Cavichiolo F. (2010). Selecting appropriate bedding to reduce locomotion problems in broilers. Revista Brasileira de Ciência Avícola 12: 189-195.

  • Andrews P.A. (1989). Disulfiram and histidine induce tibial dyschondroplasia in broiler chickens. Master's thesis University of Wisconsin Madison WI.

  • Angel R. (2007). Metabolic disorders: limitations to growth of and mineral deposition into the broiler skeleton after hatch and potential implications for leg problems. J. App. Poultry Res. 16: 138-149.

  • Applegate T. Lilburn M. (2002). Growth of the femur and tibia ofacommercial broiler line. Poultry Sci. 81: 1289-1294.

  • Belay T. Wiernusz C. Teeter R. (1992). Mineral balance and urinary and fecal mineral excretion profile of broilers housed in thermoneutral and heat-distressed environments. Poultry Sci. 71: 1043-1047.

  • Bizeray D. Estevez I. Leterrier C. Faure J. (2002). Influence of increased environmental complexity on leg condition performance and level of fearfulness in broilers. Poultry Sci. 81: 767-773.

  • Boling S.D. Webel D.M. Mavromichalis I. Parsons C.M. Baker D.H. (2000). The effects of citric acid on phytate-phosphorus utilization in young chicks and pigs. J. Anim. Sci. 78: 682-689.

  • Bolton W. Dewar W. (1965). The digestibility of acetic propionic and butyric acids by the fowl. Brit. Poultry Sci. 6: 103-105.

  • Boskey A. Wright T. Blank R. (1999). Collagen and bone strength. J. Bone Miner. Res. 14: 330-335.

  • Brickett K. Dahiya J. Classen H. Gomis S. (2007). Influence of dietary nutrient density feed form and lighting on growth and meat yield of broiler chickens. Poultry Sci. 86: 2172-2181.

  • Bruno L. Furlan R. Malheiros E. Macari M. (2000). Influence of early quantitative food restriction on long bone growth at different environmental temperatures in broiler chickens. Brit. Poultry Sci. 41: 389-394.

  • Bryła M. Waśkiewicz A. Podolska G. Szymczyk K. J ędrzejczak R. Damaziak K. Sułek A. (2016). Occurrence of 26 mycotoxins in the grain of cereals cultivated in Poland. Toxins 8 p. 160.

  • Butterworth A. (1999). Infectious components of broiler lameness:areview. World Poultry Sci. J. 55: 327-352.

  • Butterworth A. Haslam S.M. (2009). Alameness control strategy for broiler fowl. Welfare Quality reports No. 13. Available: http://www.welfarequality.net/everyone/44892/7/0/22

  • Charles D. Groom C. Bray T. (1981). The effects of temperature on broilers: interactions between temperature and feeding regime. Brit. Poultry Sci. 22: 475-481.

  • Charuta A. Cooper R.G. (2012). Computed tomographic and densitometric analysis of tibiotarsal bone mineral density and content in postnatal Peking ducks (Anas platyrhynchos var. domestica) as influenced by age and sex. Pol. J. Vet. Sci. 15: 537-545.

  • Charuta A. Cooper R.G. Pierzchała M. Horbańczuk J.O. (2012 a). Computed tomographic analysis of tibiotarsal bone mineral density and content in turkeys as influenced by age and sex. Czech J. Anim. Sci. 57: 573-80.

  • Charuta A. Dzierzęcka M. Czerwiński E. Cooper R.G. Horbańczuk J.O. (2012 b). Sex- and age-related changes of trabecular bone of tibia in growing domestic geese (Anser domesticus). Folia Biol. 60: 205-212.

  • Charuta A. Dzierzęcka M. Komosa M. Biesiada - Drzazga B. Działa-Szczepańczyk E. Cooper R.G. (2013 a). Age- and sex-related changes in mineral density and mineral content of the tibiotarsal bone in quails during post-hatching development. Kafkas Univ. Vet. Fak. Derg. 19: 31-36.

  • Charuta A. Dzierzęcka M. Komosa M. Kalinowski Ł. Pierzchała M. (2013 b). Age- and sex-related differences of morphometric densitometric and geometric parameters of tibiotarsal bone in Ross broiler chickens. Folia Biol. 61: 211-220.

  • Chowdhury R. Islam K. Khan M. Karim M. Haque M. Khatun M. Pesti G. (2009). Effect of citric acid avilamycin and their combination on the performance tibia ash and immune status of broilers. Poultry Sci. 88: 1616-1622.

  • Christensen V.L. Donalson W.E. Nestor K.E. (1994). Incubation temperature effects on metabolism and survival of turkey embryos. In: Proc. 9th European Poultry Conference. Vol. II. World’s Poultry Science Association Glasgow UK pp. 399-402

  • Church L.E. Johnson L.C. (1964). Growth of long bones in the chicken. Rates of growth in length and diameter of the humerus tibia and metatarsus. Am. J. Anat. 114: 521-538.

  • Classen H. Riddell C. (1989). Photoperiodic effects on performance and leg abnormalities in broiler chickens. Poultry Sci. 68: 873-879.

  • Classen H. Riddell C. Robinson F. (1991). Effects of increasing photoperiod length on performance and health of broiler chickens. Brit. Poultry Sci. 32: 21-29.

  • Cook M. (2000). Skeletal deformities and their causes: introduction. Poultry Sci. 79: 982-984.

  • Crespo R. Shivaprasad H.L. (2011). Developmental metabolic and other noninfectious disorders. In: Diseases of Poultry 12th edition Saif Y.M. Fadly A.M. Glisson J.R. Mc Dougald L.R. Nolan L.K. Swayne D.E. (eds) Blackwell Publishing Oxford UK pp. 1154-1156.

  • Dawkins M.S. Donnelly C.A. Jones T.A. (2004). Chicken welfare is influenced more by housing conditions than by stocking density. Nature 427: 342-344.

  • Deaton J. Reece F. Lott B. (1984). Effect of differing temperature cycles on broiler performance. Poultry Sci. 63: 612-615.

  • Deaton J. Reece F. Mc Naughton J. (1978). The effect of temperature during the growing period on broiler performance. Poultry Sci. 57: 1070-1074.

  • Decuypere E. Michels H. (1992). Incubation temperature asamanagement tool: Areview. World’s Poultry Sci. J. 48: 28-38.

  • Deng Y.F. Hou J.F. (2003). Effect of Gushukang on laying percentage and bone mineral content of cage layer. Anim. Husbandry Vet. Med. 35: 14-16.

  • Derache C. Labas V. Aucagne V. Meudal H. Landon C. Delmas A.F. Magallon T. Lalmanach A.-C. (2009). Primary structure and antibacterial activity of chicken bone marrow-derived β-defensins. Antimicrob. Agents Ch. 53: 4647-4655.

  • Derakhshanfar A. Kheirandish R. Alidadi S. Bidadkosh A. (2013). Study of long effects of administration of aspirin (acetylsalicylic acid) on bone in broiler chickens. Comparat. Clin. Pathol. 22: 1201-1204.

  • Dinev I. (2009). Clinical and morphological investigations on the prevalence of lameness associated with femoral head necrosis in broilers. Brit. Poultry Sci. 50: 284-290.

  • El Hussieny O. Creger C. (1981). Effect of ambient-temperature on minerals retention and balance of the broiler chicks. Poultry Sci. 60 (Suppl. 1): 1651-1651.

  • Englmaierova M. Skrivanova V. Skrivan M. (2014). The effect of non-phytate phosphorus and phytase levels on performance egg and tibia quality and p Hof the digestive tract in hens fed higher-calcium-content diets. Czech J. Anim Sci. 59: 107-115.

  • Etches R.J. (1987). Calcium logistics in the laying hen. J. Nutr. 117: 619-628.

  • FAO (2010). Poultry welfare in developing countries - Welfare issues in commercial broiler production. pp. 117-118. Available: http://www.fao.org/3/a-al723e.pdf

  • Falcone C. Mench J.A. Wakenell P. (2004). Can perches and platforms act the incidence of gait abnormalities in broiler chickens? J. Anim. Sci. 82 (Suppl. 1) p. 362.

  • Fleming R. Mc Cormack H. Whitehead C. (1998). Bone structure and strength at different ages in laying hens and effects of dietary particulate limestone vitamin Kand ascorbic acid. Brit. Poultry Sci. 39: 434-440.

  • Fleming R. Mc Cormack H. Mc Teir L. Whitehead C. (2004). Incidence pathology and prevention of keel bone deformities in the laying hen. Brit. Poultry Sci. 45: 320-330.

  • Fleming R. Mc Cormack H. Mc Teir L. Whitehead C. (2006). Relationships between genetic environmental and nutritional factors influencing osteoporosis in laying hens. Brit. Poultry Sci. 47: 742-755.

  • Fleming R.H. (2008). Nutritional factors affecting poultry bone health. P. Nutr. Soc. 67: 177-183.

  • French N.A. (1994). Do incubation temperature requirements vary between eggs? In: Proc. 9th European Poultry Conference. Vol II. World’s Poultry Science Association Glasgow UK pp. 395-398.

  • Garcia V. Catala - Gregori P. Hernandez F. Megias M.D. Madrid J. (2007). Effect of formic acid and plant extracts on growth nutrient digestibility intestine mucosa morphology and meat yield of broilers. J. App. Poultry Res. 16: 555-562.

  • Genin O. Hasdai A. Shinder D. Pines M. (2012). The effect of inhibition of heatshock proteins on thiram-induced tibial dyschondroplasia. Poultry Sci. 91: 1619-1626.

  • Gorski J.P. (1998). Is all bone the same? Distinctive distributions and properties of non-collagenous matrix proteins in lamellar vs. woven bone imply the existence of different underlying osteogenic mechanisms. Crit. Rev. Oral Biol. M. 9: 201-223.

  • Groves P.J. Muir W.I. (2016). Earlier hatching time predisposes Cobb broiler chickens to tibial dyschondroplasia. Animal 11: 112-120.

  • Guinotte F. Nys Y. (1991). Effects of particle size and origin of calcium sources on eggshell quality and bone mineralization in egg laying hens. Poultry Sci. 70: 583-592.

  • Hamilton P.B. Tung H.T. Wyatt R.D. Donaldson W.E. (1974). Interaction of dietary aflatoxin with some vitamin deficiencies. Poultry Sci. 53: 871-877.

  • Hammond C.L. Simbi B.H. Stickland N.C. (2007). In ovo temperature manipulation influences embryonic motility and growth of limb tissues in the chick (Gallus gallus). J. Exp. Biol. 210: 2667-2675.

  • Henry P. Ammerman C. Campbell D. Miles R. (1987). Effect of antibiotics on tissue trace mineral concentration and intestinal tract weight of broiler chicks. Poultry Sci. 66: 1014-1018.

  • Hocking P. (1993). Welfare of broiler breeder and layer females subjected to food and water control during rearing: Quantifying the degree of restriction. Brit. Poultry Sci. 34: 53-64.

  • Horvath- Papp I. (2008). Practical guide to broiler health management. BetüVet Limited pp. 375-381.

  • Houshmand M. Azhar K. Zulkifli I. Bejo M.H. Meimandipour A. Kamyab A. (2011). Effects of non-antibiotic feed additives on performance tibial dyschondroplasia incidence and tibia characteristics of broilers fed low-calcium diets. J. Anim. Physiol. Anim. Nutr. 95: 351-358.

  • Huff W. Moore P. Balog J. Bayyari G. Rath N. (1996). Evaluation of the toxicity of alum (aluminum sulfate) in young broiler chickens. Poultry Sci. 75: 1359-1364.

  • Huff W.E. Doerr J.A. Hamilton P.B. Hamann D.D. Peterson R.E. Ciegler A. (1980). Evaluation of bone strength during aflatoxicosis and ochratoxicosis. Appl. Environ. Microb. 40: 102-107.

  • Hulan H. Proudfoot F. (1987). Effects of light source ambient temperature and dietary energy source on the general performance and incidence of leg abnormalities of roaster chickens. Poultry Sci. 66: 645-651.

  • Hulet R. (2006). Managing incubation: Where are we and why? Poultry Sci. 80: 140-140.

  • Ingram D. Hattens L. Mc Pherson B. (2000). Effects of light restriction on broiler performance and specific body structure measurements. J. Appl. Poultry Res. 9: 501-504.

  • Iqbal T. Lewis K. Cooper B. (1994). Phytase activity in the human and rat small intestine. Gut 35: 1233-1236.

  • Irani M. Gharahveysi S. Zamani M. Rahmatian R. (2011). The effect of butyric acid glycerides on performance and some bone parameters of broiler chickens. Afr. J. Biotechnol. 10: 12812-12818.

  • Jamroz D. Wertelecki T. Żyłka R. (2007). The retention of mineral substances quality and chemical composition of bones of chickens fed diets containing different calcium and phosphorus levels. Electr. J. Polish Agricult. Univ. 10 p. 04

  • Johnson N. Harland B. Ross E. Gautz L. Dunn M. (1992). Effects of dietary aluminum and niacin on chick tibiae. Poultry Sci. 71: 1188-1195.

  • Joseph N. Moran E. (2005). Effect of flock age and postemergent holding in the hatcher on broiler live performance and further-processing yield. J. Appl. Poultry Res. 14: 512-520.

  • Käppeli S. Gebhardt - Henrich S. Fröhlich E. Pfulg A. Schäublin H. Stoffel M. (2011). Effects of housing perches genetics and 25-hydroxycholecalciferol on keel bone deformities in laying hens. Poultry Sci. 90: 1637-1644.

  • Katono T. Kawato T. Tanabe N. Suzuki N. Iida T. Morozumi A. Ochiai K. Maeno M. (2008). Sodium butyrate stimulates mineralized nodule formation and osteoprotegerin expression by human osteoblasts. Arch. Oral Biol. 53: 903-909.

  • Kaukonen E. Norring M. Valros A. (2016). Perches and elevated platforms in commercial broiler farms: use and effect on walking ability incidence of tibial dyschondroplasia and bone mineral content. Animal pp. 1-8.

  • Kense M. Landman W.J. (2011). Enterococcus cecorum infections in broiler breeders and their offspring: molecular epidemiology. Avian Pathol. 40: 603-612.

  • Kierończyk B. Rawski M. Długosz J. Świątkiewicz S. Józefiak D. (2016). Avian crop function -areview. Ann. Anim. Sci. 16: 653-678.

  • Kirn B. Firman J. (1993). Leg strength and performance of large white tom turkeys fed various protein and energy levels. Avian Dis. 37: 37-46.

  • Klasing K. (1998). Nutritional modulation of resistance to infectious diseases. Poultry Sci. 77: 1119-1125.

  • Knott L. Bailey A. (1998). Collagen cross-links in mineralizing tissues:areview of their chemistry function and clinical relevance. Bone 22: 181-187.

  • Knott L. Whitehead C.C. Fleming R. Bailey A. (1995). Biochemical changes in the collagenous matrix of osteoporotic avian bone. Biochem. J. 310: 1045-1051.

  • Knowles T.G. Kestin S.C. Haslam S.M. Brown S.N. Green L.E. Butterworth A. Pope S.J. Pfeiffer D. Nicol C.J. (2008). Leg disorders in broiler chickens: prevalence risk factors and prevention. PLo S One 3: e1545.

  • Koreleski J. Świątkiewicz S. (2005). Efficacy of different levels ofacholecalciferol 25-OHderivative in diets with two limestone forms in laying hen nutrition. J. Anim. Feed Sci. 14: 305-315.

  • Laing P. (1976). Lameness and leg weakness in rapidly growing turkeys associated with hip lesions. Vet. Rec. 99: 391-392.

  • Langenfeld M.S. (1992). Anatomy of the Hen. Wydawnictwo Naukowe PWN (in Polish).

  • Lee Y.W. Mirocha C.J. Shroeder D.J. Walser M.M. (1985). TDP-1atoxic component causing tibial dyschondroplasia in broiler chickens and trichothecenes from Fusarium roseum 'Graminearum'. Appl. Environ. Microb. 50: 102-107.

  • Lemus J. Blanco G. Arroyo B. Martinez F. Grande J. (2009). Fatal embryo chondral damage associated with fluoroquinolones in eggs of threatened avian scavengers. Environ. Pollut. 157: 2421-2427.

  • Levenick C. Leighton A. (1988). Effects of photoperiod and filtered light on growth reproduction and mating behavior of turkeys. 1. Growth performance of two lines of males and females. Poultry Sci. 67: 1505-1513.

  • Lewis N. Hurnik J. (1990). Locomotion of broiler chickens in floor pens. Poultry Sci. 69: 1087-1093.

  • Lilburn M.S. (1994). Skeletal growth of commercial poultry species. Poultry Sci. 73: 897-903.

  • Lundy M.W. Russell J.E. Avery J. Wergedal J.E. Baylink D.J. (1992). Effect of sodium fluoride on bone density in chickens. Calcified Tissue Int. 50: 420-426.

  • Lynn D.J. Higgs R. Gaines S. Tierney J. James T. Lloyd A.T. Fares M.A. Mulcahy G. O ’ Farrelly C. (2004). Bioinformatic discovery and initial characterisation of nine novel antimicrobial peptide genes in the chicken. Immunogenetics 56: 170-177.

  • Martland M. (1984). Wet litter asacause of plantar pododermatitis leading to foot ulceration and lameness in fattening turkeys. Avian Pathol. 13: 241-252.

  • Mc Lean K.A. Baxter M.R. Michie W. (1986). Comparison of the welfare of laying hens in battery cages and inaperchery. Res. Dev. Agric. 3: 93-98.

  • Mc Namee P. Mc Cullagh J. Thorp B. Ball H. Graham D. Mc Cullough S. Mc Conaghy D. Smyth J. (1998). Study of leg weakness in two commercial broiler flocks. Vet. Rec. 143 p. 131.

  • Mc Namee P.T. (1998). Investigation of bacterial chondronecrosis with osteomyelitis in broiler chickens. Doctor of Philosophy thesis. The Queen's University of Belfast Northern Ireland UK.

  • Mc Namee P.T. Smyth J.A. (2000). Bacterial chondronecrosis with osteomyelitis (‘femoral head necrosis’) of broiler chickens:areview. Avian Pathol. 29: 477-495.

  • Mc Namee P.T. Mc Cullagh J. Rodgers J. Thorp B. Ball H. Connor T. Mc Conaghy D. Smyth J.A. (1999). Development of an experimental model of bacterial chondronecrosis with osteomyelitis in broilers following exposure to Staphylococcus aureus by aerosol and inoculation with chicken anaemia and infectious bursal disease viruses. Avian Pathol. 28: 26-35.

  • Meijerhof R. (2002). Design and operation of commercial incubators. In: Practical Aspects of Commercial Incubation. Deeming D.C. (eds). Ratite Conference Books Lincolnshire UK pp. 41-46.

  • Mench J. (2002). Broiler breeders: feed restriction and welfare. World Poultry Sci. J. 58: 23-29.

  • Mituniewicz T. (2014). Water quality in poultry breeding. Ogólnopolski Informator Drobiarski 272: 20-24 (in Polish).

  • Mutalib A. Riddell C. Osborn A. (1983). Studies on the pathogenesis of staphylococcal osteomyelitis in chickens. II. Role of the respiratory tract asaroute of infection. Avian Dis. 27: 157-160.

  • Mutuş R. Kocabağli N. Alp M. Acar N. Eren M. Gezen Ş. (2006). The effect of dietary probiotic supplementation on tibial bone characteristics and strength in broilers. Poultry Sci. 85: 1621-1625.

  • Nahashon S. Nakaue H. Mirosh L. (1994). Production variables and nutrient retention in single comb White Leghorn laying pullets fed diets supplemented with direct-fed microbials. Poultry Sci. 73: 1699-1711.

  • Newberry R. Hunt J. Gardiner E. (1988). Influence of light intensity on behavior and performance of broiler chickens. Poultry Sci. 67: 1020-1025.

  • Nicoll T. Jensen M. (1987 a). Preliminary studies on bacterial interference of staphylococcosis of chickens. Avian Dis. 31: 140-144.

  • Nicoll T. Jensen M. (1987 b). Staphylococcosis of turkeys. 5. Large-scale control programs using bacterial interference. Avian Dis. 31: 85-88.

  • Nielsen B.L. Litherland M. Nøddegaard F. (2003). Effects of qualitative and quantitative feed restriction on the activity of broiler chickens. Appl. Anim. Behav. Sci. 83: 309-323.

  • Nigg B.M. Grimstone S.K. (1994). Bone. In: Biomechanics of Musculoskeletal System. Nigg B.M. Herzog W. (eds) John Wiley & Sons New York NY pp. 48-78.

  • North M.O. Bell D.D. (1990). Light systems for broilers. In: Commercial Chicken Production Manual Chapman & Hall New York and London pp. 472-473.

  • Ogan M. Petek M. Balci F. (1999). Effects of different lighting programs on the performance of broilers. J. Fac. Vet. Med. Univ. Uludag 18: 1-10 (in Turkish).

  • Okiki P.A. Ojeizeh T.I. Ogbimi A.O. (2010). Effects of feeding diet rich in mycotoxins on the health and growth performances of broiler chicken. Int. J. Poultry Sci. 9: 1136-1139.

  • Orth M.W. Bai Y. Zeytun I.H. Cook M.E. (1992). Excess levels of cysteine and homocysteine induce tibial dyschondroplasia in broiler chicks. J. Nutr. 122: 482-487.

  • Oso A. Idowu A. Niameh O. (2011). Growth response nutrient and mineral retention bone mineralisation and walking ability of broiler chickens fed with dietary inclusion of various unconventional mineral sources. J. Anim. Physiol. Anim. N. 95: 461-467.

  • Osphal W. Zeronian H. Ellison M. Lewis D. Rucker R.S. Riggins R. (1982). Role of copper in collagen-linking and its influence on selected mechanical properties of chick bone and tendon. J. Nutr. 12: 708-716.

  • Oviedo - Rondón E.O. Ferket P.R. (2005). Nutritional factors that affect leg problems in meat poultry: Areview. Proc. Ann. Carolina Poult. Nutr. Conf. Research Triangle Park NC. North Carolina State University Raleigh pp. 58-88.

  • Oviedo - Rondón E. Small J. Wineland M. Christensen V. Grimes J. Funderburk S. Ort D. Mann K. (2008). Effects of incubator temperature and oxygen concentration during the plateau stage of oxygen consumption on turkey embryo long bone development. Poultry Sci. 87: 1484-1492.

  • Oviedo - Rondón E. Wineland M. Funderburk S. Small J. Cutchin H. Mann M. (2009 a). Incubation conditions affect leg health in large high-yield broilers. J. App. Poultry Res. 18: 640-646.

  • Oviedo - Rondón E. Wineland M. Small J. Cutchin H. Mc Elroy A. Barri A. Martin S. (2009 b). Effect of incubation temperatures and chick transportation conditions on bone development and leg health. J. App. Poultry Res. 18: 671-678.

  • Oznurlu Y. Celik I. Sur E. Ozaydın T. Oğuz H. Altunbaş K. (2012). Determination of the effects of aflatoxin B1 given in ovo on the proximal tibial growth plate of broiler chickens: histological histometric and immunohistochemical findings. Avian Pathol. 41: 469-477.

  • Padron M. (1990). Salmonella typhimurium outbreak in broiler chicken flocks in Mexico. Avian Dis. 34: 221-223.

  • Panda A.K. Rao S.V.R. Raju M.V. Sharma S.R. (2006). Dietary supplementation of Lactobacillus sporogenes on performance and serum biochemico-lipid profile of broiler chickens. J. Poultry Sci. 43: 235-240.

  • Pastore S.M. Gomes P.C. Rostagno H.S. Albino L.F.T. Calderano A.A. Vellasco C.R. Da Silva Viana G. Almeida R.L.D. (2012). Calcium levels and calcium: available phosphorus ratios in diets for white egg layers from 42 to 58 weeks of age. Rev. Bras. Zoot. 41: 2424- 2432.

  • Pastorelli L. De Salvo C. Mercado J.R. Vecchi M. Pizarro T.T. (2013). Central role of the gut epithelial barrier in the pathogenesis of chronic intestinal inflammation: lessons learned from animal models and human genetics. Front. Immunol. 4 p. 280.

  • Pattison M. (2008). Poultry Diseases. 6th ed. Elsevier Edinburgh.

  • Petersen V.E. Jensen O. (1983). Halm høvlspaaner eller makuleret avispapir som strøelse til slagtekyllinger (in Danish). In: Statens Husdyrbrugsforsøg Meddelelse Denmark 522: 1-4.

  • Phillips C.J.C. (1992). Environmental factors influencing the production and welfare of farm animals: Photoperiod. In: Farm Animals and the Environment. Phillips C.J.C. Piggins D. (eds) CAB International Oxford UK pp. 49-65.

  • Pierson F.W. Hester P.Y. Wilson E.K. (1981). The effect of caponization and dietary 17 α-methyltestosterone on the incidence of leg abnormalities in turkeys. Poultry Sci. 60: 2144-2149.

  • Pinchasov Y. Elmaliah S. (1995). Broiler chick responses to anorectic agents: dietary acetic and propionic acids and the blood metabolites. Ann. Nutr. Metab. 39: 107-116.

  • Pintar J. Bujan M. Homen B. Gazic K. Sikiric M. Cerny T. (2005). Effects of supplemental phytase on the mineral content in tibia of broilers fed different cereal based diets. Czech J. Anim. Sci. 50: 68-73.

  • Plavnik I. Scott M. L. (1980). Effects of additional vitamins minerals or brewers yeast upon leg weaknesses in broiler chickens. Poultry Sci. 59: 459-464.

  • Prayitno D. Phillips C. (1997). Equating the perceived brightness of blue and red lights to hens. Brit. Poultry Sci. 38: 136-141.

  • Ptak A. Józefiak D. Kierończyk B. Rawski M. Żyła K. Świątkiewicz S. (2013). Effect of different phytases on the performance nutrient retention and tibia composition in broiler chickens. Archiv. Tierzucht 56: 1028-1038.

  • Rajput I.R. Hussain A. Li Y.L. Zhang X. Xu X. Long M.Y. You D.Y. Li W.F. (2014). Saccharomyces boulardii and Bacillus subtilis B10 modulate TLRs mediated signaling to induce immunity by chicken BMDCs. J. Cell. Biochem. 115: 189-198.

  • Rao S.R. Raju M. Reddy M. Pavani P. (2006). Interaction between dietary calcium and nonphytate phosphorus levels on growth bone mineralization and mineral excretion in commercial broilers. Anim. Feed Sci. Tech. 131: 135-150.

  • Rath N. Balog J. Huff W. Huff G. Kulkarni G. Tierce J. (1999). Comparative differences in the composition and biomechanical properties of tibiae of seven-and seventy-two-week-old male and female broiler breeder chickens. Poultry Sci. 78: 1232-1239.

  • Rath N. Huff G. Huff W. Balog J. (2000). Factors regulating bone maturity and strength in poultry. Poultry Sci. 79: 1024-1032.

  • Rath N.C. Huff W.E. Balog J.M. Huff G.R. (2004). Comparative efficacy of different dithiocarbamates to induce tibial dyschondroplasia in poultry. Poultry Sci. 83: 266-274.

  • Rath N.C. Huff W.E. Huff G.R. Kannan L. (2007). Induction of tibial dyschondroplasia by carbamate and thiocarbamate pesticides. Avian Dis. 51: 590-593.

  • Rath N.C. Rasaputra K.S. Liyanage R. Huff G.R. Huff W.E. (2011). Dithiocarbamate toxicity - an appraisal. Pesticides in the Modern World - Effects of Pesticides Exposure Stoytcheva M. (eds) In Tech Publishing Online New York pp. 323-340.

  • Reginatto A.R. Menconi A. Londero A. Lovato M. Rosa A.P. Shivaramaiah S. Wolfenden A.D. Huff W.E. Huff G.R. Rath N.C. Donoghue A.M. Hargis B.M. Tellez G. (2011). Effects of dietary aspergillus meal prebiotic on turkey poults production parameters and bone qualities. Int. J. Poultry Sci. 10: 496-499.

  • Reiter K. Bessei W. (1995). Influence of running on leg weakness of slow and fast growing broilers. In: Proceedings of the 29th International Congress for Applied Ethology Exeter pp. 211-213.

  • Reiter K. Bessei W. (1996). Effect of the distance between feeder and drinker on behaviour and leg disorders of broilers. In: Proceedings of the 30th International Congress of the International Society for Applied Ethology: 14-17 August 1996 Guelph Ontario Canada.

  • Rennie J. Fleming R. Mc Cormack H. Mc Corquodale C. Whitehead C. (1997). Studies on effects of nutritional factors on bone structure and osteoporosis in laying hens. Brit. Poultry Sci. 38: 417-424.

  • Riggs C. Vaughan L. Evans G. Lanyon L. Boyde A. (1993). Mechanical implications of collagen fibre orientation in cortical bone of the equine radius. Anatomy and embryology 187: 239-248.

  • Rosenberger J. Olson N. (1991). Reovirus infections. In: Diseases of Poultry 9th ed. Calnek B.W. (ed.) pp. 639-646.

  • Ross E. Yacowitz H. (1954). Effect of penicillin on growth and bone ash of chicks fed different levels of vitamin Dand phosphorus. Poultry Sci. 33: 262-265.

  • Sandilands V. Tolkamp B.J. Kyriazakis I. (2005). Behaviour of food restricted broilers during rearing and lay - effects of an alternative feeding method. Physiol. Behav. 85: 115-123.

  • Saunders - Blades J. Mac Isaac J. Korver D. Anderson D. (2009). The effect of calcium source and particle size on the production performance and bone quality of laying hens. Poultry Sci. 88: 338-353.

  • Savory C. Hocking P. Mann J. Maxwell M. (1996). Is broiler breeder welfare improved by using qualitative rather than quantitative food restriction to limit growth rate? Anim. Welfare 5: 105-127.

  • Savory C.J. Maros K. (1993). Influence of degree of food restriction age and time of day on behaviour of broiler breeder chickens. Behav. Processes 29: 179-189.

  • Scott M. Hull S. Mullenhoff P. (1971). The calcium requirements of laying hens and effects of dietary oyster shell upon egg shell quality. Poultry Sci. 50: 1055-1063.

  • Scott T. (2002). Evaluation of lighting programs diet density and short term use of mash as compared to crumbled starter to reduce incidence of sudden death syndrome in broiler chicks to 35dof age. Can. J. Anim. Sci. 82: 375-383.

  • Seifert M.F. Watkins B.A. (1997). Role of dietary lipid and antioxidants in bone metabolism. Nutr. Res. 17: 1209-1228.

  • Shim M. Pesti G. (2011). Effects of incubation temperature on the bone development of broilers. Poultry Sci. 90: 1867-1877.

  • Shim M.Y. (2010). Leg problems of modern broilers as affected by incubation temperature fluoride and fast growth. Doctor of Philosophy thesis. The University of Georgia.

  • Siegel H. Drury L. Patterson W. (1973). Bone characteristics and growth of broilers housed in plastic coops or on moderate and high temperatures 4th European Poultry Conference London England pp. 159-164.

  • Simmons P. (1982). Effect of lighting regimes on twisted legs feed conversion and growth of broiler chickens. Poultry Sci. 61: 1546-1546.

  • Škrbić Z. Pavlovski Z. Vitorović D. Lukić M. Petričević V. (2009). The effects of stocking density and light program on tibia quality of broilers of different genotype. Archiva Zootechnica 12: 3-56.

  • Soares J. Kerr J. Gray R. (1995). 25-hydroxycholecalciferol in poultry nutrition. Poultry Sci. 74: 1919-1934.

  • Soltan M. (2008). Effect of dietary organic acid supplementation on egg production egg quality and some blood serum parameters in laying hens. Int. J. Poultry Sci. 7: 613-621.

  • Štofaníková J. Šály J. Molnár L. Sesztáková E. Bílek J. (2011). The influence of dietary zinc content on mechanical properties of chicken tibiotarsal bone. Acta Vet. 61: 531-541.

  • Su G. Sørensen P. Kestin S.C. (1999). Meal feeding is more effective than early feed restriction at reducing the prevalence of leg weakness in broiler chickens. Poultry Sci. 78: 949- 955.

  • Su G. Sørensen P. Kestin S. (2000). Anote on the effects of perches and litter substrate on leg weakness in broiler chickens. Poultry Sci. 79: 1259-1263.

  • Subapriya S. Vairamuthu S. Manohar B.M. Balachandran C. (2007). Pathomorphological changes in thiram toxicosis in broiler chicken. Int. J. Poultry Sci. 6: 251-254.

  • Sullivan T.W. (1994). Skeletal problems in poultry: estimated annual cost and descriptions. Poultry Sci. 73: 879-882.

  • Sun Q. Guo Y. Li J. Zhang T. Wen J. (2012). Effects of methionine hydroxy analog chelated Cu/Mn/Zn on laying performance egg quality enzyme activity and mineral retention of laying hens. J. Poultry Sci. 49: 20-25.

  • Svihus B. Sacranie A. Denstadli V. Choct M. (2010). Nutrient utilization and functionality of the anterior digestive tract caused by intermittent feeding and inclusion of whole wheat in diets for broiler chickens. Poultry Sci. 89: 2617-2625.

  • Svihus B. Lund V. Borjgen B. Bedford M. Bakken M. (2013). Effect of intermittent feeding structural components and phytase on performance and behaviour of broiler chickens. Brit. Poultry Sci. 54: 222-230.

  • Swick R. Ivey F. (1990). Effect of dietary phytase addition on broiler performance in phosphorus deficient diets. Poultry Sci. 69: 133.

  • Świątkiewicz S. Koreleski J. (2008). The effect of zinc and manganese source in the diet for laying hens on eggshell and bones quality. Vet. Med-Czech. 53: 555-563.

  • Świątkiewicz S. Korelewski J. Arczewska- Włosek A. (2010). Effect of prebiotic fructans and organic acids on mineral retention in laying hens. Acta Agric. Scand. A Anim. Sci. 60: 125-128.

  • Świątkiewicz S. Arczewska- Włosek A. Jozefiak D. (2014). The efficacy of organic minerals in poultry nutrition: review and implications of recent studies. World’s Poultry Sci. J. 70: 475-486.

  • Thorp B. Whitehead C. Dick L. Bradbury J. Jones R. Wood A. (1993). Proximal femoral degeneration in growing broiler fowl. Avian Pathol. 22: 325-342.

  • Toghyani M. Toghyani M. Tavalaeian E. Mohammadrezaei M. (2011). Effect of wet and sequential feeding subsequent to early skipaday feeding on leg weakness in broiler chicks. 9th Asia Pacific Poultry Congress At Taiwan.

  • Tona K. Onagbesan O. Jego Y. Kamers B. Decuypere E. Bruggeman V. (2004). Comparison of embryo physiological parameters during incubation chick quality and growth performance of three lines of broiler breeders differing in genetic composition and growth rate. Poultry Sci. 83: 507-513.

  • Tona K. Onagbesan O.M. Kamers B. Everaert N. Bruggeman V. Decuypere E. (2010). Comparison of Cobb and Ross strains in embryo physiology and chick juvenile growth. Poultry Sci. 89: 1677-1683.

  • Tucker S.A. Walker A.W. (1992). Hock burn in broilers. In: Recent Advances in Animal Nutrition. Garnsworthy P.C. Haresign W. Cole J.D.A. (eds). Butterworth Heinemann Oxford the United Kingdom pp. 33−49.

  • Turek S.L. (1984). Mineralization of bone. In: Orthopaedics: Principles and Their Application. Vol. I. Lippincot J.B. (ed.) Philadelphia PA pp. 164-179.

  • Vander Heide L. Lütticken D. Horzinek M. (1981). Isolation of avian reovirus as a possible etiologic agent of osteoporosis (“brittle bone disease”; “femoral head necrosis”) in broiler chickens. Avian Dis. 25: 847-856.

  • Viveros A. Brenes A. Arija I. Centeno C. (2002). Effects of microbial phytase supplementation on mineral utilization and serum enzyme activities in broiler chicks fed different levels of phosphorus. Poultry Sci. 81: 1172-1183.

  • Wang X. Fosmire G.J. Gay C.V. Leach R.M. (2002). Short-term zinc deficiency inhibits chondrocyte proliferation and induces cell apoptosis in the epiphyseal growth plate of young chickens. J. Nutr. 132: 665-673.

  • Wideman R. Hamal K. Stark J. Blankenship J. Lester H. Mitchell K. Lorenzoni G. Pevzner I. (2012). Awire-flooring model for inducing lameness in broilers: Evaluation of probiotics asaprophylactic treatment. Poultry Sci. 91: 870-883.

  • Wideman R.F. Al - Rubaye A. Reynolds D. Yoho D. Lester H. Spencer C. Hughes J.D. Pevzner I. Y. (2014). Bacterial chondronecrosis with osteomyelitis in broilers: Influence of sires and straight-run versus sex-separate rearing. Poultry Sci. 93: 1675-1687.

  • Wiedmer H. Hadorn R. (1996). Broilermast: Welche Einstreu ist die beste? DGS Magazin Woche 27: 17-18.

  • Wilson H.R. (1991). Physiological requirements of developing embryo: Temperature and turning. In: Avian Incubation. Tullet S.G. (ed.) Butterworth-Heinemann Oxford UK pp. 145-156.

  • Wilson J. Ruszler P. (1998). Long term effects of boron on layer bone strength and production parameters. Brit. Poultry Sci. 39: 11-15.

  • Wilson J. Weaver W. Beane W. Cherry J. (1984). Effects of light and feeding space on leg abnormalities in broilers. Poultry Sci. 63: 565-567.

  • Wise D. Ranaweera K. (1978). Shaky leg syndrome and hip lesions in turkeys. Vet. Rec. 103: 206-209.

  • Wolfenson D. Sklan D. Graber Y. Kedar O. Bengal I. Hurwitz S. (1987). Absorption of protein fatty acids and minerals in young turkeys under heat and cold stress. Brit. Poultry Sci. 28: 739-742.

  • Wu W. Li G. Liu T. Vesonder R.R. (1995). The effect of fumonisin B1 on isolated chondrocytes and on bone formation. Poultry Sci. 74: 1431-1436.

  • Xin H. Harmon J.D. (1996). Responses of group-housed neonatal chicks to posthatch holding environment. Transactions of the ASAE 39 p. 2249.

  • Xin H. Rieger S.R. (1995). Physical conditions and mortalities associated with international air transport of young chicks. T. ASAE. 38 p. 1863.

  • Yair R. Uni Z. (2011). Content and uptake of minerals in the yolk of broiler embryos during incubation and effect of nutrient enrichment. Poultry Sci. 90: 1523-1531.

  • Yalçin S. Molayoğlu H.B. Baka M. Genin O. Pines M. (2007). Effect of temperature during the incubation period on tibial growth plate chondrocyte differentiation and the incidence of tibial dyschondroplasia. Poultry Sci. 86: 1772-1783.

  • Yang H. Xing H. Wang Z. Xia J. Wan Y. Hou B. Zhang J. (2015). Effects of intermittent lighting on broiler growth performance slaughter performance serum biochemical parameters and tibia parameters. Ital. J. Anim. Sci. 14 p. 4143.

  • Yi Z. Kornegay E. Denbow D. (1996). Supplemental microbial phytase improves zinc utilization in broilers. Poultry Sci. 75: 540-546.

  • Zhou Z.L. Deng Y.F. Tao Q.S. Hu Y.F. Hou J.F. (2009). Effects of Gushukanga Chinese herbal medicine on bone characteristics and osteoporosis in laying hens. Poultry Sci. 88: 2342-2345.

  • Ziaie H. Bashtani M. Torshizi M.K. Naeeimipour H. Farhangfar H. Zeinali A. (2011). Effect of antibiotic and its alternatives on morphometric characteristics mineral content and bone strength of tibia in Ross broiler chickens. Global Vet. 7: 315-322.

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