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Rapid growth problems: ascites and skeletal deformities in broilers
Rapid Growth Problems: Ascites and Skeletal Deformities in Broilers R. J. JULIAN1 Department of Pathology, Ontario Veterinary College, University of Guelph, Guelph, Ontario, Canada, N1G 2W1 death produce high mortality in turkeys. Rapid growth induced by high nutrient intake alone can cause severe lameness, bone defects, and deformity, as these problems are seen in animals that have not been selected for rapid growth: dogs, horses, pigs, ratites and wild birds kept in zoologic gardens. In meat-type poultry, growth-related disease can be reduced or eliminated by reducing feed intake without affecting final body weight. Rapid growth alone may not be the pathogenic mechanism that results in cardiovascular or musculoskeletal defects. Metabolic imbalance induced by high nutrient intake may cause some of the conditions. These metabolic problems might be corrected without reducing growth rate.
(Key words: ascites, broiler, metabolic disease, rapid growth, skeletal deformity) 1998 Poultry Science 77:1773–1780
INTRODUCTION Rapid growth and heavy body weight, particularly associated with a small skeletal frame, have been implicated in musculoskeletal and cardiovascular disease in meat-type poultry (Riddell, 1992; Julian, 1993; Lilburn, 1994). Research on these conditions has frequently produced contradictory results. Although many of the problems can be reduced or eliminated by slowing growth rate, rapid growth and weight do not necessarily result in disease. Perhaps we should consider whether some of these problems are the result of metabolic imbalances associated with rapid growth and should be more correctly called metabolic disease.
ASCITES Ascites caused by valvular insufficiency and right ventricular failure (RVF) following right ventricular dilation and hypertrophy from pulmonary hypertension (PH) has become a prominent cause of illness, death, and condemnation in meat-type chickens. Rapid growth in a bird with insufficient pulmonary vascular capacity
Received for publication August 12, 1995. Accepted for publication December 22, 1997. 1To whom correspondence should [email protected]
be
addressed:
is the primary cause of PH, and when it is related to rapid growth it has been called pulmonary hypertension syndrome (PHS) (Huchzermeyer and de Ruyck, 1986; Julian, 1993). There are a variety of additional or secondary causes that can increase the incidence of PHS. Additive factors that increase the incidence of ascites may result from higher blood flow because of higher metabolic rate (cold, heat, certain nutrients or chemicals, etc.) or greater resistance to flow that is the result of hypoxemia increasing blood viscosity (high altitude, rickets, respiratory disease, reduced oxygen transfer), red blood cell rigidity, or reduced vascular capacity in the lung (Julian and Goryo, 1990; Julian and Squires, 1994; Mirsalimi et al., 1992, 1993). The anatomy and physiology of the avian respiratory system are important in the susceptibility of meat-type chickens to PHS. The small stature of the modern meattype chicken, the large, heavy breast mass, the pressure from abdominal contents on air sacs, and the small lung volume may all be involved in the increased incidence of PHS. The lungs of birds are smaller as a percentage of body weight than those of mammals, and the lungs of meat-type chickens are smaller than those of Leghorns
Abbreviation Key: PH = pulmonary hypertension; PHS = pulmonary hypertension syndrome; RVF = right ventricular failure; TD = tibial dyschondroplasia.
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ABSTRACT Over the last 40 yr, genetic selection for rapid growth and improved feed efficiency has been very effective in meat-type poultry. Combined with changes in the feed that have increased both the nutritional and physical density to encourage a high nutrient intake, growth rate has more than doubled. The effect of genetic selection for high muscle to bone ratio and high calorie intake of a ration that supplies all nutritional requirements causes significant mortality from cardiovascular disease. In the chicken, sudden death syndrome (flip-over) and pulmonary hypertension syndrome resulting in ascites are the most important. Ruptured aorta, spontaneous turkey cardiomyopathy (round heart), and cardiomyopathy causing sudden
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hypoxemia. This increased pressure would also decrease the size of the already small blood capillaries and could further increase the resistance to blood-flow. Severe pulmonary edema as the result of PH would result in hypoxic respiratory failure and death and would explain the increasing incidence of death without ascites in PHS. These broilers show marked right ventricular hypertrophy and lung edema and die from lung edema. The sudden increase in PHS in meat-type chickens in the 1980s was associated with a rapid increase in growth rate and feed conversion. These increases were a result of a combination of genetic selection for fast-growing, heavy broilers with low feed conversion and a more dense, high caloric, pelleted feed that supplied all the nutrients required for rapid growth and encouraged a high nutrient intake (Havenstein et al., 1994). In meattype chickens, PHS is usually primary pulmonary hypertension; there is no evidence of prior heart or lung disease that could account for the increase in blood flow or resistance to flow that results in the increased pressure in the pulmonary arteries. Ascites caused by PH is a production-related disease at low altitude. It can be prevented easily by restricting growth rate (Arce et al., 1992; Julian et al., 1995). It is possible that some meat-type chickens of the phenotype we have created have reached the limit of blood flow through their lungs, and future improvements in growth rate will only be possible if the lung and abdominal cavity capacities are enlarged. Ascites at moderate (above 800 m) and high altitude is a much more severe problem because of the polycythemia induced by hypoxia, but it can be reduced by restricting growth rate. Research on oxygen hemoglobin saturation in meattype chickens indicates that fast-growing broilers have a lower oxygen hemoglobin saturation than slow-growing broilers (Julian and Mirsalimi, 1992). These results suggest that some meat-type chickens are not fully oxygenating their hemoglobin even at low altitude.
SKELETAL DEFORMITIES Skeletal deformities can be caused in a variety of ways. Nutritional deficiencies can result in skeletal disease in all birds. Rapidly growing birds have a higher requirement for specific nutrients, and many skeletal defects in broiler and roaster chickens are rare or absent in slower growing strains (Havenstein et al., 1994). Mechanically induced or trauma-associated problems are also much more frequent in fast-growing broilers. These problems may have more to do with immaturity and weight than rapid growth because tissue becomes stronger and more resilient with age. This age-related effect is particularly true of bone, tendon, and ligament. Toxins in feed or water can cause skeletal deformities. Toxin effects are not usually associated with rapid growth, although rapidly growing birds would consume more of the offending product. Genetic faults may also
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(Julian, 1989). The lungs of birds are also firm and fixed in the thoracic cavity. They do not expand and contract with each breath as mammalian lungs do. The blood and air capillaries form a network that allows the small blood capillaries of the lung to dilate only very little to accommodate increased blood flow. Increased blood flow to supply the oxygen required for metabolism in fast-growing meat-type chickens causes an increase in the blood pressure required to push the blood through the blood capillaries in the lung (pulmonary hypertension). This increase in workload for the right side of the heart results in sporadic cases of RVF and ascites. Secondary factors that increase the oxygen requirement of the bird, reduce oxygen pick-up or transfer in the lung or release in the tissue, reduce oxygen carrying capacity of the blood, or increase blood volume or interfere with blood flow through the lung (polycythemia with increased blood viscosity, increased red blood cell rigidity, lung pathology narrowing or occluding capillaries) may result in flock outbreaks of ascites caused by PHS (Monge and Leo´n-Velarde, 1991; Julian, 1993; Diaz et al. 1994a). When PH occurs, the right ventricle responds very rapidly to the increased workload, as muscle does, by enlargement (hypertrophy). If PH continues, the right ventricle has to pump against that pressure, and the muscle wall continues to thicken and enlarge, increasing the pressure in the lung. The right atrioventricular valve is a muscle flap made up mainly of fibers from the right ventricle. As the ventricle thickens (hypertrophies) and dilates, the right atrioventricular valve also thickens and becomes stiff until it no longer covers the opening back to the body, at which time valvular insufficiency occurs. This results in a volume overload and causes dilation and right ventricular failure. The increased blood pressure in the veins, liver, and abdominal vessels forces plasma fluid (edema) out of the vessels, particularly the fenestrated sinusoids of the liver, into the peritoneal spaces, where it is called ascitic fluid. The condition is called ascites (waterbelly) (Wilson et al., 1988). There is normally a small quantity of fluid in the eight peritoneal spaces that drains back to the blood stream by the lymph channels. However, the increased pressure in the vena cava in broilers with valvular insufficiency interferes with lymph return, and the fluid accumulates in the peritoneal spaces (Julian, 1993). Most of the fluid is found in the ventral hepato-peritoneal spaces and in the pericardial space. There may be fluid in the very narrow pleural spaces and in the abdominal cavity. Fluid is not found in the air sacs. It is the pressure from this fluid on the air sacs that causes the respiratory signs and death. If the capillaries are the resistance vessels in PH in broiler chickens, right ventricular hypertrophy would result in increased pressure in the normally low pressure capillary bed of the lung and would cause interstitial and air capillary edema, which would increase the thickness of the respiratory membrane as described by Maxwell et al. (1986) and could result in
FIRST NORTH AMERICAN SYMPOSIUM ON POULTRY WELFARE
SPECIFIC DEFECTS
Chronic Painful Lameness in Older Broilers and Roasters The problem of lameness in broilers is not restricted to deformity, trauma, or infection. Many heavy, older
FIGURE 2. Proximal tibias from four broilers cut through the growth plate to show severe tibial dyschondroplasia. The proximal tibia has been pulled backward in the bone on the left. The debility or pain associated with this type of deformity has slowed growth and allowed some repair with reduction in the size of the dyschondroplastic mass. Enlargement of the proximal end of the tibia is obvious in the other three bones and there is some necrosis (the dark lines) in the bone on the right. Weight bearing would cause pain because of compression in this bird.
broilers that have no obvious disease, either on gross or histologic examination, walk as if they were in severe pain and prefer to sit. When forced to rise, they hobble a few steps and squat again. It is not clear whether the pain is associated with bones, tendons, ligaments, or muscles. This lameness is reduced by programs that slow growth by providing long daily dark periods in the first 2 wk, and accelerate sexual maturity and increase activity by lengthening light periods in the last 4 wk, which suggests that the pain is related to body weight and stress on immature bone and soft tissue. Severe tibial dyschondroplasia (TD) lesions can produce a similar lameness.
Angular Bone Deformity and Valgus-Varus Deformity
FIGURE 1. Broiler with angular bone deformity and disuse atrophy of muscle of left leg. This broiler was condemned for emaciation at processing.
Angular bone deformity is the most frequent skeletal defect in broilers on a nutritionally adequate ratio (Julian, 1984). It may be seen as early as 6 to 8 d, or not become prominent until 3 to 4 wk. It is usually progressive, and when young broilers are affected they usually become crippled and cannot get to the feed and water. If only one leg is affected, the bird may not go down. Pain associated with the deformity reduces activity and restricts feeding. These broilers may be condemned for emaciation at processing or there may be disuse atrophy of the muscle of the affected leg (Figure 1). Angular bone deformity appears to be specifically related to rapid growth with insufficient time for proper alignment and remodelling of the bones of the distal tibio-tarsus. It can be reduced by slowing growth in the first 10 to 21 d and by extended daily rest (long, dark) periods (Classen and Riddell, 1989; Fontana et al., 1992; Yu and Robinson, 1992; Gordon, 1994).
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result in skeletal defects, and are not usually growthrelated. If the hypothesis that rapid growth results in musculoskeletal deformity is valid, perhaps we should consider how specific defects could be associated with rapid growth. 1) The defect could be related to high body weight. 2) The defect could occur because tissues (bones, ligaments, tendons, and muscles) are immature. The production of strong tissue, remodelling, and alignment of bone requires more time than rapid growth allows. 3) The defect could be related to high specific nutrient, enzyme, hormone, or oxygen requirement by specialized cells (proliferating chondrocytes). 4) The defect could be related to metabolic by-products (lactic acid, carbon dioxide) that are increased by rapid growth. 5) Young rapidly multiplying cells could be more susceptible to toxic or metabolic injury.
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poultry and rare or absent in other birds. The proximal tibia is the fastest growing growth plate in broilers. Tibial dyschondroplasia is likely caused by lack of specific nutrients required by proliferating chondrocytes. It can be markedly reduced by 1,25-dihydroxycholecalciferol (RenFIGURE 3. Spontaneous fracture through the proximal tibias of a broiler with severe tibial dyschondroplasia. This bird was unable to walk and died from dehydration.
Vitamin B and trace mineral deficiency may produce similar deformity by causing growth plate damage.
Tibial Dyschondroplasia and Osteochondrosis Tibial dyschondroplasia occurs as a result of failure of proliferating chondrocytes in the growth plate to hypertrophy to allow vascular penetration and the production of bone (Thorp et al., 1991, 1993, 1995; Cook and Bai, 1994; Hester, 1994). Mild and moderate lesions may not cause lameness, although the proximal end of the tibia may be enlarged. Severe lesions cause weakening of the proximal tibia which is compressed by body weight as the bird walks, causing painful lameness. The weakened proximal tibia may be pulled backward by the strong gastrocnemius muscle (Riddell, 1992), causing deformity, or the large cartilage mass may develop avascular necrosis and there will be spontaneous fracture of the proximal tibia (Figures 2 and 3). In either case, the bird is a “creeper”, moving around on its hocks (Figure 4), and may be unable to reach feed and water. Tibial dyschondroplasia is most specifically related to rapid growth (likely because of a requirement for very rapid long bone growth) as it is common in meat-type
FIGURE 5. Radiograph of vertebrae of two broilers with spondylolisthesis (normal above).
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FIGURE 4. Crippled broilers classed as creepers. These broilers were unable to rise and could only move around on their hocks because of severe tibial dyschondroplasia causing deformity or fracture, spondylolisthesis, osteomyelitis of the vertebrae, impingement of the spinal cord by cartilage or because of ruptured tendons.
FIRST NORTH AMERICAN SYMPOSIUM ON POULTRY WELFARE
nie et al., 1993; Leach and Twal, 1994). Because availability of 1,25-dihydroxycholecalciferol is affected by the acid/ base balance in the growth plate, high dietary Cl– or P– may increase TD through this mechanism. Rapid growth causes metabolic acidosis, and panting in hot temperature causes respiratory acidosis, so rapid growth may have more than one effect. Dyschondroplasia is frequently present at other growth centers, particularly the proximal metatarsals and femur. It is not clear how toxins (cobalt, fusarium, etc.) cause dyschondroplasia (Haynes et al., 1985; Edwards, 1987; Diaz et al., 1994b) but they may interfere with 1,25-dihydroxycholecalciferol. There is a genetic susceptibility to TD that could be associated with growth rate, acid/base balance, or some other mechanism (Leach and Nesheim, 1965). Tibial dyschondroplasia can be reduced by replacing some NaCl in the diet with NaHCO3, and by avoiding a high P:Ca ratio.
FIGURE 7. Vertebrae cut in midline with spinal cord removed to show narrowing of the spinal canal and pinching of the cord (normal above).
on the spinal cord and causing leg weakness and ataxia (Figures 5, 6, 7, and 8). Affected birds sit on their tail with their legs extended or are “creepers” (Figure 4); they may be unable to reach feed and water. This deformity is the only rapid growth-associated skeletal deformity that is
Spondylolisthesis (Kinky Back) Spondylolisthesis occurs when the ligaments between the third and fourth thoracic vertebrae tear or avulse and allow the anterior end of the fourth vertebra to dislocate ventrally. The posterior end rotates upward, impinging
FIGURE 8. Vertebrae cut in midline to show pinching of the spinal cord by cartilage at the fourth thoracic vertebra in the two vertebrae in the center. Normal vertebrae are shown at the top and bottom. The broilers with the damaged vertebrae were unable to rise, and could only struggle around on their hocks.
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FIGURE 6. Vertebrae cut in the midline to show pinching of the spinal cord by the posterior lip of the fourth thoracic vertebra following ventral dislocation of the anterior end of that vertebra. This is the only nonfused vertebra in the back of chickens. These birds were unable to rise or walk.
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FIGURE 11. Broiler from processing line showing bilateral rupture of the gastrocnemius tendons. The tendons and sheaths are thickened above the point of rupture and there is blood in the tissue where the injury occurred.
more frequent in females. Osteochondrosis of the articular cartilage of the fourth thoracic vertebra may result in impingement on the spinal cord and cause similar signs, and is more frequent in males. Poor ligament strength or weak attachment to bone because of immaturity, and heavy breast muscle mass are the most likely cause of spondylolisthesis. There is a moderate genetic component (Julian, 1990). Osteochondrosis of the articular cartilage of the fourth thoracic vertebra and of articular cartilage in other joints is the result of avascular degeneration and is directly related to rapid growth of cartilage that becomes too thick because of insufficient time for remodelling and failure of chondrocyte differentiation (Thorp et al., 1993).
cartilage is frequently pulled off the femoral head and trochanter by the joint capsule, leaving the smooth shiny growth plate (Figure 9). Occasionally, part of the growth plate also pulls away, leaving rough, irregular, necroticlooking subchondral bone. This growth plate separation may occur spontaneously in live birds that have dyschondroplasia or osteomyelitis. When it occurs in live birds it is usually caused by injury, the most frequent being when a bird is caught and held by one leg (Figure 10). Rapid growth does not allow sufficient time for strong tissue formation.
Epiphyseal Separation When the legs of young rapidly growing broiler chickens are disarticulated at necropsy, the articular
Ruptured gastrocnemius tendons occur most frequent in older broilers, roasters, and broiler breeders. The gastrocnemius tendon separates by pulling apart just above the hocks (Figure 11). When the lesion is bilateral,
FIGURE 10. Blood in muscle and tissue of the hip in a broiler that was found dead in a crate at the processing plant (dead on arrival). This broiler bled to death through the end of the proximal femur following epiphyseal separation during catching and crating.
FIGURE 12. Proximal tibias in roasters lame from rickets. There is swelling of the epiphyses and backward bending of the proximal end of the bone on the left. This lesion could be confused with dyschondroplasia.
Ruptured Gastrocnemius Tendon
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FIGURE 9. Iatrogenic epiphyseal separation. This lesion is seen frequently in the legs of broiler chickens when the hip is disarticulated during the necropsy procedure. This is not associated with femoral head necrosis or fragile bones.
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Rickets Rickets can occur in either slow- or fast-growing birds, but is made worse by the higher nutrient requirements of growth. On marginally deficient diets, only the most rapidly growing broilers are affected. Rickets causes enlargement of the epiphyseal area and occasionally deformity of the soft, rubbery bone (Figure 12). Magnesium toxicity may cause similar bone deformity (Lee et al., 1980). The thickened growth plate in rickets may be similar to early TD, and mild rickets may be classed grossly as TD.
Other Deformities
the bird is down on its hocks (creeper). This condition is the result of heavy weight and poor tendon development (Riddell, 1991). Rapid growth may result in poor blood supply and avascular degeneration, or poor tendon strength. As the tendon separates prior to rupture, the tendon and tendon sheath are frequently thickened by fibroplasia and other repair process.
Other skeletal deformities that cause lameness, such as slipped tendon (Figure 13), rotated tibia (Figure 14), and straddled legs, are mechanical defects and do not appear to be growth related. High or low incubator temperature may also increase the incidence of these defects. Lateral curvature of the upper tibia in broilers that are straddled or have one leg out to the side (twisters), is also mechanical and occurs from pressure on the growing bone after the bird is down (Figure 15). Scoliosis and twisted necks are congenital defects, not associated with growth. Some nutritional deficiencies may increase the incidence of these.
WELFARE CONCERNS
Chronic Pain Chronic pain and the distress associated with it is a major concern in animal welfare and euthanasia should be considered in severely affected birds. Prevention of chronic pain in broilers should be the goal, and more effort should be made to find management and nutritional techniques to reduce chronic pain. Lighting programs
FIGURE 14. Rotated tibia (normal on right). The distal tibia rotates laterally through its length. The fibula is pulled around as the distal tibia rotates.
FIGURE 15. Lateral curvature of the upper tibia (affected bone on the top, normal on bottom) in a young broiler that has had one leg out to the side because of failure of the adductor muscle. This leg was out laterally for 12 to 14 d and the defect developed because of the position of the leg as the leg bone grew.
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FIGURE 13. Condyle asymmetry in a broiler, lame because of slipped gastrocnemius tendon. Most chickens with slipped tendons have normal condyles.
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appear to improve broiler mobility and reduce chronic pain that is not associated with deformity.
Acute Pain Acute pain often has to do with the trauma of catching and handling. Better methods of catching and moving broilers to processing must be devised to reduce traumatic injury to bones, joints, and muscles.
Cripples
REFERENCES Arce, J., M. Berger, and C. Lopez-Coello, 1992. Control of ascites syndrome by feed restriction techniques. J. Appl. Poult. Res. 1:1–5. Classen, H. L., and C. Riddell, 1989. Photoperiodic effects on performance and leg abnormalities in broiler chickens. Poultry Sci. 68:873–879. Cook, M. E., and Y. Bai, 1994. Factors influencing growth plate cartilage turnover. Poultry Sci. 73:889–896. Diaz, G. J., R. J. Julian, and E. J. Squires, 1994a. Cobalt-induced polycythaemia causing right ventricular hypertrophy and ascites in meat-type chickens. Avian Pathol. 23:91–104. Diaz, G. J., R. J. Julian, and E. J. Squires, 1994b. Lesions in broiler chickens following experimental intoxication with cobalt. Avian Dis. 38:308–316. Edwards, H. M., Jr., 1984. Studies on the etiology of tibial dyschondroplasia in chickens. J. Nutr. 114:1001–1013. Edwards, H. M., Jr., 1987. Effects of thiuram, disulfiram and a trace element mixture on the incidence of tibial dyschondroplasia in chickens. J. Nutr. 117:964–969. Fontana, E. A., W. D. Weaver, B. A. Watkins, and D. M. Denbow, 1992. Effect of early feed restriction on growth, feed conversion, and mortality in broiler chickens. Poultry Sci. 71:1296–1305. Gordon, S. H., 1994. Effects of day length and increasing day length programmes on broiler welfare and performance. World’s Poult. Sci. J. 50:269–282. Havenstein, G. B., P. R. Ferket, S. E. Scheideler, and B. T. Larson, 1994. Growth, livability, and feed conversion of 1957 vs 1991 broilers when fed “typical” 1957 and 1991 broiler diets. Poultry Sci. 73:1785–1794. Haynes, J. S., M. M. Walser, and E. M. Lawler, 1985. Morphogenesis of Fusarium sp.-induced tibial dyschondroplasia in chickens. Vet. Pathol. 22:629–636. Hester, P. Y., 1994. The role of environment and management on leg abnormalities in meat-type fowl. Poultry Sci. 73:904–915. Huchzermeyer, F. W., and A.M.C. De Ruyck, 1986. Pulmonary hypertension syndrome associated with ascites in broilers. Vet. Rec. 119:94. Julian, R. J., 1984. Valgus-varus deformity of the intertarsal joint in broiler chickens. Can. Vet. J. 25:254–258. Julian, R. J., 1989. Lung volume of meat-type chickens. Avian Dis. 33:174–176.
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Many of the skeletal deformities in broilers result in birds that are down and unable to walk. There may be chronic pain as well as anxiety associated with aggression from other birds and with the difficulty of getting to feed and water. Many of these broilers lie on the floor until they die of dehydration. Poultry workers should be instructed to remove and euthanatize crippled broilers daily.
Julian, R. J., 1990. Avian Skeletal Disease Symposium, Pages 1–11 in: Annual Meeting of the American Association of Avian Pathologists/AVMA, 1990, San Antonio, TX. Julian, R. J., 1993. Ascites in poultry. Avian Pathol. 22:419–454. Julian, R. J., and M. Goryo, 1990. Pulmonary aspergillosis causing right ventricular failure and ascites in meat-type chickens. Avian Pathol. 19:643–654. Julian R. J., and S. M. Mirsalimi, 1992. Blood oxygen concentration of fast-growing and slow-growing broiler chickens with ascites from right ventricular failure. Avian Dis. 36:730–732. Julian R. J., and E. J. Squires, 1994. Haematopoietic and right ventricular response to intermittent hypobaric hypoxia in meat-type chickens. Avian Pathol. 23:539–545. Julian, R. J., M. Boulianne, and J.-P. Vaillancourt, 1995. Pre´vention de la de´faillance ventriculaire droite secondaire a` l’hypertension pulmonaire et de l’ascite chez le poulet de chair. Med. Vet. Que´bec 25:73–76. Leach, R. M., and M. C. Nesheim, 1965. Nutritional, genetic and morphological studies of an abnormal cartilage formation in young chicks. J. Nutr. 86:236–244. Leach, R. M., and W. O. Twal, 1994. Autocrine, paracrine and hormonal signals involved in growth plate chondrocyte differentiation. Poultry Sci. 73:883–888. Lee, S. R., W. M. Britton and G. N. Rowland, 1980. Magnesium toxicity: bone lesions. Poultry Sci. 59:2403–2411. Lilburn, M. S., 1994. Skeletal growth of commercial poultry species. Poultry Sci. 73:897–903. Maxwell, M. H., G. W. Robertson, and S. Spence, 1986. Studies on an ascitic syndrome in young broilers. 2. Ultrastructure. Avian Pathol. 15:525–538. Mirsalimi, S. M., P. J. O’Brien, and R. J. Julian, 1992. Changes in erythrocyte deformability in NaCl-induced right-sided cardiac failure in broiler chickens. Am. J. Vet. Res. 53: 2359–2363. Mirsalimi, S. M., R. J. Julian, and E. J. Squires, 1993. Effect of hypobaric hypoxia on slow- and fast-growing chickens fed diets with high and low protein levels. Avian Dis. 37: 660–667. Monge, C. and F. Leo´n-Velarde, 1991. Physiological adaptation to high altitude: oxygen transport in mammals and birds. Physiol. Rev. 71:1136–1171. Rennie, J. S., C. C. Whitehead, and B. H. Thorp, 1993. The effect of dietary 1, 25-dehydroxycholecalciferal in preventing tibial dyschondroplasia in broilers fed on diets imbalanced in calcium and phosphorus. Br. J. Nutr. 69:809–816. Riddell, C., 1992. Non-infectious skeletal disorders of poultry: an overview, Pages 119–145 in: Bone Biology and Skeletal Disorders in Poultry. C. C. Whitehead, ed. Carfax Publishing Co., Abingdon, UK. Thorp, B. H., C. Farquharson, A.P.L. Kwan, and N. Loveridge, 1993. Osteochondrosis/dyschondroplasia: a failure of chondrocyte differentiation. Equine Vet. J. Suppl. 16:13–18. Thorp, B. H., S. B. Jakowlew, and C. Goddard, 1995. Avian dyschondroplasia: local deficiencies in growth factors are integral to the aetiopathogenesis. Avian Pathol. 24:135–148. Thorp, B. H., C. C. Whitehead, and J. S. Rennie, 1991. Avian tibial dyschondroplasia: a comparison of the incidence and severity as assessed by gross examination and histopathology. Res. Vet. Sci. 51:48–54. Wilson, J. B., R. J. Julian, and I. K. Barker, 1988. Lesions of right heart failure and ascites in broiler chickens. Avian Dis. 32: 246–261. Yu, M. W., and F. E. Robinson, 1992. The application of shortterm feed restriction to broiler chicken production: A review. J. Appl. Poult. Res. 1:147–153.
(Key words: ascites, broiler, metabolic disease, rapid growth, skeletal deformity) 1998 Poultry Science 77:1773–1780
INTRODUCTION Rapid growth and heavy body weight, particularly associated with a small skeletal frame, have been implicated in musculoskeletal and cardiovascular disease in meat-type poultry (Riddell, 1992; Julian, 1993; Lilburn, 1994). Research on these conditions has frequently produced contradictory results. Although many of the problems can be reduced or eliminated by slowing growth rate, rapid growth and weight do not necessarily result in disease. Perhaps we should consider whether some of these problems are the result of metabolic imbalances associated with rapid growth and should be more correctly called metabolic disease.
ASCITES Ascites caused by valvular insufficiency and right ventricular failure (RVF) following right ventricular dilation and hypertrophy from pulmonary hypertension (PH) has become a prominent cause of illness, death, and condemnation in meat-type chickens. Rapid growth in a bird with insufficient pulmonary vascular capacity
Received for publication August 12, 1995. Accepted for publication December 22, 1997. 1To whom correspondence should [email protected]
be
addressed:
is the primary cause of PH, and when it is related to rapid growth it has been called pulmonary hypertension syndrome (PHS) (Huchzermeyer and de Ruyck, 1986; Julian, 1993). There are a variety of additional or secondary causes that can increase the incidence of PHS. Additive factors that increase the incidence of ascites may result from higher blood flow because of higher metabolic rate (cold, heat, certain nutrients or chemicals, etc.) or greater resistance to flow that is the result of hypoxemia increasing blood viscosity (high altitude, rickets, respiratory disease, reduced oxygen transfer), red blood cell rigidity, or reduced vascular capacity in the lung (Julian and Goryo, 1990; Julian and Squires, 1994; Mirsalimi et al., 1992, 1993). The anatomy and physiology of the avian respiratory system are important in the susceptibility of meat-type chickens to PHS. The small stature of the modern meattype chicken, the large, heavy breast mass, the pressure from abdominal contents on air sacs, and the small lung volume may all be involved in the increased incidence of PHS. The lungs of birds are smaller as a percentage of body weight than those of mammals, and the lungs of meat-type chickens are smaller than those of Leghorns
Abbreviation Key: PH = pulmonary hypertension; PHS = pulmonary hypertension syndrome; RVF = right ventricular failure; TD = tibial dyschondroplasia.
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ABSTRACT Over the last 40 yr, genetic selection for rapid growth and improved feed efficiency has been very effective in meat-type poultry. Combined with changes in the feed that have increased both the nutritional and physical density to encourage a high nutrient intake, growth rate has more than doubled. The effect of genetic selection for high muscle to bone ratio and high calorie intake of a ration that supplies all nutritional requirements causes significant mortality from cardiovascular disease. In the chicken, sudden death syndrome (flip-over) and pulmonary hypertension syndrome resulting in ascites are the most important. Ruptured aorta, spontaneous turkey cardiomyopathy (round heart), and cardiomyopathy causing sudden
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hypoxemia. This increased pressure would also decrease the size of the already small blood capillaries and could further increase the resistance to blood-flow. Severe pulmonary edema as the result of PH would result in hypoxic respiratory failure and death and would explain the increasing incidence of death without ascites in PHS. These broilers show marked right ventricular hypertrophy and lung edema and die from lung edema. The sudden increase in PHS in meat-type chickens in the 1980s was associated with a rapid increase in growth rate and feed conversion. These increases were a result of a combination of genetic selection for fast-growing, heavy broilers with low feed conversion and a more dense, high caloric, pelleted feed that supplied all the nutrients required for rapid growth and encouraged a high nutrient intake (Havenstein et al., 1994). In meattype chickens, PHS is usually primary pulmonary hypertension; there is no evidence of prior heart or lung disease that could account for the increase in blood flow or resistance to flow that results in the increased pressure in the pulmonary arteries. Ascites caused by PH is a production-related disease at low altitude. It can be prevented easily by restricting growth rate (Arce et al., 1992; Julian et al., 1995). It is possible that some meat-type chickens of the phenotype we have created have reached the limit of blood flow through their lungs, and future improvements in growth rate will only be possible if the lung and abdominal cavity capacities are enlarged. Ascites at moderate (above 800 m) and high altitude is a much more severe problem because of the polycythemia induced by hypoxia, but it can be reduced by restricting growth rate. Research on oxygen hemoglobin saturation in meattype chickens indicates that fast-growing broilers have a lower oxygen hemoglobin saturation than slow-growing broilers (Julian and Mirsalimi, 1992). These results suggest that some meat-type chickens are not fully oxygenating their hemoglobin even at low altitude.
SKELETAL DEFORMITIES Skeletal deformities can be caused in a variety of ways. Nutritional deficiencies can result in skeletal disease in all birds. Rapidly growing birds have a higher requirement for specific nutrients, and many skeletal defects in broiler and roaster chickens are rare or absent in slower growing strains (Havenstein et al., 1994). Mechanically induced or trauma-associated problems are also much more frequent in fast-growing broilers. These problems may have more to do with immaturity and weight than rapid growth because tissue becomes stronger and more resilient with age. This age-related effect is particularly true of bone, tendon, and ligament. Toxins in feed or water can cause skeletal deformities. Toxin effects are not usually associated with rapid growth, although rapidly growing birds would consume more of the offending product. Genetic faults may also
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(Julian, 1989). The lungs of birds are also firm and fixed in the thoracic cavity. They do not expand and contract with each breath as mammalian lungs do. The blood and air capillaries form a network that allows the small blood capillaries of the lung to dilate only very little to accommodate increased blood flow. Increased blood flow to supply the oxygen required for metabolism in fast-growing meat-type chickens causes an increase in the blood pressure required to push the blood through the blood capillaries in the lung (pulmonary hypertension). This increase in workload for the right side of the heart results in sporadic cases of RVF and ascites. Secondary factors that increase the oxygen requirement of the bird, reduce oxygen pick-up or transfer in the lung or release in the tissue, reduce oxygen carrying capacity of the blood, or increase blood volume or interfere with blood flow through the lung (polycythemia with increased blood viscosity, increased red blood cell rigidity, lung pathology narrowing or occluding capillaries) may result in flock outbreaks of ascites caused by PHS (Monge and Leo´n-Velarde, 1991; Julian, 1993; Diaz et al. 1994a). When PH occurs, the right ventricle responds very rapidly to the increased workload, as muscle does, by enlargement (hypertrophy). If PH continues, the right ventricle has to pump against that pressure, and the muscle wall continues to thicken and enlarge, increasing the pressure in the lung. The right atrioventricular valve is a muscle flap made up mainly of fibers from the right ventricle. As the ventricle thickens (hypertrophies) and dilates, the right atrioventricular valve also thickens and becomes stiff until it no longer covers the opening back to the body, at which time valvular insufficiency occurs. This results in a volume overload and causes dilation and right ventricular failure. The increased blood pressure in the veins, liver, and abdominal vessels forces plasma fluid (edema) out of the vessels, particularly the fenestrated sinusoids of the liver, into the peritoneal spaces, where it is called ascitic fluid. The condition is called ascites (waterbelly) (Wilson et al., 1988). There is normally a small quantity of fluid in the eight peritoneal spaces that drains back to the blood stream by the lymph channels. However, the increased pressure in the vena cava in broilers with valvular insufficiency interferes with lymph return, and the fluid accumulates in the peritoneal spaces (Julian, 1993). Most of the fluid is found in the ventral hepato-peritoneal spaces and in the pericardial space. There may be fluid in the very narrow pleural spaces and in the abdominal cavity. Fluid is not found in the air sacs. It is the pressure from this fluid on the air sacs that causes the respiratory signs and death. If the capillaries are the resistance vessels in PH in broiler chickens, right ventricular hypertrophy would result in increased pressure in the normally low pressure capillary bed of the lung and would cause interstitial and air capillary edema, which would increase the thickness of the respiratory membrane as described by Maxwell et al. (1986) and could result in
FIRST NORTH AMERICAN SYMPOSIUM ON POULTRY WELFARE
SPECIFIC DEFECTS
Chronic Painful Lameness in Older Broilers and Roasters The problem of lameness in broilers is not restricted to deformity, trauma, or infection. Many heavy, older
FIGURE 2. Proximal tibias from four broilers cut through the growth plate to show severe tibial dyschondroplasia. The proximal tibia has been pulled backward in the bone on the left. The debility or pain associated with this type of deformity has slowed growth and allowed some repair with reduction in the size of the dyschondroplastic mass. Enlargement of the proximal end of the tibia is obvious in the other three bones and there is some necrosis (the dark lines) in the bone on the right. Weight bearing would cause pain because of compression in this bird.
broilers that have no obvious disease, either on gross or histologic examination, walk as if they were in severe pain and prefer to sit. When forced to rise, they hobble a few steps and squat again. It is not clear whether the pain is associated with bones, tendons, ligaments, or muscles. This lameness is reduced by programs that slow growth by providing long daily dark periods in the first 2 wk, and accelerate sexual maturity and increase activity by lengthening light periods in the last 4 wk, which suggests that the pain is related to body weight and stress on immature bone and soft tissue. Severe tibial dyschondroplasia (TD) lesions can produce a similar lameness.
Angular Bone Deformity and Valgus-Varus Deformity
FIGURE 1. Broiler with angular bone deformity and disuse atrophy of muscle of left leg. This broiler was condemned for emaciation at processing.
Angular bone deformity is the most frequent skeletal defect in broilers on a nutritionally adequate ratio (Julian, 1984). It may be seen as early as 6 to 8 d, or not become prominent until 3 to 4 wk. It is usually progressive, and when young broilers are affected they usually become crippled and cannot get to the feed and water. If only one leg is affected, the bird may not go down. Pain associated with the deformity reduces activity and restricts feeding. These broilers may be condemned for emaciation at processing or there may be disuse atrophy of the muscle of the affected leg (Figure 1). Angular bone deformity appears to be specifically related to rapid growth with insufficient time for proper alignment and remodelling of the bones of the distal tibio-tarsus. It can be reduced by slowing growth in the first 10 to 21 d and by extended daily rest (long, dark) periods (Classen and Riddell, 1989; Fontana et al., 1992; Yu and Robinson, 1992; Gordon, 1994).
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result in skeletal defects, and are not usually growthrelated. If the hypothesis that rapid growth results in musculoskeletal deformity is valid, perhaps we should consider how specific defects could be associated with rapid growth. 1) The defect could be related to high body weight. 2) The defect could occur because tissues (bones, ligaments, tendons, and muscles) are immature. The production of strong tissue, remodelling, and alignment of bone requires more time than rapid growth allows. 3) The defect could be related to high specific nutrient, enzyme, hormone, or oxygen requirement by specialized cells (proliferating chondrocytes). 4) The defect could be related to metabolic by-products (lactic acid, carbon dioxide) that are increased by rapid growth. 5) Young rapidly multiplying cells could be more susceptible to toxic or metabolic injury.
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poultry and rare or absent in other birds. The proximal tibia is the fastest growing growth plate in broilers. Tibial dyschondroplasia is likely caused by lack of specific nutrients required by proliferating chondrocytes. It can be markedly reduced by 1,25-dihydroxycholecalciferol (RenFIGURE 3. Spontaneous fracture through the proximal tibias of a broiler with severe tibial dyschondroplasia. This bird was unable to walk and died from dehydration.
Vitamin B and trace mineral deficiency may produce similar deformity by causing growth plate damage.
Tibial Dyschondroplasia and Osteochondrosis Tibial dyschondroplasia occurs as a result of failure of proliferating chondrocytes in the growth plate to hypertrophy to allow vascular penetration and the production of bone (Thorp et al., 1991, 1993, 1995; Cook and Bai, 1994; Hester, 1994). Mild and moderate lesions may not cause lameness, although the proximal end of the tibia may be enlarged. Severe lesions cause weakening of the proximal tibia which is compressed by body weight as the bird walks, causing painful lameness. The weakened proximal tibia may be pulled backward by the strong gastrocnemius muscle (Riddell, 1992), causing deformity, or the large cartilage mass may develop avascular necrosis and there will be spontaneous fracture of the proximal tibia (Figures 2 and 3). In either case, the bird is a “creeper”, moving around on its hocks (Figure 4), and may be unable to reach feed and water. Tibial dyschondroplasia is most specifically related to rapid growth (likely because of a requirement for very rapid long bone growth) as it is common in meat-type
FIGURE 5. Radiograph of vertebrae of two broilers with spondylolisthesis (normal above).
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FIGURE 4. Crippled broilers classed as creepers. These broilers were unable to rise and could only move around on their hocks because of severe tibial dyschondroplasia causing deformity or fracture, spondylolisthesis, osteomyelitis of the vertebrae, impingement of the spinal cord by cartilage or because of ruptured tendons.
FIRST NORTH AMERICAN SYMPOSIUM ON POULTRY WELFARE
nie et al., 1993; Leach and Twal, 1994). Because availability of 1,25-dihydroxycholecalciferol is affected by the acid/ base balance in the growth plate, high dietary Cl– or P– may increase TD through this mechanism. Rapid growth causes metabolic acidosis, and panting in hot temperature causes respiratory acidosis, so rapid growth may have more than one effect. Dyschondroplasia is frequently present at other growth centers, particularly the proximal metatarsals and femur. It is not clear how toxins (cobalt, fusarium, etc.) cause dyschondroplasia (Haynes et al., 1985; Edwards, 1987; Diaz et al., 1994b) but they may interfere with 1,25-dihydroxycholecalciferol. There is a genetic susceptibility to TD that could be associated with growth rate, acid/base balance, or some other mechanism (Leach and Nesheim, 1965). Tibial dyschondroplasia can be reduced by replacing some NaCl in the diet with NaHCO3, and by avoiding a high P:Ca ratio.
FIGURE 7. Vertebrae cut in midline with spinal cord removed to show narrowing of the spinal canal and pinching of the cord (normal above).
on the spinal cord and causing leg weakness and ataxia (Figures 5, 6, 7, and 8). Affected birds sit on their tail with their legs extended or are “creepers” (Figure 4); they may be unable to reach feed and water. This deformity is the only rapid growth-associated skeletal deformity that is
Spondylolisthesis (Kinky Back) Spondylolisthesis occurs when the ligaments between the third and fourth thoracic vertebrae tear or avulse and allow the anterior end of the fourth vertebra to dislocate ventrally. The posterior end rotates upward, impinging
FIGURE 8. Vertebrae cut in midline to show pinching of the spinal cord by cartilage at the fourth thoracic vertebra in the two vertebrae in the center. Normal vertebrae are shown at the top and bottom. The broilers with the damaged vertebrae were unable to rise, and could only struggle around on their hocks.
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FIGURE 6. Vertebrae cut in the midline to show pinching of the spinal cord by the posterior lip of the fourth thoracic vertebra following ventral dislocation of the anterior end of that vertebra. This is the only nonfused vertebra in the back of chickens. These birds were unable to rise or walk.
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FIGURE 11. Broiler from processing line showing bilateral rupture of the gastrocnemius tendons. The tendons and sheaths are thickened above the point of rupture and there is blood in the tissue where the injury occurred.
more frequent in females. Osteochondrosis of the articular cartilage of the fourth thoracic vertebra may result in impingement on the spinal cord and cause similar signs, and is more frequent in males. Poor ligament strength or weak attachment to bone because of immaturity, and heavy breast muscle mass are the most likely cause of spondylolisthesis. There is a moderate genetic component (Julian, 1990). Osteochondrosis of the articular cartilage of the fourth thoracic vertebra and of articular cartilage in other joints is the result of avascular degeneration and is directly related to rapid growth of cartilage that becomes too thick because of insufficient time for remodelling and failure of chondrocyte differentiation (Thorp et al., 1993).
cartilage is frequently pulled off the femoral head and trochanter by the joint capsule, leaving the smooth shiny growth plate (Figure 9). Occasionally, part of the growth plate also pulls away, leaving rough, irregular, necroticlooking subchondral bone. This growth plate separation may occur spontaneously in live birds that have dyschondroplasia or osteomyelitis. When it occurs in live birds it is usually caused by injury, the most frequent being when a bird is caught and held by one leg (Figure 10). Rapid growth does not allow sufficient time for strong tissue formation.
Epiphyseal Separation When the legs of young rapidly growing broiler chickens are disarticulated at necropsy, the articular
Ruptured gastrocnemius tendons occur most frequent in older broilers, roasters, and broiler breeders. The gastrocnemius tendon separates by pulling apart just above the hocks (Figure 11). When the lesion is bilateral,
FIGURE 10. Blood in muscle and tissue of the hip in a broiler that was found dead in a crate at the processing plant (dead on arrival). This broiler bled to death through the end of the proximal femur following epiphyseal separation during catching and crating.
FIGURE 12. Proximal tibias in roasters lame from rickets. There is swelling of the epiphyses and backward bending of the proximal end of the bone on the left. This lesion could be confused with dyschondroplasia.
Ruptured Gastrocnemius Tendon
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FIGURE 9. Iatrogenic epiphyseal separation. This lesion is seen frequently in the legs of broiler chickens when the hip is disarticulated during the necropsy procedure. This is not associated with femoral head necrosis or fragile bones.
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Rickets Rickets can occur in either slow- or fast-growing birds, but is made worse by the higher nutrient requirements of growth. On marginally deficient diets, only the most rapidly growing broilers are affected. Rickets causes enlargement of the epiphyseal area and occasionally deformity of the soft, rubbery bone (Figure 12). Magnesium toxicity may cause similar bone deformity (Lee et al., 1980). The thickened growth plate in rickets may be similar to early TD, and mild rickets may be classed grossly as TD.
Other Deformities
the bird is down on its hocks (creeper). This condition is the result of heavy weight and poor tendon development (Riddell, 1991). Rapid growth may result in poor blood supply and avascular degeneration, or poor tendon strength. As the tendon separates prior to rupture, the tendon and tendon sheath are frequently thickened by fibroplasia and other repair process.
Other skeletal deformities that cause lameness, such as slipped tendon (Figure 13), rotated tibia (Figure 14), and straddled legs, are mechanical defects and do not appear to be growth related. High or low incubator temperature may also increase the incidence of these defects. Lateral curvature of the upper tibia in broilers that are straddled or have one leg out to the side (twisters), is also mechanical and occurs from pressure on the growing bone after the bird is down (Figure 15). Scoliosis and twisted necks are congenital defects, not associated with growth. Some nutritional deficiencies may increase the incidence of these.
WELFARE CONCERNS
Chronic Pain Chronic pain and the distress associated with it is a major concern in animal welfare and euthanasia should be considered in severely affected birds. Prevention of chronic pain in broilers should be the goal, and more effort should be made to find management and nutritional techniques to reduce chronic pain. Lighting programs
FIGURE 14. Rotated tibia (normal on right). The distal tibia rotates laterally through its length. The fibula is pulled around as the distal tibia rotates.
FIGURE 15. Lateral curvature of the upper tibia (affected bone on the top, normal on bottom) in a young broiler that has had one leg out to the side because of failure of the adductor muscle. This leg was out laterally for 12 to 14 d and the defect developed because of the position of the leg as the leg bone grew.
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FIGURE 13. Condyle asymmetry in a broiler, lame because of slipped gastrocnemius tendon. Most chickens with slipped tendons have normal condyles.
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appear to improve broiler mobility and reduce chronic pain that is not associated with deformity.
Acute Pain Acute pain often has to do with the trauma of catching and handling. Better methods of catching and moving broilers to processing must be devised to reduce traumatic injury to bones, joints, and muscles.
Cripples
REFERENCES Arce, J., M. Berger, and C. Lopez-Coello, 1992. Control of ascites syndrome by feed restriction techniques. J. Appl. Poult. Res. 1:1–5. Classen, H. L., and C. Riddell, 1989. Photoperiodic effects on performance and leg abnormalities in broiler chickens. Poultry Sci. 68:873–879. Cook, M. E., and Y. Bai, 1994. Factors influencing growth plate cartilage turnover. Poultry Sci. 73:889–896. Diaz, G. J., R. J. Julian, and E. J. Squires, 1994a. Cobalt-induced polycythaemia causing right ventricular hypertrophy and ascites in meat-type chickens. Avian Pathol. 23:91–104. Diaz, G. J., R. J. Julian, and E. J. Squires, 1994b. Lesions in broiler chickens following experimental intoxication with cobalt. Avian Dis. 38:308–316. Edwards, H. M., Jr., 1984. Studies on the etiology of tibial dyschondroplasia in chickens. J. Nutr. 114:1001–1013. Edwards, H. M., Jr., 1987. Effects of thiuram, disulfiram and a trace element mixture on the incidence of tibial dyschondroplasia in chickens. J. Nutr. 117:964–969. Fontana, E. A., W. D. Weaver, B. A. Watkins, and D. M. Denbow, 1992. Effect of early feed restriction on growth, feed conversion, and mortality in broiler chickens. Poultry Sci. 71:1296–1305. Gordon, S. H., 1994. Effects of day length and increasing day length programmes on broiler welfare and performance. World’s Poult. Sci. J. 50:269–282. Havenstein, G. B., P. R. Ferket, S. E. Scheideler, and B. T. Larson, 1994. Growth, livability, and feed conversion of 1957 vs 1991 broilers when fed “typical” 1957 and 1991 broiler diets. Poultry Sci. 73:1785–1794. Haynes, J. S., M. M. Walser, and E. M. Lawler, 1985. Morphogenesis of Fusarium sp.-induced tibial dyschondroplasia in chickens. Vet. Pathol. 22:629–636. Hester, P. Y., 1994. The role of environment and management on leg abnormalities in meat-type fowl. Poultry Sci. 73:904–915. Huchzermeyer, F. W., and A.M.C. De Ruyck, 1986. Pulmonary hypertension syndrome associated with ascites in broilers. Vet. Rec. 119:94. Julian, R. J., 1984. Valgus-varus deformity of the intertarsal joint in broiler chickens. Can. Vet. J. 25:254–258. Julian, R. J., 1989. Lung volume of meat-type chickens. Avian Dis. 33:174–176.
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Many of the skeletal deformities in broilers result in birds that are down and unable to walk. There may be chronic pain as well as anxiety associated with aggression from other birds and with the difficulty of getting to feed and water. Many of these broilers lie on the floor until they die of dehydration. Poultry workers should be instructed to remove and euthanatize crippled broilers daily.
Julian, R. J., 1990. Avian Skeletal Disease Symposium, Pages 1–11 in: Annual Meeting of the American Association of Avian Pathologists/AVMA, 1990, San Antonio, TX. Julian, R. J., 1993. Ascites in poultry. Avian Pathol. 22:419–454. Julian, R. J., and M. Goryo, 1990. Pulmonary aspergillosis causing right ventricular failure and ascites in meat-type chickens. Avian Pathol. 19:643–654. Julian R. J., and S. M. Mirsalimi, 1992. Blood oxygen concentration of fast-growing and slow-growing broiler chickens with ascites from right ventricular failure. Avian Dis. 36:730–732. Julian R. J., and E. J. Squires, 1994. Haematopoietic and right ventricular response to intermittent hypobaric hypoxia in meat-type chickens. Avian Pathol. 23:539–545. Julian, R. J., M. Boulianne, and J.-P. Vaillancourt, 1995. Pre´vention de la de´faillance ventriculaire droite secondaire a` l’hypertension pulmonaire et de l’ascite chez le poulet de chair. Med. Vet. Que´bec 25:73–76. Leach, R. M., and M. C. Nesheim, 1965. Nutritional, genetic and morphological studies of an abnormal cartilage formation in young chicks. J. Nutr. 86:236–244. Leach, R. M., and W. O. Twal, 1994. Autocrine, paracrine and hormonal signals involved in growth plate chondrocyte differentiation. Poultry Sci. 73:883–888. Lee, S. R., W. M. Britton and G. N. Rowland, 1980. Magnesium toxicity: bone lesions. Poultry Sci. 59:2403–2411. Lilburn, M. S., 1994. Skeletal growth of commercial poultry species. Poultry Sci. 73:897–903. Maxwell, M. H., G. W. Robertson, and S. Spence, 1986. Studies on an ascitic syndrome in young broilers. 2. Ultrastructure. Avian Pathol. 15:525–538. Mirsalimi, S. M., P. J. O’Brien, and R. J. Julian, 1992. Changes in erythrocyte deformability in NaCl-induced right-sided cardiac failure in broiler chickens. Am. J. Vet. Res. 53: 2359–2363. Mirsalimi, S. M., R. J. Julian, and E. J. Squires, 1993. Effect of hypobaric hypoxia on slow- and fast-growing chickens fed diets with high and low protein levels. Avian Dis. 37: 660–667. Monge, C. and F. Leo´n-Velarde, 1991. Physiological adaptation to high altitude: oxygen transport in mammals and birds. Physiol. Rev. 71:1136–1171. Rennie, J. S., C. C. Whitehead, and B. H. Thorp, 1993. The effect of dietary 1, 25-dehydroxycholecalciferal in preventing tibial dyschondroplasia in broilers fed on diets imbalanced in calcium and phosphorus. Br. J. Nutr. 69:809–816. Riddell, C., 1992. Non-infectious skeletal disorders of poultry: an overview, Pages 119–145 in: Bone Biology and Skeletal Disorders in Poultry. C. C. Whitehead, ed. Carfax Publishing Co., Abingdon, UK. Thorp, B. H., C. Farquharson, A.P.L. Kwan, and N. Loveridge, 1993. Osteochondrosis/dyschondroplasia: a failure of chondrocyte differentiation. Equine Vet. J. Suppl. 16:13–18. Thorp, B. H., S. B. Jakowlew, and C. Goddard, 1995. Avian dyschondroplasia: local deficiencies in growth factors are integral to the aetiopathogenesis. Avian Pathol. 24:135–148. Thorp, B. H., C. C. Whitehead, and J. S. Rennie, 1991. Avian tibial dyschondroplasia: a comparison of the incidence and severity as assessed by gross examination and histopathology. Res. Vet. Sci. 51:48–54. Wilson, J. B., R. J. Julian, and I. K. Barker, 1988. Lesions of right heart failure and ascites in broiler chickens. Avian Dis. 32: 246–261. Yu, M. W., and F. E. Robinson, 1992. The application of shortterm feed restriction to broiler chicken production: A review. J. Appl. Poult. Res. 1:147–153.