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Received for publication August 12, 1995.Accepted for publication December 22, 1997.1 T o w h om c o rr e sp on d en c e s h ou l d b e a dd r es s ed :

rjulian@ovcnet.uoguelph.ca

Abbreviation Key: PH = pulmonary hypertension; PHS= pulmonaryhypertension syndrome; RVF = right ventricular failure; TD = tibialdyschondroplasia.

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

ABSTRACT Over the last 40 yr, genetic selection forrapid growth and improved feed efficiency has beenvery effective in meat-type poultry. Combined withchanges in the feed that have increased both thenutritional and physical density to encourage a highnutrient intake, growth rate has more than doubled. Theeffect of genetic selection for high muscle to bone ratioand high calorie intake of a ration that supplies allnutritional requirements causes significant mortalityfrom cardiovascular disease. In the chicken, suddendeath syndrome (flip-over) and pulmonary hypertensionsyndrome resulting in ascites are the most important.Ruptured aorta, spontaneous turkey cardiomyopathy(round heart), and cardiomyopathy causing sudden

death produce high mortality in turkeys. Rapid growthinduced by high nutrient intake alone can cause severelameness, bone defects, and deformity, as theseproblems are seen in animals that have not been selectedfor 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 withoutaffecting final body weight. Rapid growth alone may not

be the pathogenic mechanism that results in cardiovas-cular or musculoskeletal defects. Metabolic imbalanceinduced by high nutrient intake may cause some of theconditions. These metabolic problems might be cor-rected without reducing growth rate.

(Key words: ascites, broiler, metabolic disease, rapid growth, skeletal deformity)

1998 Poultry Science 77:17731780

INTRODUCTION

Rapid growth and heavy body weight, particularlyassociated with a small skeletal frame, have beenimplicated in musculoskeletal and cardiovascular dis-ease in meat-type poultry (Riddell, 1992; Julian, 1993;

Lilburn, 1994). Research on these conditions has fre-quently produced contradictory results. Although manyof the problems can be reduced or eliminated byslowing growth rate, rapid growth and weight do notnecessarily result in disease. Perhaps we should considerwhether some of these problems are the result ofmetabolic imbalances associated with rapid growth andshould be more correctly called metabolic disease.

ASCITES

Ascites caused by valvular insufficiency and rightventricular 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 growthin a bird with insufficient pulmonary vascular capacity

is the primary cause of PH, and when it is related torapid growth it has been called pulmonary hypertensionsyndrome (PHS) (Huchzermeyer and de Ruyck, 1986;

Julian, 1993). There are a variety of additional orsecondary causes that can increase the incidence of PHS.Additive factors that increase the incidence of ascites

may result from higher blood flow because of highermetabolic rate (cold, heat, certain nutrients or chemicals,etc.) or greater resistance to flow that is the result ofhypoxemia increasing blood viscosity (high altitude,rickets, respiratory disease, reduced oxygen transfer),red blood cell rigidity, or reduced vascular capacity inthe lung (Julian and Goryo, 1990; Julian and Squires,1994; Mirsalimi et al., 1992, 1993).

The anatomy and physiology of the avian respiratorysystem are important in the susceptibility of meat-typechickens to PHS. The small stature of the modern meat-type chicken, the large, heavy breast mass, the pressure

from abdominal contents on air sacs, and the small lungvolume may all be involved in the increased incidenceof PHS. The lungs of birds are smaller as a percentage of

body weight than those of mammals, and the lungs ofmeat-type chickens are smaller than those of Leghorns

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(Julian, 1989). The lungs of birds are also firm and fixedin the thoracic cavity. They do not expand and contractwith each breath as mammalian lungs do. The blood andair capillaries form a network that allows the small

blood capillaries of the lung to dilate only very little toaccommodate increased blood flow. Increased bloodflow to supply the oxygen required for metabolism infast-growing meat-type chickens causes an increase in

the blood pressure required to push the blood throughthe blood capillaries in the lung (pulmonary hyperten-sion). This increase in workload for the right side of theheart results in sporadic cases of RVF and ascites.Secondary factors that increase the oxygen requirementof the bird, reduce oxygen pick-up or transfer in thelung or release in the tissue, reduce oxygen carryingcapacity of the blood, or increase blood volume orinterfere with blood flow through the lung (polycythe-mia with increased blood viscosity, increased red bloodcell rigidity, lung pathology narrowing or occludingcapillaries) may result in flock outbreaks of ascites

caused by PHS (Monge and Leon-Velarde, 1991; Julian,1993; Diaz et al. 1994a).When PH occurs, the right ventricle responds very

rapidly to the increased workload, as muscle does, byenlargement (hypertrophy). If PH continues, the rightventricle has to pump against that pressure, and themuscle wall continues to thicken and enlarge, increasingthe pressure in the lung. The right atrioventricular valveis a muscle flap made up mainly of fibers from the rightventricle. As the ventricle thickens (hypertrophies) anddilates, the right atrioventricular valve also thickens and

becomes stiff until it no longer covers the opening backto the body, at which time valvular insufficiency occurs.

This results in a volume overload and causes dilationand right ventricular failure. The increased bloodpressure in the veins, liver, and abdominal vessels forcesplasma fluid (edema) out of the vessels, particularly thefenestrated sinusoids of the liver, into the peritonealspaces, where it is called ascitic fluid. The condition iscalled ascites (waterbelly) (Wilson et al., 1988). There isnormally a small quantity of fluid in the eight peritonealspaces that drains back to the blood stream by thelymph channels. However, the increased pressure in thevena cava in broilers with valvular insufficiency inter-feres with lymph return, and the fluid accumulates inthe peritoneal spaces (Julian, 1993). Most of the fluid isfound in the ventral hepato-peritoneal spaces and in thepericardial space. There may be fluid in the very narrowpleural spaces and in the abdominal cavity. Fluid is notfound in the air sacs. It is the pressure from this fluid onthe air sacs that causes the respiratory signs and death.

If the capillaries are the resistance vessels in PH inbroiler chickens, right ventricular hypertrophy wouldresult in increased pressure in the normally lowpressure capillary bed of the lung and would causeinterstitial and air capillary edema, which wouldincrease the thickness of the respiratory membrane asdescribed by Maxwell et al. (1986) and could result in

hypoxemia. This increased pressure would also decreasethe size of the already small blood capillaries and couldfurther increase the resistance to blood-flow. Severepulmonary edema as the result of PH would result inhypoxic respiratory failure and death and would explainthe increasing incidence of death without ascites in PHS.These broilers show marked right ventricular hyper-trophy and lung edema and die from lung edema.

The sudden increase in PHS in meat-type chickens inthe 1980s was associated with a rapid increase in growthrate and feed conversion. These increases were a resultof a combination of genetic selection for fast-growing,heavy broilers with low feed conversion and a moredense, high caloric, pelleted feed that supplied all thenutrients required for rapid growth and encouraged ahigh nutrient intake (Havenstein et al., 1994). In meat-type chickens, PHS is usually primary pulmonaryhypertension; there is no evidence of prior heart or lungdisease that could account for the increase in blood flowor resistance to flow that results in the increased

pressure in the pulmonary arteries.Ascites caused by PH is a production-related diseaseat low altitude. It can be prevented easily by restrictinggrowth rate (Arce et al., 1992; Julian et al., 1995). It ispossible that some meat-type chickens of the phenotypewe have created have reached the limit of blood flowthrough their lungs, and future improvements in growthrate will only be possible if the lung and abdominalcavity capacities are enlarged. Ascites at moderate(above 800 m) and high altitude is a much more severeproblem because of the polycythemia induced byhypoxia, but it can be reduced by restricting growthrate.

Research on oxygen hemoglobin saturation in meat-type chickens indicates that fast-growing broilers have alower oxygen hemoglobin saturation than slow-growing

broilers (Julian and Mirsalimi, 1992). These resultssuggest that some meat-type chickens are not fullyoxygenating their hemoglobin even at low altitude.

SKELETAL DEFORMITIES

Skeletal deformities can be caused in a variety ofways. Nutritional deficiencies can result in skeletaldisease in all birds. Rapidly growing birds have a higherrequirement for specific nutrients, and many skeletaldefects in broiler and roaster chickens are rare or absentin slower growing strains (Havenstein et al., 1994).Mechanically induced or trauma-associated problemsare also much more frequent in fast-growing broilers.These problems may have more to do with immaturityand weight than rapid growth because tissue becomesstronger and more resilient with age. This age-relatedeffect is particularly true of bone, tendon, and ligament.Toxins in feed or water can cause skeletal deformities.Toxin effects are not usually associated with rapidgrowth, although rapidly growing birds would consumemore of the offending product. Genetic faults may also

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FIGURE 1. Broiler with angular bone deformity and disuse atrophyof muscle of left leg. This broiler was condemned for emaciation atprocessing.

FIGURE 2. Proximal tibias from four broilers cut through the growthplate to show severetibialdyschondroplasia.The proximal tibia hasbeenpulled backward in the bone on the left. The debility or pain associatedwith this type of deformity has slowed growth and allowed some repairwithreduction in the size of the dyschondroplastic mass. Enlargementoftheproximal endof thetibia is obvious in the other threebones and thereis some necrosis (the dark lines) in the bone on the right. Weight bearingwould cause pain because of compression in this bird.

result in skeletal defects, and are not usually growth-related.

If the hypothesis that rapid growth results inmusculoskeletal deformity is valid, perhaps we shouldconsider how specific defects could be associated withrapid 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, andalignment of bone requires more time than rapid growthallows. 3) The defect could be related to high specificnutrient, enzyme, hormone, or oxygen requirement byspecialized cells (proliferating chondrocytes). 4) Thedefect could be related to metabolic by-products (lacticacid, carbon dioxide) that are increased by rapid growth.5) Young rapidly multiplying cells could be moresusceptible to toxic or metabolic injury.

SPECIFIC DEFECTS

Chronic Painful Lameness in OlderBroilers and Roasters

The problem of lameness in broilers is not restricted todeformity, trauma, or infection. Many heavy, older broilers that have no obvious disease, either on gross or

histologic examination, walk as if they were in severe painand prefer to sit. When forced to rise, they hobble a fewsteps and squat again. It is not clear whether the pain isassociated 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, andaccelerate sexual maturity and increase activity bylengthening light periods in the last 4 wk, which suggests

that the pain is related to body weight and stress onimmature bone and soft tissue. Severe tibial dyschon-droplasia (TD) lesions can produce a similar lameness.

Angular Bone Deformity andValgus-Varus Deformity

Angular bone deformity is the most frequent skeletaldefect in broilers on a nutritionally adequate ratio (Julian,1984). It may be seen as early as 6 to 8 d, or not becomeprominent until 3 to 4 wk. It is usually progressive, andwhen young broilers are affected they usually become

crippled and cannot get to the feed and water. If only oneleg is affected, the bird may not go down. Pain associatedwith the deformity reduces activity and restricts feeding.These broilers may be condemned for emaciation atprocessing or there may be disuse atrophy of the muscle ofthe affected leg (Figure 1). Angular bone deformityappears to be specifically related to rapid growth withinsufficient time for proper alignment and remodelling ofthe bones of the distal tibio-tarsus. It can be reduced byslowing growth in the first 10 to 21 d and by extendeddaily rest (long, dark) periods (Classen and Riddell, 1989;Fontana etal., 1992; Yu and Robinson, 1992; Gordon, 1994).

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FIGURE 3. Spontaneous fracture through the proximal tibias of abroiler with severe tibial dyschondroplasia. This bird was unable to walkand died from dehydration.

FIGURE 4. Crippled broilers classed as creepers. These broilers wereunable to rise and could only move around on their hocks because ofsevere tibial dyschondroplasia causing deformity or fracture, spon-dylolisthesis, osteomyelitis of the vertebrae, impingement of the spinalcord by cartilage or because of ruptured tendons.

FIGURE 5. Radiograph of vertebrae of two broilers with spon-dylolisthesis (normal above).

Vitamin B and trace mineral deficiency may producesimilar deformity by causing growth plate damage.

Tibial Dyschondroplasia andOsteochondrosis

Tibial dyschondroplasia occurs as a result of failure ofproliferating chondrocytes in the growth plate to hyper-trophy to allow vascular penetration and the productionof bone (Thorp et al., 1991, 1993, 1995; Cook and Bai, 1994;Hester, 1994). Mild and moderate lesions may not causelameness, although the proximal end of the tibia may beenlarged. Severe lesions cause weakening of the proximaltibia which is compressed by body weight as the birdwalks, causing painful lameness. The weakened proximaltibia may be pulled backward by the strong gastroc-nemius muscle (Riddell, 1992), causing deformity, or thelarge cartilage mass may develop avascular necrosis andthere 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 unableto reach feed and water.

Tibial dyschondroplasia is most specifically related torapid growth (likely because of a requirement for veryrapid long bone growth) as it is common in meat-type

poultry and rare or absent in other birds. The proximaltibia is the fastest growing growth plate in broilers. Tibialdyschondroplasia is likely caused by lack of specificnutrients required by proliferating chondrocytes. It can bemarkedly reduced by 1,25-dihydroxycholecalciferol (Ren-

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FIGURE 6. Vertebrae cut in the midline to show pinching of thespinal cord by the posterior lip of the fourth thoracic vertebra followingventral dislocation of the anterior end of that vertebra. This is the onlynonfused vertebra in the back of chickens. These birds were unableto riseor walk.

FIGURE 7. Vertebrae cut in midline with spinal cord removed toshow narrowing of the spinal canal and pinching of the cord (normalabove).

FIGURE 8. Vertebrae cut in midline to show pinching of the spinalcord by cartilage at the fourth thoracic vertebra in the two vertebrae inthe center. Normal vertebrae are shown at the top and bottom. The

broilers with the damaged vertebrae were unable to rise, and could onlystruggle around on their hocks.

nie et al., 1993; Leach and Twal, 1994). Because availabilityof 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 growthcauses metabolic acidosis, and panting in hot temperaturecauses respiratory acidosis, so rapid growth may havemore than one effect. Dyschondroplasia is frequentlypresent at other growth centers, particularly the proximalmetatarsals 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 mayinterfere with 1,25-dihydroxycholecalciferol. There is agenetic susceptibility to TD that could be associated withgrowth rate, acid/base balance, or some other mechanism(Leach and Nesheim, 1965). Tibial dyschondroplasia can

be reduced by replacing some NaCl in the diet withNaHCO3, and by avoiding a high P:Ca ratio.

Spondylolisthesis (Kinky Back)

Spondylolisthesis occurs when the ligaments betweenthe third and fourth thoracic vertebrae tear or avulse andallow the anterior end of the fourth vertebra to dislocateventrally. The posterior end rotates upward, impinging

on the spinal cord and causing leg weakness and ataxia(Figures 5, 6, 7, and 8). Affected birds sit on their tail withtheir legs extended or are creepers (Figure 4); they may

be unable to reach feed and water. This deformity is theonly rapid growth-associated skeletal deformity that is

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FIGURE 9. Iatrogenic epiphyseal separation. This lesion is seenfrequently in the legs of broiler chickens when the hip is disarticulatedduring the necropsy procedure. This is not associated with femoral headnecrosis or fragile bones.

FIGURE 10. Bloodin muscle and tissue of the hipin a broilerthatwasfound dead in a crate at the processing plant (dead on arrival). This

broiler bled to death through the end of the proximal femur followingepiphyseal separation during catching and crating.

FIGURE 11. Broiler from processingline showing bilateral rupture ofthe gastrocnemius tendons. The tendons and sheaths are thickenedabove the point of rupture and there is blood in the tissue where theinjury occurred.

FIGURE 12. Proximal tibias in roasters lame from rickets. There isswelling of the epiphyses and backward bending of the proximal end ofthe bone on the left. This lesion could be confused with dyschondropla-sia.

more frequent in females. Osteochondrosis of the articularcartilage of the fourth thoracic vertebra may result inimpingement on the spinal cord and cause similar signs,and is more frequent in males. Poor ligament strength orweak attachment to bone because of immaturity, andheavy breast muscle mass are the most likely cause ofspondylolisthesis. There is a moderate genetic component(Julian, 1990). Osteochondrosis of the articular cartilage ofthe fourth thoracic vertebra and of articular cartilage inother joints is the result of avascular degeneration and isdirectly related to rapid growth of cartilage that becomestoo thick because of insufficient time for remodelling andfailure of chondrocyte differentiation (Thorp et al., 1993).

Epiphyseal Separation

When the legs of young rapidly growing broilerchickens are disarticulated at necropsy, the articular

cartilage is frequently pulled off the femoral head andtrochanter by the joint capsule, leaving the smooth shinygrowth plate (Figure 9). Occasionally, part of the growthplate also pulls away, leaving rough, irregular, necrotic-looking subchondral bone. This growth plate separationmay occur spontaneously in live birds that have dyschon-droplasia or osteomyelitis. When it occurs in live birds it isusually caused by injury, the most frequent being when a

bird is caught and held by one leg (Figure 10). Rapidgrowth does not allow sufficient time for strong tissueformation.

Ruptured Gastrocnemius Tendon

Ruptured gastrocnemius tendons occur most frequentin older broilers, roasters, and broiler breeders. Thegastrocnemius tendon separates by pulling apart justabove the hocks (Figure 11). When the lesion is bilateral,

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FIGURE 13. Condyle asymmetry in a broiler, lame because of slippedgastrocnemius tendon. Most chickenswith slipped tendons havenormalcondyles.

FIGURE 14. Rotated tibia (normal on right). The distal tibia rotateslaterally through its length. The fibula is pulled around as the distal tibiarotates.

FIGURE 15. Lateral curvature of the upper tibia (affected bone on thetop, normal on bottom) in a young broiler that has had one leg out to theside because of failure of the adductor muscle. This leg was out laterallyfor 12 to 14 d and the defect developed because of the position of the legas the leg bone grew.

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 bloodsupply and avascular degeneration, or poor tendonstrength. As the tendon separates prior to rupture, thetendon and tendon sheath are frequently thickened byfibroplasia and other repair process.

Rickets

Rickets can occur in either slow- or fast-growing birds,but is made worse by the higher nutrient requirements ofgrowth. On marginally deficient diets, only the mostrapidly growing broilers are affected. Rickets causesenlargement of the epiphyseal area and occasionallydeformity of the soft, rubbery bone (Figure 12). Mag-

nesium toxicity may cause similar bone deformity (Lee etal., 1980). The thickened growth plate in rickets may besimilar to early TD, and mild rickets may be classedgrossly as TD.

Other Deformities

Other skeletal deformities that cause lameness, such asslipped tendon (Figure 13), rotated tibia (Figure 14), andstraddled legs, are mechanical defects and do not appearto be growth related. High or low incubator temperaturemay also increase the incidence of these defects. Lateralcurvature of the upper tibia in broilers that are straddled

or have one leg out to the side (twisters), is alsomechanical and occurs from pressure on the growing boneafter the bird is down (Figure 15). Scoliosis and twistednecks are congenital defects, not associated with growth.Some nutritional deficiencies may increase the incidenceof these.

WELFARE CONCERNS

Chronic Pain

Chronic pain and the distress associated with it is amajor concern in animal welfare and euthanasia should be

considered in severely affected birds. Prevention ofchronic pain in broilers should be the goal, and more effortshould be made to find management and nutritionaltechniques to reduce chronic pain. Lighting programs

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appear to improve broiler mobility and reduce chronicpain that is not associated with deformity.

Acute Pain

Acute pain often has to do with the trauma of catchingand handling. Better methods of catching and moving

broilers to processing must be devised to reduce traumatic

injury to bones, joints, and muscles.

Cripples

Many of the skeletal deformities in broilers result inbirds that are down and unable to walk. There may bechronic pain as well as anxiety associated with aggressionfrom other birds and with the difficulty of getting to feedand water. Many of these broilers lie on the floor until theydie of dehydration. Poultry workers should be instructedto remove and euthanatize crippled broilers daily.

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