- Email: [email protected]
Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion
The Veterinary Journal xxx (2013) xxx–xxx
Contents lists available at SciVerse ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Review
Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion Isabelle D. Kalmar a,b,⇑, Daisy Vanrompay b, Geert P.J. Janssens a a b
Laboratory of Animal Nutrition, Ghent University, Belgium Department of Molecular Biotechnology, Ghent University, Belgium
a r t i c l e
i n f o
Article history: Accepted 2 March 2013 Available online xxxx Keywords: Broiler ascites syndrome Pulmonary hypertension Pathogenesis Prevention
a b s t r a c t Chickens have been raised as food for human consumption for over 4000 years. Over this time they have been continuously selected for specific desirable characteristics by active selection of parents to produce birds which fit perceived needs. Despite this long history of selective breeding and improvements in rearing techniques, the efficiency with which broiler meat is produced has shown a remarkable leap in recent decades. Persistent selection for rapid growth, high feed utilisation efficiency and large cut yield has resulted in modern meat-type poultry lines with superior genetic potential with regard to productivity. However, mortality and the incidence of metabolic diseases has increased in parallel with growth rate. One such disease is broiler ascites syndrome, which has been shown to be closely associated with the fast growth and high meat yield resulting from intense selection and with modern rearing techniques. The review is focused on the historical background, pathogenesis, epidemiology and prevention of broiler ascites syndrome in modern broiler production. Ó 2013 Elsevier Ltd. All rights reserved.
Introduction The short generation interval of poultry, the relatively high heredity of production traits and industrial-scaled selection have contributed to the success of broiler breeding programs, which have resulted in highly efficient modern broiler strains. In addition to these genetic improvements, the increase in knowledge of nutritional physiology has led to the development of diets which enable rapid growth. Furthermore, better understanding of the response of chickens to the climatic environment has led to housing that provides the most optimal conditions for growth. This enhanced general management has improved production efficiency and supported maximal exploitation of improved genetic traits (Wheeler and Campion, 1993; Rauw et al., 1998). The extent of recent advances achieved in broiler production has been provided by performance trials using 2 2 factorial designs, comparing broiler lines and diets representative of modern systems with those of a few decades earlier. Havenstein et al. (2003a) measured the technical performance of the original 1957 Athens Canadian Randombred Control (ACRBC) strain and the modern 2001 Ross-308 strain fed either a 1957 or a 2001 representative diet. Bodyweight at 42 days of age was only 539 and 578 g in the ACRBC strain when fed the 1957 and 2001 diet, respectively. At the same age, the modern Ross breed reached 2126 and 2672 g
⇑ Corresponding author at: Department of Molecular Biotechnology, Ghent University, Belgium. Tel.: +32 9 264 75 27. E-mail address: [email protected] (I.D. Kalmar).
when fed the same diets. Diet optimisation resulted in a decrease in feed intake relative to bodyweight gain in the ACRBC and Ross strains from 2.34 to 2.14 and from 1.92 to 1.63, respectively (Havenstein et al., 2003a). In conjunction with technical performance, carcass yield expressed as a percentage of bodyweight was also more profoundly increased by genetics rather than dietary improvements. It is clear that dietary modifications showed greater response in the modern compared to the older strain. Carcass yield at the age of 43 days in the ACRBC strain was 60.0% and 61.0% compared to 68.3% and 72.3% in the Ross strain when fed the 1957 and 2001 diets, respectively. In addition, this superior carcass yield in the modern broiler strain was almost entirely attributable to a near doubling of breast meat yield, which is the most valuable cut yield in broilers (Havenstein et al., 2003b). Moreover, Havenstein et al. (2003a) estimated that the sum of all improvements in broiler production achieved between 1957 and 2001 approximated to a reduction in rearing period from 101 to 32 days, and a reduction in feed conversion ratio from 4.42 to 1.47 to yield 1815 g broilers. The significance of this is shown by the fact that a 5 day reduction in rearing period yields an additional raising round per year (Emmerson, 1997). The economic advantage of maximum product yield per kg feed intake becomes obvious considering that feed cost is the principal variable cost in broiler production (Rauw et al., 1998). Intense selection pressure and modern rearing techniques have enabled enhanced production rate and efficiency. However, these advances in productivity have coincided with increased mortality and incidence of metabolic diseases, including broiler ascites syndrome.
1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.03.011
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
2
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Definition Ascites is defined as excessive accumulation of transudate fluid within the peritoneal spaces due to increased vascular permeability, increased tissue or decreased plasma oncotic pressure, obstructed lymph drainage, increased hydraulic pressure in the splanchnic venous system or a combination of these (Julian, 1993). Broiler ascites syndrome or pulmonary hypertension induced ascites is the most prevalent form of ascites in broilers and primarily associated with increased intravascular pressure in the portal system resulting from right ventricular failure secondary to pulmonary hypertension. This mechanism is distinct from ascites caused by liver pathology, such as fibrosis, neoplasia, granuloma, amyloidosis or infectious causes of obstructed hepatic venous return. Yet, it also leads to increased fluid pressure in the hepatic capillary bed, through which high protein lymph transudates from the fenestrated hepatic sinusoids (Julian, 1993; Currie, 1999).
Diagnostic criteria Independent of the numerous pathologies leading to ascites in broilers, the common end result is pressure on the air sacs causing respiratory signs (Bottje et al., 1998; Julian, 1998). Clinical signs are non-specific and include dullness, depression, open beak breathing, distended abdomen, reluctance to move, dilated superficial veins, cyanosis, tachypnoea and bradycardia (Julian, 1993; Currie, 1999; Rehman et al., 1999). Death generally occurs late in the rearing period or even during transport to the slaughter house (Nijdam et al., 2006). Post-mortem findings of broiler ascites syndrome include accumulation of ascitic fluid in the peritoneal cavities, hydropericardium, right ventricular hypertrophy, and generalized venous congestion (Hakim, 1988). Right ventricular hypertrophy denotes pulmonary hypertension and is indicated by an increase in right ventricular weight to total ventricular weight ratio (RV:TV P 0.27) or by right mean electrical axis deviation on electrocardiogram (Julian, 1993; Zhou et al., 2008). Right ventricular failure due to pulmonary hypertension is indicated by an RV:TV P 0.30 (Zhou et al., 2008). The ascitic fluid is a straw-yellow coloured, noninflammatory transudate with or without fibrin clots (Rehman et al., 1999). The presence of a large amount of ascitic fluid with strands of fibrin in the hepatoperitoneal space suggests ascites in response to pulmonary hypertension or to hepatopathies with obstructed venous flow. Fibrin clots with fluid in other spaces, especially if the quantity of fluid is limited, is suggestive of ascites associated with increased vascular permeability, for example due to bacterial or chemical induced endothelial damage (Julian, 1993). Further macroscopic lesions of broiler ascites syndrome include congested, oedematous lungs and haemorrhagic and swollen liver and kidneys. Histopathology of lung tissue shows pneumonic lesions with congestion of alveoli, infiltration of heterophils and proliferation of connective tissue in alveolar septa and in severe cases in interlobular septa. The liver shows congestion, necrosis, lymphocyte aggregates and proliferation of connective tissue in the sinusoidal spaces and hepatic triad, which is also infiltrated with inflammatory cells. Lesions in the kidney include congestion, vacuolar degeneration, and necrosis and lymphocyte aggregation in renal tubules (Rehman et al., 1999). Physiological blood parameters indicative of ascites susceptibility as well as ascites syndrome include a progressive increase in haematocrit and progressive hypercapnia (increased partial pressure of CO2 in venous blood) and hypoxaemia (reduced partial pressure of O2 in venous blood) (van As et al., 2010). Further haematological parameters indicative of ascites from right ventricular
failure include an increase in erythrocyte number, haemoglobin and mean cell volume. Blood protein is low, mainly due to reduced albumin. Biochemistry parameters show only minor changes in electrolytes, but enzymes reflecting tissue damage are elevated (Cardenas et al., 1985).
Pathogenesis A significant increase in the incidence of pulmonary hypertension induced ascites in broilers arose as a negative side-effect of improved rearing techniques and selective breeding towards fast growing, high meat-yielding modern broiler strains (Julian, 1993; Rauw et al., 1998). The central aetiology of the disease is a hypoxaemic condition resulting from an imbalance between oxygen requirement and oxygen supply (Fig. 1). A cascade of compensatory mechanisms eventually leads to increased pulmonary pressure, which is initially overcome by right ventricular heart hypertrophy. If persistent, this leads to right ventricular valve insufficiency, volume overload, right heart dilatation, and right ventricular failure. As a result, venous blood pressure increases and fluid leaks out of the veins and accumulates in peritoneal cavities and pericardium, resulting in ascites and further impairment of cardiac function (Julian, 1998; Currie, 1999). The causes of the high incidence of insufficient oxygen supply and subsequent development of broiler ascites syndrome in modern broiler lines are threefold. Firstly, a superior growth rate inherently implies a high oxygen demand to sustain metabolic needs. Secondly, the increased growth rate of modern broilers results in a significant reduction in relative heart and lung size, and thus diminished cardiopulmonary capacity. This was shown by Havenstein et al. (2003b), who demonstrated a 10.3% and 9.0% decline in relative heart and lung size in 43-day-old birds when comparing the ACBRC strain fed a 1957 representative diet with the 2001 Ross-308 strain fed a 2001 representative diet. Low thyroid hormone activity accompanying selection for rapid growth and improved feed efficiency, for instance, has been shown to impair lung development in broilers (Hassanzadeh et al., 2008). Compared to other birds, the respiratory membrane is thicker in poultry, and in meat-type chickens in particular, and broilers are presumed to display a lower rate of oxygen diffusion from the lungs into red blood cell haemoglobin (Baghbanzadeh and Decuypere, 2008). In addition, a high growth rate implies a faster blood flow through the capillary bed of the lungs, which possibly further impairs oxygenation of blood (Wideman and Kirby, 1995a, 1995b). Thirdly, an increase in metabolic rate not only augments oxygen requirement at tissue level, but also elevates mitochondrial production of reactive oxygen species. Oxidative stress, in turn, causes lipid peroxidation mediated damage to the pulmonary vasculature, which further deteriorates oxygenation and aggravates hypoxaemia (Bottje and Wideman, 1995; Diaz-Cruz et al., 2003; Aksit et al., 2008). In succession, augmented free radical release caused by hypoxic lung injury feeds a vicious cycle which leads to progressive hypoxaemia (Herget et al., 2000). Given these additional impairments, it is not surprising that fast growth (which implies increased oxygen requirement) in broiler strains that are already faced with a relatively undersized cardiopulmonary capacity, may result in hypoxaemia. Besides genetic and management factors supporting fast and profitable growth, other contributing factors in the pathogenesis of pulmonary hypertension induced ascites include environmental, dietary or animal factors that additionally augment the physiological oxygen requirement or decrease oxygen supply. To maintain normal body temperature in conditions of cold stress, for instance, endogenous heat production is upregulated through an increase in metabolic rate and concomitantly both oxygen requirement and
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
3
PULMONARY HYPERTENSION
Fig. 1. Pathogenesis of and preventive measures for broiler ascites syndrome. FA; fatty acids; UFA, unsaturated fatty acids; PUFA, polyunsaturated fatty acids; SFA, saturated fatty acids.
blood flow are elevated (Julian et al., 1989; Lubritz and McPherson, 1994; Julian, 2000). Respiratory disease and poor air quality comprise examples of conditions that additionally may impair blood oxygenation and thus lower oxygen supply (Julian, 2000). Poor air quality is typically attributable to insufficient ventilation, through which dust and gaseous pollutants (such as ammonia and carbon monoxide) build up in the air (Bottje et al., 1998). A well-known dietary ascites inciting condition is salt intoxication. Excess sodium intake in the form of salt from drinking water or feed increases plasma sodium concentrations, especially in young chickens, and this results in volume expansion and increased blood flow. The small pulmonary blood capillaries in the
rigid avian lung cannot dilate sufficiently to accommodate the increased blood flow effectively (Mirsalimi et al., 1992). The resulting pulmonary hypertension is further exacerbated due to increased resistance to blood flow by sodium-induced arteriolar vasoconstriction and reduced erythrocyte deformability (Hakim, 1988). Thus salt-induced volume overload causes right ventricular hypertrophy subsequent to pulmonary hypertension in birds (Julian, 1987). In general, hypertension exciting factors appear to be additive to other conditions that incite ascites (Julian, 1987; Julian et al., 1992) in broilers in contrast to mammals, where excess salt induces left ventricular hypertrophy subsequent to systemic hypertension (Fields et al., 1991).
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
4
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Epidemiology Broiler ascites syndrome used to be primarily observed in birds raised at high altitude, which entails low partial oxygen pressure and thus diminished oxygen supply. However, since 1980, its incidence has steadily increased and, more importantly, it has been reported at lower altitudes and even at sea level (Julian, 1993). In 1997, the world broiler ascites survey revealed an average incidence of ascites in 4.7% of live broilers worldwide (Maxwell and Robertson, 1997). In the UK, the incidence of ascites mortality increased from 0.03% to 0.04% in 1965 to 0.7%, 0.9% and 1.4% in 1991, 1992 and 1993, respectively (Hemsley, 1965; Maxwell and Robertson, 1998). Similarly, in Western Canada, mortality due to ascites increased from 0% to 0.02% in 1975, to 1% to 2% in 1995 (Brigden and Riddell, 1975; Olkowski et al., 1996). These figures clearly indicate that this metabolic disorder had become a major non-infectious cause of loss in the modern broiler industry. Of notice is a high variation in incidence between flocks. For instance, ascites mortality in UK broiler flocks in 1993 ranged between 0% and 10% and in USA broiler flocks in 2002 between 0% and 30% (Maxwell and Robertson, 1998; Pavlidis et al., 2007). To date, broiler breeder companies have developed and implemented strategies to select against ascites susceptibility. Genetic analyses have demonstrated moderate to high heritability estimates (0.11–0.44) for ascites indicator traits. Divergent selection for ascites susceptibility following exposure to ascites-inciting conditions has been shown to be feasible within a few generations and with acceptable losses in productivity (Druyan et al., 2007a, 2007b, 2008; Pavlidis et al., 2007). Nonetheless, the available literature data indicates that ascites susceptibility is still present in modern broiler lines and remains positively associated with growth rate. This is substantiated by an incidence of ascites mortality of 5–10% in modern broilers when fed high-energy pellets ad libitum (Druyan and Cahaner, 2007). Arce-Menocal et al. (2009) reported ascites mortality rates of 10.4% and 12.4% in modern strain A and 3.9% and 7.7% in modern strain B when reared to 42 days of age on a diet based on the 1994 National Research Council recommendations presented as either a mash or as a crumb (which promotes growth), respectively. Moreover, veterinary condemnation records of the Canadian Food Inspection Agency show that although the proportion of broiler carcass condemnations related to ascites peaked at 19% in 1996, in 2011, 8% of such condemnations, representing 0.08% of slaughtered chickens or over half a million birds, were rejected for consumption because of ascites (AAC, 2012). These data do not include ascites mortality at farm level or during transport to the slaughter house. Nevertheless, compared to its peak, broiler ascites syndrome is considerably less common as a result of management practices that reduce growth rate (Druyan and Cahaner, 2007; Hassanzadeh, 2009). Some of those are even legally imposed. New EU welfare regulations, for example, prohibit the use of photoperiods longer than 18 h after the age of 7 days, for which one of the key intentions is exactly aimed at reducing growth rate and consequently ascites mortality and skeletal diseases (EC, 2007).
The most common prevention strategies are feed and lighting regimes that slow down early growth (Ozkan et al., 2010). Limitation of early growth rate can be achieved by qualitative feed restriction, which implies dilution of the energetic density of the ration, or by quantitative feed restriction through offering a diminished quantity of feed each day, periodic feed withdrawal or a lighting schedule with increased dark hours. However, there a several concerns regarding these methods. Firstly, the effectiveness of limiting early growth rate to diminish the incidence of ascites is debatable (reviewed by Madrigal et al. (2002)). Secondly, several trials indicate inadequate compensatory growth in later growth phases, resulting in depressed bodyweight or yield at market age (see, for example, Acar et al., 1995; Lee and Leeson, 2001). Thirdly, Lee and Leeson (2001) pointed out that qualitative feed restriction entails extra costs in the form of non-nutritive fillers and higher transport costs per unit of feed. The authors suggested that quantitative feed restriction is therefore preferable at an industrial scale. Fourthly, feed restriction in broiler lines that were selected for high feed intake may impair welfare as demonstrated both by physiological stress parameters and behavioural criteria indicative of frustration to hunger (Savory and Lariviere, 2000). Quantitative feed restriction through limiting daily amounts of feed does not however seem to diminish broiler welfare more than qualitative feed restriction through lowered energetic density of the diet (Savory et al., 1996; Savory and Lariviere, 2000). Baghbanzadeh and Decuypere (2008) drew attention to adverse secondary effects of imprudent feed restriction on adequate intake of, for example, anti-coccidial products on the control of coccidiosis, or pigmentation precursors on product quality. Optimisation of the diet to ameliorate ascites syndrome has been investigated to a limited extent. The multi-factorial aetiology of the syndrome means that pulmonary hypertension can be responsive to dietary strategies other than limitation of early growth. Such interventions need to have a low economic cost, have minimal effects on performance traits, product quality, and animal health and welfare. A dietary shift in fatty acid profile towards a higher ratio of unsaturated to saturated fatty acids has been shown to improve erythrocyte deformability and so diminish the resistance of blood flow through the lung capillaries (Bond et al., 1996; Walton et al., 1999). Furthermore, as suggested by Bond et al. (1996) and Walton et al. (1999), dietary fat sources with a high proportion of n-3 and n6 polyunsaturated fatty acids (such as flaxseed oil) may additionally slow down the development of broiler ascites syndrome due to the release of endogenous coronary relaxants and attenuated inflammatory compounds derived from cellular membrane lipids. A reduction in reactive oxygen mediated damage to the cardiopulmonary system forms yet another approach that could alleviate the predisposition of fast-growing birds to ascites mortality (Herget et al., 2000). Dietary supplementation with anti-oxidant vitamins can reduce oxidative damage and improve pulmonary vascular performance (see, for example, Lorenzoni and Ruiz-Feria, 2006; Nain et al., 2008; Bautista-Ortega and Ruiz-Feria, 2010). However, substantial beneficial effects on the incidence of broiler ascites syndrome cannot always be demonstrated (Baghbanzadeh and Decuypere, 2008; Nain et al., 2008; Xiang et al., 2002).
Prevention Impact on the broiler industry The effect on productivity is a crucial factor in evaluating ascites abating strategies not only from an economic point of view, but also because the pathogenesis of broiler ascites syndrome is positively interconnected with growth rate. Genetic selection for ascites resistant broiler lines is considered to be the ideal permanent solution to the ascites problem. However, until selection programs successfully develop such broiler lines and these new strains are shown to be satisfactory, alternative preventive measures have to be considered.
Ascites mortality generally occurs late in the production round. In addition, ascitic birds are rejected for consumption (Haslam et al., 2008). Thus affected birds have been fed for the entire rearing cycle, but have no economic value (Druyan and Cahaner, 2007). Even at a low incidence, the economic cost of broiler ascites syndrome is therefore considerable. Moreover, it is a severe welfare problem as the symptoms, such as breathing difficulties, are progressive and distressing (Aksit et al., 2008).
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Conclusions Intense selection of broilers for fast growth and high meat yield has been highly successful, but has resulted in a significant increase in the incidence of broiler ascites syndrome and associated mortality. The central aetiology of this metabolic syndrome is a hypoxaemic condition resulting from an imbalance between oxygen requirement and oxygen supply. Modern broiler lines are highly metabolically active, which facilitates growth but requires a high oxygen supply. This is compounded by the fact that selective breeding for high meat yield led to birds with a disproportionately low heart and lung size, which consequently have a relatively underdeveloped capacity for blood oxygenation. A high metabolic rate implies increased free radical mediated damage to the pulmonary vasculature as well as a faster blood flow through the lungs, which both further diminish oxygenation of blood. The resultant imbalance between oxygen demand and supply incites pulmonary hypertension and subsequently right heart failure followed by transudation of fluid into the abdominal cavity, which is defined as ascites. Selection for ascites resistance and management practices reducing early growth have lowered the overall incidence of ascites compared to its peak years. However, provided allowance of performance at full genetic potential, ascites susceptibility is still present in modern broiler lines. Ideally preventive measures should preserve optimal performance while sustaining product quality and animal welfare. Selective breeding for ascites resistant strains is considered a permanent solution to the problem. However, until resistant strains are successfully developed and implemented on a global scale, alternative measures remain imperative. Optimisation of the diet and rearing conditions, and development of new feed additives that ameliorate the ascites syndrome form such alternative measures. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. References Agriculture and Agrifood Canada (AAC), 2012. The Veterinary Condemnation Records of the Canadian Food Inspection Agency. www.agr-gc.ca. Acar, N., Sizemore, F.G., Leach, G.R., Wideman, R.F., Owen, R.L., Barbato, G.F., 1995. Growth of broiler-chickens in response to feed restriction regimens to reduce ascites. Poultry Science 74, 833–843. Aksit, M., Altan, O., Karul, A.B., Balkaya, M., Ozdemir, D., 2008. Effects of cold temperature and vitamin E supplementation on oxidative stress, troponin-T level, and other ascites-related traits in broilers. Archiv Fur Geflugelkunde 72, 221–230. Arce-Menocal, J., Evila-Gonzalez, E., Lopez-Coello, C., Garibay-Torres, L., MartinezLemus, L.A., 2009. Bodyweight, feed-particle size, and ascites incidence revisited. Journal of Applied Poultry Research 18, 465–471. Baghbanzadeh, A., Decuypere, E., 2008. Ascites syndrome in broilers: Physiological and nutritional perspectives. Avian Pathology 37, 117–126. Bautista-Ortega, J., Ruiz-Feria, C.A., 2010. L-arginine and antioxidant vitamins E and C improve the cardiovascular performance of broiler chickens grown under chronic hypobaric hypoxia. Poultry Science 89, 2141–2146. Bond, J.M., Julian, R.J., Squires, E.J., 1996. Effect of dietary flax oil and hypobaric hypoxia on right ventricular hypertrophy and ascites in broiler chickens. British Poultry Science 37, 731–741. Bottje, W.G., Wideman, R.F., 1995. Potential role of free radicals in the pathogenesis of pulmonary hypertension syndrome. Poultry and Avian Biology Reviews 6, 211–231. Bottje, W.G., Wang, S., Kelly, F.J., Dunster, C., Williams, A., Mudway, I., 1998. Antioxidant defenses in lung lining fluid of broilers: Impact of poor ventilation conditions. Poultry Science 77, 516–522. Brigden, J.L., Riddell, C., 1975. A survey of mortality in four broiler flocks in Western Canada. Canadian Veterinary Journal 16, 194–200. Cardenas, D.M., Hernandez, A., Osuna, O., 1985. Algunos valores hematimétricos y de proteinas totales en polios Arbor Acres sanos y asciticos en la Sabana de Bogota. Revista Acovez 9, 42–44.
5
Currie, R.J.W., 1999. Ascites in poultry: Recent investigations. Avian Pathology 28, 313–326. Diaz-Cruz, A., Serret, M., Ramirez, G., Avila, E., Guinzberg, R., Pina, E., 2003. Prophylactic action of lipoic acid on oxidative stress and growth performance in broilers at risk of developing ascites syndrome. Avian Pathology 32, 645–653. Druyan, S., Cahaner, A., 2007. Segregation among test-cross progeny suggests that two complementary dominant genes explain the difference between ascitesresistant and ascites-susceptible broiler lines. Poultry Science 86, 2295–2300. Druyan, S., Ben-David, A., Cahaner, A., 2007a. Development of ascites-resistant and ascites-susceptible broiler lines. Poultry Science 86, 811–822. Druyan, S., Shlosberg, A., Cahaner, A., 2007b. Evaluation of growth-rate, bodyweight, heart rate, and blood parameters as potential indicators for selection against susceptibility to the ascites syndrome in broilers. Poultry Science 86, 621–629. Druyan, S., Hadad, Y., Cahaner, A., 2008. Growth rate of ascites-resistant versus ascites-susceptible broilers in commercial and experimental lines. Poultry Science 87, 904–911. European Council (EC), 2007. Council Directive 2007/43/EC: Minimum rules for the protection of chickens kept for meat production. Official Journal of the European Union 182, 19–28. Emmerson, D.A., 1997. Commercial approaches to genetic selection for growth and feed conversion in domestic poultry. Poultry Science 76, 1121–1125. Fields, N.G., Yuan, B.X., Leenen, F.H., 1991. Sodium induced cardiac hypertrophy. Circulation Research 68, 745–755. Hakim, T.S., 1988. Erythrocyte deformability and segmental pulmonary vascular resistance: Osmolarity and heat treatment. Journal of Applied Physiology 65, 1634–1641. Haslam, S.M., Knowles, T.G., Brown, S.N., Wilkins, L.J., Kestin, S.C., Warriss, P.D., Nicol, C.J., 2008. Prevalence and factors associated with it, of birds dead on arrival at the slaughterhouse and other rejection conditions in broiler chickens. British Poultry Science 49, 685–696. Hassanzadeh, M., 2009. New approach for the incidence of ascites syndrome in broiler chickens and management control of the metabolic disorders. International Journal of Poultry Science 8, 90–98. Hassanzadeh, M., Buyse, J., Decuypere, E., 2008. Further evidence for the involvement of anatomical parameters of cardiopulmonary system in the development of ascites syndrome in broiler chickens. Acta Veterinaria Hungarica 71, 71–80. Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003a. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 1509–1518. Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003b. Growth, liveability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 1500–1508. Hemsley, L.A., 1965. Causes of mortality in fourteen flocks of broiler chickens. Veterinary Record 77, 467–472. Herget, J., Wilhelm, J., Novotna, J., Eckhardt, A., Vytasek, R., Mrazkova, L., Ostadal, M., 2000. A possible role of the oxidant tissue injury in the development of hypoxic pulmonary hypertension. Physiological Research 49, 493–501. Julian, R.J., 1987. The effect of increased sodium in the drinking-water on right ventricular hypertrophy, right ventricular failure and ascites in broilerchickens. Avian Pathology 16, 61–71. Julian, R.J., 1993. Ascites in poultry. Avian Pathology 22, 419–454. Julian, R.J., 1998. Rapid growth problems: Ascites and skeletal deformities in broilers. Poultry Science 77, 1773–1780. Julian, R.J., 2000. Physiological, management and environmental triggers of the ascites syndrome: A review. Avian Pathology 29, 519–527. Julian, R.J., Mcmillan, I., Quinton, M., 1989. The effect of cold and dietary energy on right ventricular hypertrophy, right ventricular failure and ascites in meat-type chickens. Avian Pathology 18, 675–684. Julian, R.J., Caston, L.J., Leeson, S., 1992. The effect of dietary-sodium on right ventricular failure-induced ascites, gain and fat deposition in meat-type chickens. Canadian Journal of Veterinary Research 56, 214–219. Lee, K.H., Leeson, S., 2001. Performance of broilers fed limited quantities of feed or nutrients during seven to fourteen days of age. Poultry Science 80, 446–454. Lorenzoni, A.G., Ruiz-Feria, C.A., 2006. Effects of vitamin E and L-arginine on cardiopulmonary function and ascites parameters in broiler chickens reared under subnormal temperatures. Poultry Science 85, 2241–2250. Lubritz, D.L., McPherson, B.N., 1994. Effect of genotype and cold stress on incidence of ascites in cockerels. Journal of Applied Poultry Research 3, 171–178. Madrigal, S.E., Watkins, S.E., Anthony, N.B., Wall, C.E., Fritts, C.A., Waldroup, P.W., 2002. Effect of dietary modifications designed to reduce early growth rate on live performance and on incidence and severity of ascites in two commercial broiler strains when maintained under low ventilation or low temperature models. International Journal of Poultry Science 1, 150–157. Maxwell, M.H., Robertson, G.W., 1997. World broiler ascites survey. Poultry International 36, 16–30. Maxwell, M.H., Robertson, G.W., 1998. UK survey of broiler ascites and sudden death syndromes in 1993. British Poultry Science 39, 203–215. Mirsalimi, S.M., O’Brien, P.J., Julian, R.J., 1992. Blood volume increase in salt-induced pulmonary hypertension, heart failure and ascites in broiler and white leghorn chickens. Canadian Journal of Veterinary Research 57, 110–113. Nain, S., Wojnarowicz, C., Laarveld, B., Olkowski, A.A., 2008. Effects of dietary vitamin E and C supplementation on heart failure in fast growing commercial broiler chickens. British Poultry Science 49, 697–704. Nijdam, E., Zailan, A.R.M., van Eck, J.H.H., Decuypere, E., Stegeman, J.A., 2006. Pathological features in dead on arrival broilers with special reference to heart disorders. Poultry Science 85, 1303–1308.
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
6
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Olkowski, A.A., Kumor, L., Classen, H.L., 1996. Changing epidemiology of ascites in broiler chickens. Canadian Journal of Animal Science 76, 135–140. Ozkan, S., Takma, C., Yahav, S., Sogut, B., Turkmut, L., Erturun, H., Cahaner, A., 2010. The effects of feed restriction and ambient temperature on growth and ascites mortality of broilers reared at high altitude. Poultry Science 89, 974–985. Pavlidis, H.O., Balog, J.M., Stamps, L.K., Hughes, J.D., Huff, W.E., Anthony, N.B., 2007. Divergent selection for ascites incidence in chickens. Poultry Science 86, 2517– 2529. Rauw, W.M., Kanis, E., Noordhuizen-Stassen, E.N., Grommers, F.J., 1998. Undesirable side effects of selection for high production efficiency in farm animals: A review. Livestock Production Science 56, 15–33. Rehman, H., Khan, A., Khan, M.Z., 1999. Clinical, gross and histopathological observations in spontaneous cases of ascites syndrome in broiler chickens reared at low altitude. Pakistan Veterinary Journal 19, 115–118. Savory, C.J., Lariviere, J.M., 2000. Effects of qualitative and quantitative food restriction treatments on feeding motivational state and general activity level of growing broiler breeders. Applied Animal Behaviour Science 69, 135–147. Savory, C.J., Hocking, P.M., Mann, J.S., Maxwell, M.H., 1996. Is broiler breeder welfare improved by using qualitative rather than quantitative food restriction to limit growth rate? Animal Welfare 5, 105–127.
van As, P., Elferink, M.G., Closter, A.M., Vereijken, A., Bovenhuis, H., Crooijmans, R.P.M.A., 2010. The use of blood gas parameters to predict ascites susceptibility in juvenile broilers. Poultry Science 89, 1684–1691. Walton, J.P., Bond, J.M., Julian, R.J., Squires, E.J., 1999. Effect of dietary flax oil and hypobaric hypoxia on pulmonary hypertension and haematological variables in broiler chickens. British Poultry Science 40, 385–391. Wheeler, M.B., Campion, D.R., 1993. Animal production – A longstanding biotechnological success. American Journal of Clinical Nutrition 58, S276–S281. Wideman, R.F., Kirby, Y.K., 1995a. A pulmonary-artery clamp model for inducing pulmonary-hypertension syndrome (ascites) in broilers. Poultry Science 74, 805–812. Wideman, R.F., Kirby, Y.K., 1995b. Evidence of a ventilation–perfusion mismatch during acute unilateral pulmonary-artery occlusion in broilers. Poultry Science 74, 1209–1217. Xiang, R.P., Sun, W.D., Wang, J.Y., Wang, X.L., 2002. Effect of vitamin c on pulmonary hypertension and muscularisation of pulmonary arterioles in broilers. British Poultry Science 43, 705–712. Zhou, D.H., Wu, J., Yang, S.J., Cheng, D.C., Guo, D.Z., 2008. Intravenous endothelin-1 triggers pulmonary hypertension syndrome (ascites) in broilers. Veterinarni Medicina 53, 381–391.
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
Contents lists available at SciVerse ScienceDirect
The Veterinary Journal journal homepage: www.elsevier.com/locate/tvjl
Review
Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion Isabelle D. Kalmar a,b,⇑, Daisy Vanrompay b, Geert P.J. Janssens a a b
Laboratory of Animal Nutrition, Ghent University, Belgium Department of Molecular Biotechnology, Ghent University, Belgium
a r t i c l e
i n f o
Article history: Accepted 2 March 2013 Available online xxxx Keywords: Broiler ascites syndrome Pulmonary hypertension Pathogenesis Prevention
a b s t r a c t Chickens have been raised as food for human consumption for over 4000 years. Over this time they have been continuously selected for specific desirable characteristics by active selection of parents to produce birds which fit perceived needs. Despite this long history of selective breeding and improvements in rearing techniques, the efficiency with which broiler meat is produced has shown a remarkable leap in recent decades. Persistent selection for rapid growth, high feed utilisation efficiency and large cut yield has resulted in modern meat-type poultry lines with superior genetic potential with regard to productivity. However, mortality and the incidence of metabolic diseases has increased in parallel with growth rate. One such disease is broiler ascites syndrome, which has been shown to be closely associated with the fast growth and high meat yield resulting from intense selection and with modern rearing techniques. The review is focused on the historical background, pathogenesis, epidemiology and prevention of broiler ascites syndrome in modern broiler production. Ó 2013 Elsevier Ltd. All rights reserved.
Introduction The short generation interval of poultry, the relatively high heredity of production traits and industrial-scaled selection have contributed to the success of broiler breeding programs, which have resulted in highly efficient modern broiler strains. In addition to these genetic improvements, the increase in knowledge of nutritional physiology has led to the development of diets which enable rapid growth. Furthermore, better understanding of the response of chickens to the climatic environment has led to housing that provides the most optimal conditions for growth. This enhanced general management has improved production efficiency and supported maximal exploitation of improved genetic traits (Wheeler and Campion, 1993; Rauw et al., 1998). The extent of recent advances achieved in broiler production has been provided by performance trials using 2 2 factorial designs, comparing broiler lines and diets representative of modern systems with those of a few decades earlier. Havenstein et al. (2003a) measured the technical performance of the original 1957 Athens Canadian Randombred Control (ACRBC) strain and the modern 2001 Ross-308 strain fed either a 1957 or a 2001 representative diet. Bodyweight at 42 days of age was only 539 and 578 g in the ACRBC strain when fed the 1957 and 2001 diet, respectively. At the same age, the modern Ross breed reached 2126 and 2672 g
⇑ Corresponding author at: Department of Molecular Biotechnology, Ghent University, Belgium. Tel.: +32 9 264 75 27. E-mail address: [email protected] (I.D. Kalmar).
when fed the same diets. Diet optimisation resulted in a decrease in feed intake relative to bodyweight gain in the ACRBC and Ross strains from 2.34 to 2.14 and from 1.92 to 1.63, respectively (Havenstein et al., 2003a). In conjunction with technical performance, carcass yield expressed as a percentage of bodyweight was also more profoundly increased by genetics rather than dietary improvements. It is clear that dietary modifications showed greater response in the modern compared to the older strain. Carcass yield at the age of 43 days in the ACRBC strain was 60.0% and 61.0% compared to 68.3% and 72.3% in the Ross strain when fed the 1957 and 2001 diets, respectively. In addition, this superior carcass yield in the modern broiler strain was almost entirely attributable to a near doubling of breast meat yield, which is the most valuable cut yield in broilers (Havenstein et al., 2003b). Moreover, Havenstein et al. (2003a) estimated that the sum of all improvements in broiler production achieved between 1957 and 2001 approximated to a reduction in rearing period from 101 to 32 days, and a reduction in feed conversion ratio from 4.42 to 1.47 to yield 1815 g broilers. The significance of this is shown by the fact that a 5 day reduction in rearing period yields an additional raising round per year (Emmerson, 1997). The economic advantage of maximum product yield per kg feed intake becomes obvious considering that feed cost is the principal variable cost in broiler production (Rauw et al., 1998). Intense selection pressure and modern rearing techniques have enabled enhanced production rate and efficiency. However, these advances in productivity have coincided with increased mortality and incidence of metabolic diseases, including broiler ascites syndrome.
1090-0233/$ - see front matter Ó 2013 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.tvjl.2013.03.011
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
2
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Definition Ascites is defined as excessive accumulation of transudate fluid within the peritoneal spaces due to increased vascular permeability, increased tissue or decreased plasma oncotic pressure, obstructed lymph drainage, increased hydraulic pressure in the splanchnic venous system or a combination of these (Julian, 1993). Broiler ascites syndrome or pulmonary hypertension induced ascites is the most prevalent form of ascites in broilers and primarily associated with increased intravascular pressure in the portal system resulting from right ventricular failure secondary to pulmonary hypertension. This mechanism is distinct from ascites caused by liver pathology, such as fibrosis, neoplasia, granuloma, amyloidosis or infectious causes of obstructed hepatic venous return. Yet, it also leads to increased fluid pressure in the hepatic capillary bed, through which high protein lymph transudates from the fenestrated hepatic sinusoids (Julian, 1993; Currie, 1999).
Diagnostic criteria Independent of the numerous pathologies leading to ascites in broilers, the common end result is pressure on the air sacs causing respiratory signs (Bottje et al., 1998; Julian, 1998). Clinical signs are non-specific and include dullness, depression, open beak breathing, distended abdomen, reluctance to move, dilated superficial veins, cyanosis, tachypnoea and bradycardia (Julian, 1993; Currie, 1999; Rehman et al., 1999). Death generally occurs late in the rearing period or even during transport to the slaughter house (Nijdam et al., 2006). Post-mortem findings of broiler ascites syndrome include accumulation of ascitic fluid in the peritoneal cavities, hydropericardium, right ventricular hypertrophy, and generalized venous congestion (Hakim, 1988). Right ventricular hypertrophy denotes pulmonary hypertension and is indicated by an increase in right ventricular weight to total ventricular weight ratio (RV:TV P 0.27) or by right mean electrical axis deviation on electrocardiogram (Julian, 1993; Zhou et al., 2008). Right ventricular failure due to pulmonary hypertension is indicated by an RV:TV P 0.30 (Zhou et al., 2008). The ascitic fluid is a straw-yellow coloured, noninflammatory transudate with or without fibrin clots (Rehman et al., 1999). The presence of a large amount of ascitic fluid with strands of fibrin in the hepatoperitoneal space suggests ascites in response to pulmonary hypertension or to hepatopathies with obstructed venous flow. Fibrin clots with fluid in other spaces, especially if the quantity of fluid is limited, is suggestive of ascites associated with increased vascular permeability, for example due to bacterial or chemical induced endothelial damage (Julian, 1993). Further macroscopic lesions of broiler ascites syndrome include congested, oedematous lungs and haemorrhagic and swollen liver and kidneys. Histopathology of lung tissue shows pneumonic lesions with congestion of alveoli, infiltration of heterophils and proliferation of connective tissue in alveolar septa and in severe cases in interlobular septa. The liver shows congestion, necrosis, lymphocyte aggregates and proliferation of connective tissue in the sinusoidal spaces and hepatic triad, which is also infiltrated with inflammatory cells. Lesions in the kidney include congestion, vacuolar degeneration, and necrosis and lymphocyte aggregation in renal tubules (Rehman et al., 1999). Physiological blood parameters indicative of ascites susceptibility as well as ascites syndrome include a progressive increase in haematocrit and progressive hypercapnia (increased partial pressure of CO2 in venous blood) and hypoxaemia (reduced partial pressure of O2 in venous blood) (van As et al., 2010). Further haematological parameters indicative of ascites from right ventricular
failure include an increase in erythrocyte number, haemoglobin and mean cell volume. Blood protein is low, mainly due to reduced albumin. Biochemistry parameters show only minor changes in electrolytes, but enzymes reflecting tissue damage are elevated (Cardenas et al., 1985).
Pathogenesis A significant increase in the incidence of pulmonary hypertension induced ascites in broilers arose as a negative side-effect of improved rearing techniques and selective breeding towards fast growing, high meat-yielding modern broiler strains (Julian, 1993; Rauw et al., 1998). The central aetiology of the disease is a hypoxaemic condition resulting from an imbalance between oxygen requirement and oxygen supply (Fig. 1). A cascade of compensatory mechanisms eventually leads to increased pulmonary pressure, which is initially overcome by right ventricular heart hypertrophy. If persistent, this leads to right ventricular valve insufficiency, volume overload, right heart dilatation, and right ventricular failure. As a result, venous blood pressure increases and fluid leaks out of the veins and accumulates in peritoneal cavities and pericardium, resulting in ascites and further impairment of cardiac function (Julian, 1998; Currie, 1999). The causes of the high incidence of insufficient oxygen supply and subsequent development of broiler ascites syndrome in modern broiler lines are threefold. Firstly, a superior growth rate inherently implies a high oxygen demand to sustain metabolic needs. Secondly, the increased growth rate of modern broilers results in a significant reduction in relative heart and lung size, and thus diminished cardiopulmonary capacity. This was shown by Havenstein et al. (2003b), who demonstrated a 10.3% and 9.0% decline in relative heart and lung size in 43-day-old birds when comparing the ACBRC strain fed a 1957 representative diet with the 2001 Ross-308 strain fed a 2001 representative diet. Low thyroid hormone activity accompanying selection for rapid growth and improved feed efficiency, for instance, has been shown to impair lung development in broilers (Hassanzadeh et al., 2008). Compared to other birds, the respiratory membrane is thicker in poultry, and in meat-type chickens in particular, and broilers are presumed to display a lower rate of oxygen diffusion from the lungs into red blood cell haemoglobin (Baghbanzadeh and Decuypere, 2008). In addition, a high growth rate implies a faster blood flow through the capillary bed of the lungs, which possibly further impairs oxygenation of blood (Wideman and Kirby, 1995a, 1995b). Thirdly, an increase in metabolic rate not only augments oxygen requirement at tissue level, but also elevates mitochondrial production of reactive oxygen species. Oxidative stress, in turn, causes lipid peroxidation mediated damage to the pulmonary vasculature, which further deteriorates oxygenation and aggravates hypoxaemia (Bottje and Wideman, 1995; Diaz-Cruz et al., 2003; Aksit et al., 2008). In succession, augmented free radical release caused by hypoxic lung injury feeds a vicious cycle which leads to progressive hypoxaemia (Herget et al., 2000). Given these additional impairments, it is not surprising that fast growth (which implies increased oxygen requirement) in broiler strains that are already faced with a relatively undersized cardiopulmonary capacity, may result in hypoxaemia. Besides genetic and management factors supporting fast and profitable growth, other contributing factors in the pathogenesis of pulmonary hypertension induced ascites include environmental, dietary or animal factors that additionally augment the physiological oxygen requirement or decrease oxygen supply. To maintain normal body temperature in conditions of cold stress, for instance, endogenous heat production is upregulated through an increase in metabolic rate and concomitantly both oxygen requirement and
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
3
PULMONARY HYPERTENSION
Fig. 1. Pathogenesis of and preventive measures for broiler ascites syndrome. FA; fatty acids; UFA, unsaturated fatty acids; PUFA, polyunsaturated fatty acids; SFA, saturated fatty acids.
blood flow are elevated (Julian et al., 1989; Lubritz and McPherson, 1994; Julian, 2000). Respiratory disease and poor air quality comprise examples of conditions that additionally may impair blood oxygenation and thus lower oxygen supply (Julian, 2000). Poor air quality is typically attributable to insufficient ventilation, through which dust and gaseous pollutants (such as ammonia and carbon monoxide) build up in the air (Bottje et al., 1998). A well-known dietary ascites inciting condition is salt intoxication. Excess sodium intake in the form of salt from drinking water or feed increases plasma sodium concentrations, especially in young chickens, and this results in volume expansion and increased blood flow. The small pulmonary blood capillaries in the
rigid avian lung cannot dilate sufficiently to accommodate the increased blood flow effectively (Mirsalimi et al., 1992). The resulting pulmonary hypertension is further exacerbated due to increased resistance to blood flow by sodium-induced arteriolar vasoconstriction and reduced erythrocyte deformability (Hakim, 1988). Thus salt-induced volume overload causes right ventricular hypertrophy subsequent to pulmonary hypertension in birds (Julian, 1987). In general, hypertension exciting factors appear to be additive to other conditions that incite ascites (Julian, 1987; Julian et al., 1992) in broilers in contrast to mammals, where excess salt induces left ventricular hypertrophy subsequent to systemic hypertension (Fields et al., 1991).
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
4
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Epidemiology Broiler ascites syndrome used to be primarily observed in birds raised at high altitude, which entails low partial oxygen pressure and thus diminished oxygen supply. However, since 1980, its incidence has steadily increased and, more importantly, it has been reported at lower altitudes and even at sea level (Julian, 1993). In 1997, the world broiler ascites survey revealed an average incidence of ascites in 4.7% of live broilers worldwide (Maxwell and Robertson, 1997). In the UK, the incidence of ascites mortality increased from 0.03% to 0.04% in 1965 to 0.7%, 0.9% and 1.4% in 1991, 1992 and 1993, respectively (Hemsley, 1965; Maxwell and Robertson, 1998). Similarly, in Western Canada, mortality due to ascites increased from 0% to 0.02% in 1975, to 1% to 2% in 1995 (Brigden and Riddell, 1975; Olkowski et al., 1996). These figures clearly indicate that this metabolic disorder had become a major non-infectious cause of loss in the modern broiler industry. Of notice is a high variation in incidence between flocks. For instance, ascites mortality in UK broiler flocks in 1993 ranged between 0% and 10% and in USA broiler flocks in 2002 between 0% and 30% (Maxwell and Robertson, 1998; Pavlidis et al., 2007). To date, broiler breeder companies have developed and implemented strategies to select against ascites susceptibility. Genetic analyses have demonstrated moderate to high heritability estimates (0.11–0.44) for ascites indicator traits. Divergent selection for ascites susceptibility following exposure to ascites-inciting conditions has been shown to be feasible within a few generations and with acceptable losses in productivity (Druyan et al., 2007a, 2007b, 2008; Pavlidis et al., 2007). Nonetheless, the available literature data indicates that ascites susceptibility is still present in modern broiler lines and remains positively associated with growth rate. This is substantiated by an incidence of ascites mortality of 5–10% in modern broilers when fed high-energy pellets ad libitum (Druyan and Cahaner, 2007). Arce-Menocal et al. (2009) reported ascites mortality rates of 10.4% and 12.4% in modern strain A and 3.9% and 7.7% in modern strain B when reared to 42 days of age on a diet based on the 1994 National Research Council recommendations presented as either a mash or as a crumb (which promotes growth), respectively. Moreover, veterinary condemnation records of the Canadian Food Inspection Agency show that although the proportion of broiler carcass condemnations related to ascites peaked at 19% in 1996, in 2011, 8% of such condemnations, representing 0.08% of slaughtered chickens or over half a million birds, were rejected for consumption because of ascites (AAC, 2012). These data do not include ascites mortality at farm level or during transport to the slaughter house. Nevertheless, compared to its peak, broiler ascites syndrome is considerably less common as a result of management practices that reduce growth rate (Druyan and Cahaner, 2007; Hassanzadeh, 2009). Some of those are even legally imposed. New EU welfare regulations, for example, prohibit the use of photoperiods longer than 18 h after the age of 7 days, for which one of the key intentions is exactly aimed at reducing growth rate and consequently ascites mortality and skeletal diseases (EC, 2007).
The most common prevention strategies are feed and lighting regimes that slow down early growth (Ozkan et al., 2010). Limitation of early growth rate can be achieved by qualitative feed restriction, which implies dilution of the energetic density of the ration, or by quantitative feed restriction through offering a diminished quantity of feed each day, periodic feed withdrawal or a lighting schedule with increased dark hours. However, there a several concerns regarding these methods. Firstly, the effectiveness of limiting early growth rate to diminish the incidence of ascites is debatable (reviewed by Madrigal et al. (2002)). Secondly, several trials indicate inadequate compensatory growth in later growth phases, resulting in depressed bodyweight or yield at market age (see, for example, Acar et al., 1995; Lee and Leeson, 2001). Thirdly, Lee and Leeson (2001) pointed out that qualitative feed restriction entails extra costs in the form of non-nutritive fillers and higher transport costs per unit of feed. The authors suggested that quantitative feed restriction is therefore preferable at an industrial scale. Fourthly, feed restriction in broiler lines that were selected for high feed intake may impair welfare as demonstrated both by physiological stress parameters and behavioural criteria indicative of frustration to hunger (Savory and Lariviere, 2000). Quantitative feed restriction through limiting daily amounts of feed does not however seem to diminish broiler welfare more than qualitative feed restriction through lowered energetic density of the diet (Savory et al., 1996; Savory and Lariviere, 2000). Baghbanzadeh and Decuypere (2008) drew attention to adverse secondary effects of imprudent feed restriction on adequate intake of, for example, anti-coccidial products on the control of coccidiosis, or pigmentation precursors on product quality. Optimisation of the diet to ameliorate ascites syndrome has been investigated to a limited extent. The multi-factorial aetiology of the syndrome means that pulmonary hypertension can be responsive to dietary strategies other than limitation of early growth. Such interventions need to have a low economic cost, have minimal effects on performance traits, product quality, and animal health and welfare. A dietary shift in fatty acid profile towards a higher ratio of unsaturated to saturated fatty acids has been shown to improve erythrocyte deformability and so diminish the resistance of blood flow through the lung capillaries (Bond et al., 1996; Walton et al., 1999). Furthermore, as suggested by Bond et al. (1996) and Walton et al. (1999), dietary fat sources with a high proportion of n-3 and n6 polyunsaturated fatty acids (such as flaxseed oil) may additionally slow down the development of broiler ascites syndrome due to the release of endogenous coronary relaxants and attenuated inflammatory compounds derived from cellular membrane lipids. A reduction in reactive oxygen mediated damage to the cardiopulmonary system forms yet another approach that could alleviate the predisposition of fast-growing birds to ascites mortality (Herget et al., 2000). Dietary supplementation with anti-oxidant vitamins can reduce oxidative damage and improve pulmonary vascular performance (see, for example, Lorenzoni and Ruiz-Feria, 2006; Nain et al., 2008; Bautista-Ortega and Ruiz-Feria, 2010). However, substantial beneficial effects on the incidence of broiler ascites syndrome cannot always be demonstrated (Baghbanzadeh and Decuypere, 2008; Nain et al., 2008; Xiang et al., 2002).
Prevention Impact on the broiler industry The effect on productivity is a crucial factor in evaluating ascites abating strategies not only from an economic point of view, but also because the pathogenesis of broiler ascites syndrome is positively interconnected with growth rate. Genetic selection for ascites resistant broiler lines is considered to be the ideal permanent solution to the ascites problem. However, until selection programs successfully develop such broiler lines and these new strains are shown to be satisfactory, alternative preventive measures have to be considered.
Ascites mortality generally occurs late in the production round. In addition, ascitic birds are rejected for consumption (Haslam et al., 2008). Thus affected birds have been fed for the entire rearing cycle, but have no economic value (Druyan and Cahaner, 2007). Even at a low incidence, the economic cost of broiler ascites syndrome is therefore considerable. Moreover, it is a severe welfare problem as the symptoms, such as breathing difficulties, are progressive and distressing (Aksit et al., 2008).
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Conclusions Intense selection of broilers for fast growth and high meat yield has been highly successful, but has resulted in a significant increase in the incidence of broiler ascites syndrome and associated mortality. The central aetiology of this metabolic syndrome is a hypoxaemic condition resulting from an imbalance between oxygen requirement and oxygen supply. Modern broiler lines are highly metabolically active, which facilitates growth but requires a high oxygen supply. This is compounded by the fact that selective breeding for high meat yield led to birds with a disproportionately low heart and lung size, which consequently have a relatively underdeveloped capacity for blood oxygenation. A high metabolic rate implies increased free radical mediated damage to the pulmonary vasculature as well as a faster blood flow through the lungs, which both further diminish oxygenation of blood. The resultant imbalance between oxygen demand and supply incites pulmonary hypertension and subsequently right heart failure followed by transudation of fluid into the abdominal cavity, which is defined as ascites. Selection for ascites resistance and management practices reducing early growth have lowered the overall incidence of ascites compared to its peak years. However, provided allowance of performance at full genetic potential, ascites susceptibility is still present in modern broiler lines. Ideally preventive measures should preserve optimal performance while sustaining product quality and animal welfare. Selective breeding for ascites resistant strains is considered a permanent solution to the problem. However, until resistant strains are successfully developed and implemented on a global scale, alternative measures remain imperative. Optimisation of the diet and rearing conditions, and development of new feed additives that ameliorate the ascites syndrome form such alternative measures. Conflict of interest statement None of the authors of this paper has a financial or personal relationship with other people or organisations that could inappropriately influence or bias the content of the paper. References Agriculture and Agrifood Canada (AAC), 2012. The Veterinary Condemnation Records of the Canadian Food Inspection Agency. www.agr-gc.ca. Acar, N., Sizemore, F.G., Leach, G.R., Wideman, R.F., Owen, R.L., Barbato, G.F., 1995. Growth of broiler-chickens in response to feed restriction regimens to reduce ascites. Poultry Science 74, 833–843. Aksit, M., Altan, O., Karul, A.B., Balkaya, M., Ozdemir, D., 2008. Effects of cold temperature and vitamin E supplementation on oxidative stress, troponin-T level, and other ascites-related traits in broilers. Archiv Fur Geflugelkunde 72, 221–230. Arce-Menocal, J., Evila-Gonzalez, E., Lopez-Coello, C., Garibay-Torres, L., MartinezLemus, L.A., 2009. Bodyweight, feed-particle size, and ascites incidence revisited. Journal of Applied Poultry Research 18, 465–471. Baghbanzadeh, A., Decuypere, E., 2008. Ascites syndrome in broilers: Physiological and nutritional perspectives. Avian Pathology 37, 117–126. Bautista-Ortega, J., Ruiz-Feria, C.A., 2010. L-arginine and antioxidant vitamins E and C improve the cardiovascular performance of broiler chickens grown under chronic hypobaric hypoxia. Poultry Science 89, 2141–2146. Bond, J.M., Julian, R.J., Squires, E.J., 1996. Effect of dietary flax oil and hypobaric hypoxia on right ventricular hypertrophy and ascites in broiler chickens. British Poultry Science 37, 731–741. Bottje, W.G., Wideman, R.F., 1995. Potential role of free radicals in the pathogenesis of pulmonary hypertension syndrome. Poultry and Avian Biology Reviews 6, 211–231. Bottje, W.G., Wang, S., Kelly, F.J., Dunster, C., Williams, A., Mudway, I., 1998. Antioxidant defenses in lung lining fluid of broilers: Impact of poor ventilation conditions. Poultry Science 77, 516–522. Brigden, J.L., Riddell, C., 1975. A survey of mortality in four broiler flocks in Western Canada. Canadian Veterinary Journal 16, 194–200. Cardenas, D.M., Hernandez, A., Osuna, O., 1985. Algunos valores hematimétricos y de proteinas totales en polios Arbor Acres sanos y asciticos en la Sabana de Bogota. Revista Acovez 9, 42–44.
5
Currie, R.J.W., 1999. Ascites in poultry: Recent investigations. Avian Pathology 28, 313–326. Diaz-Cruz, A., Serret, M., Ramirez, G., Avila, E., Guinzberg, R., Pina, E., 2003. Prophylactic action of lipoic acid on oxidative stress and growth performance in broilers at risk of developing ascites syndrome. Avian Pathology 32, 645–653. Druyan, S., Cahaner, A., 2007. Segregation among test-cross progeny suggests that two complementary dominant genes explain the difference between ascitesresistant and ascites-susceptible broiler lines. Poultry Science 86, 2295–2300. Druyan, S., Ben-David, A., Cahaner, A., 2007a. Development of ascites-resistant and ascites-susceptible broiler lines. Poultry Science 86, 811–822. Druyan, S., Shlosberg, A., Cahaner, A., 2007b. Evaluation of growth-rate, bodyweight, heart rate, and blood parameters as potential indicators for selection against susceptibility to the ascites syndrome in broilers. Poultry Science 86, 621–629. Druyan, S., Hadad, Y., Cahaner, A., 2008. Growth rate of ascites-resistant versus ascites-susceptible broilers in commercial and experimental lines. Poultry Science 87, 904–911. European Council (EC), 2007. Council Directive 2007/43/EC: Minimum rules for the protection of chickens kept for meat production. Official Journal of the European Union 182, 19–28. Emmerson, D.A., 1997. Commercial approaches to genetic selection for growth and feed conversion in domestic poultry. Poultry Science 76, 1121–1125. Fields, N.G., Yuan, B.X., Leenen, F.H., 1991. Sodium induced cardiac hypertrophy. Circulation Research 68, 745–755. Hakim, T.S., 1988. Erythrocyte deformability and segmental pulmonary vascular resistance: Osmolarity and heat treatment. Journal of Applied Physiology 65, 1634–1641. Haslam, S.M., Knowles, T.G., Brown, S.N., Wilkins, L.J., Kestin, S.C., Warriss, P.D., Nicol, C.J., 2008. Prevalence and factors associated with it, of birds dead on arrival at the slaughterhouse and other rejection conditions in broiler chickens. British Poultry Science 49, 685–696. Hassanzadeh, M., 2009. New approach for the incidence of ascites syndrome in broiler chickens and management control of the metabolic disorders. International Journal of Poultry Science 8, 90–98. Hassanzadeh, M., Buyse, J., Decuypere, E., 2008. Further evidence for the involvement of anatomical parameters of cardiopulmonary system in the development of ascites syndrome in broiler chickens. Acta Veterinaria Hungarica 71, 71–80. Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003a. Carcass composition and yield of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 1509–1518. Havenstein, G.B., Ferket, P.R., Qureshi, M.A., 2003b. Growth, liveability, and feed conversion of 1957 versus 2001 broilers when fed representative 1957 and 2001 broiler diets. Poultry Science 82, 1500–1508. Hemsley, L.A., 1965. Causes of mortality in fourteen flocks of broiler chickens. Veterinary Record 77, 467–472. Herget, J., Wilhelm, J., Novotna, J., Eckhardt, A., Vytasek, R., Mrazkova, L., Ostadal, M., 2000. A possible role of the oxidant tissue injury in the development of hypoxic pulmonary hypertension. Physiological Research 49, 493–501. Julian, R.J., 1987. The effect of increased sodium in the drinking-water on right ventricular hypertrophy, right ventricular failure and ascites in broilerchickens. Avian Pathology 16, 61–71. Julian, R.J., 1993. Ascites in poultry. Avian Pathology 22, 419–454. Julian, R.J., 1998. Rapid growth problems: Ascites and skeletal deformities in broilers. Poultry Science 77, 1773–1780. Julian, R.J., 2000. Physiological, management and environmental triggers of the ascites syndrome: A review. Avian Pathology 29, 519–527. Julian, R.J., Mcmillan, I., Quinton, M., 1989. The effect of cold and dietary energy on right ventricular hypertrophy, right ventricular failure and ascites in meat-type chickens. Avian Pathology 18, 675–684. Julian, R.J., Caston, L.J., Leeson, S., 1992. The effect of dietary-sodium on right ventricular failure-induced ascites, gain and fat deposition in meat-type chickens. Canadian Journal of Veterinary Research 56, 214–219. Lee, K.H., Leeson, S., 2001. Performance of broilers fed limited quantities of feed or nutrients during seven to fourteen days of age. Poultry Science 80, 446–454. Lorenzoni, A.G., Ruiz-Feria, C.A., 2006. Effects of vitamin E and L-arginine on cardiopulmonary function and ascites parameters in broiler chickens reared under subnormal temperatures. Poultry Science 85, 2241–2250. Lubritz, D.L., McPherson, B.N., 1994. Effect of genotype and cold stress on incidence of ascites in cockerels. Journal of Applied Poultry Research 3, 171–178. Madrigal, S.E., Watkins, S.E., Anthony, N.B., Wall, C.E., Fritts, C.A., Waldroup, P.W., 2002. Effect of dietary modifications designed to reduce early growth rate on live performance and on incidence and severity of ascites in two commercial broiler strains when maintained under low ventilation or low temperature models. International Journal of Poultry Science 1, 150–157. Maxwell, M.H., Robertson, G.W., 1997. World broiler ascites survey. Poultry International 36, 16–30. Maxwell, M.H., Robertson, G.W., 1998. UK survey of broiler ascites and sudden death syndromes in 1993. British Poultry Science 39, 203–215. Mirsalimi, S.M., O’Brien, P.J., Julian, R.J., 1992. Blood volume increase in salt-induced pulmonary hypertension, heart failure and ascites in broiler and white leghorn chickens. Canadian Journal of Veterinary Research 57, 110–113. Nain, S., Wojnarowicz, C., Laarveld, B., Olkowski, A.A., 2008. Effects of dietary vitamin E and C supplementation on heart failure in fast growing commercial broiler chickens. British Poultry Science 49, 697–704. Nijdam, E., Zailan, A.R.M., van Eck, J.H.H., Decuypere, E., Stegeman, J.A., 2006. Pathological features in dead on arrival broilers with special reference to heart disorders. Poultry Science 85, 1303–1308.
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011
6
I.D. Kalmar et al. / The Veterinary Journal xxx (2013) xxx–xxx
Olkowski, A.A., Kumor, L., Classen, H.L., 1996. Changing epidemiology of ascites in broiler chickens. Canadian Journal of Animal Science 76, 135–140. Ozkan, S., Takma, C., Yahav, S., Sogut, B., Turkmut, L., Erturun, H., Cahaner, A., 2010. The effects of feed restriction and ambient temperature on growth and ascites mortality of broilers reared at high altitude. Poultry Science 89, 974–985. Pavlidis, H.O., Balog, J.M., Stamps, L.K., Hughes, J.D., Huff, W.E., Anthony, N.B., 2007. Divergent selection for ascites incidence in chickens. Poultry Science 86, 2517– 2529. Rauw, W.M., Kanis, E., Noordhuizen-Stassen, E.N., Grommers, F.J., 1998. Undesirable side effects of selection for high production efficiency in farm animals: A review. Livestock Production Science 56, 15–33. Rehman, H., Khan, A., Khan, M.Z., 1999. Clinical, gross and histopathological observations in spontaneous cases of ascites syndrome in broiler chickens reared at low altitude. Pakistan Veterinary Journal 19, 115–118. Savory, C.J., Lariviere, J.M., 2000. Effects of qualitative and quantitative food restriction treatments on feeding motivational state and general activity level of growing broiler breeders. Applied Animal Behaviour Science 69, 135–147. Savory, C.J., Hocking, P.M., Mann, J.S., Maxwell, M.H., 1996. Is broiler breeder welfare improved by using qualitative rather than quantitative food restriction to limit growth rate? Animal Welfare 5, 105–127.
van As, P., Elferink, M.G., Closter, A.M., Vereijken, A., Bovenhuis, H., Crooijmans, R.P.M.A., 2010. The use of blood gas parameters to predict ascites susceptibility in juvenile broilers. Poultry Science 89, 1684–1691. Walton, J.P., Bond, J.M., Julian, R.J., Squires, E.J., 1999. Effect of dietary flax oil and hypobaric hypoxia on pulmonary hypertension and haematological variables in broiler chickens. British Poultry Science 40, 385–391. Wheeler, M.B., Campion, D.R., 1993. Animal production – A longstanding biotechnological success. American Journal of Clinical Nutrition 58, S276–S281. Wideman, R.F., Kirby, Y.K., 1995a. A pulmonary-artery clamp model for inducing pulmonary-hypertension syndrome (ascites) in broilers. Poultry Science 74, 805–812. Wideman, R.F., Kirby, Y.K., 1995b. Evidence of a ventilation–perfusion mismatch during acute unilateral pulmonary-artery occlusion in broilers. Poultry Science 74, 1209–1217. Xiang, R.P., Sun, W.D., Wang, J.Y., Wang, X.L., 2002. Effect of vitamin c on pulmonary hypertension and muscularisation of pulmonary arterioles in broilers. British Poultry Science 43, 705–712. Zhou, D.H., Wu, J., Yang, S.J., Cheng, D.C., Guo, D.Z., 2008. Intravenous endothelin-1 triggers pulmonary hypertension syndrome (ascites) in broilers. Veterinarni Medicina 53, 381–391.
Please cite this article in press as: Kalmar, I.D., et al. Broiler ascites syndrome: Collateral damage from efficient feed to meat conversion. The Veterinary Journal (2013), http://dx.doi.org/10.1016/j.tvjl.2013.03.011