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Metabolic Disorders: Limitations to Growth of and Mineral Deposition into the Broiler Skeleton after Hatch and Potential Implications for Leg Problems

Department of Animal and Avian Sciences, University of Maryland, College Park 20742

Correspondence: ¹ Corresponding author: rangel{at}umd.edu

	SUMMARY

TOP SUMMARY DESCRIPTION OF PROBLEM SKELETAL GROWTH AND MINERAL... ECONOMIC LOSSES DUE TO... CONCLUSIONS AND APPLICATIONS REFERENCES AND NOTES

 
Metabolic diseases are associated with a rapid early growth rate in poultry, especially in broilers, and their incidence can be decreased by slowing early growth. Leg problems seen in the absence of infectious agents are often the result of fast early growth and thus can be related to metabolic diseases. At hatch, the broiler skeleton is poorly mineralized; growth and mineralization occur most rapidly in the first 2 wk of life. Except for Ca, the embryo has limited access to minerals. Most minerals in the egg cannot be influenced by maternal diet, but embryo mineral uptake can be improved by dietary mineral source selection. The use of management tools to reduce metabolic diseases that rely primarily on decreasing feed consumption, without increasing prestarter mineral density, may have negative unintended consequences on skeletal development. Incidence of losses due to leg problems during growout and processing have decreased since the early 1990s, in part due to breeding programs, but not enough information is available to estimate the proportion of losses related to metabolic diseases. This information is needed if improvements are to be made.

Key Words: skeletal development • neonatal • egg nutrient • bone nutrient

	DESCRIPTION OF PROBLEM

TOP SUMMARY DESCRIPTION OF PROBLEM SKELETAL GROWTH AND MINERAL... ECONOMIC LOSSES DUE TO... CONCLUSIONS AND APPLICATIONS REFERENCES AND NOTES

 
Metabolic problems have been a fact of life in poultry productions for at least the last few decades, exacerbated by the fast pace of improvements in the genetic potential of poultry for growth and efficiency. The genetic potential for growth and feed efficiency has been greatly improved in the last 50 yr [1, 2]. The 42-d weight of a broiler from a 1991 commercial strain fed a 1991 diet was 2,297 g, compared with a weight of 680 g for a 1957 commercial strain broiler fed the same 1991 diet [1]. Similarly, the 42-d weight of a 1991 strain broiler fed a 1957 diet was 3.4 times the weight of 1957 strain broiler fed a 1957 diet (1,877 vs 538 g) [1]. Clearly, genetic changes account for the greatest proportion of the improvement in growth. In 2003, similar differences were reported between 1957 and 2001 male broiler strains [2], in which the 1957 strain weighed 591 g at 42 d compared to 2,903 g for the 2001 strain fed a representative diet for their respective year. The effect of genetic improvements related with growth can clearly be seen when male broilers of the 1957 strain were fed the same 2001 commercial diet as the 2001 broiler strain. At 42 d of age, the 2001 male broilers weighed 4.5 times more than the 1957 male broilers (2,903 and 641 g, respectively) [2].

Efficiency of feed conversion was also primarily affected by genetic changes. Male broilers fed the same commercial 2001 diet converted feed to gain at a rate of 1.58 in the 2001 strain and 2.05 in the 1957 strain [2]. Not only has the ability to grow rapidly (4.5 times more rapidly) and to convert feed more efficiently been improved, but the proportion of saleable product (carcass yield) and of the different muscles in the carcass has been changed [2, 3]. Carcass yield for male broilers fed the same 2001 commercial diet was 72.3% in the 2001 strain, whereas it was 61.5% in the 1957 strain. More importantly, the proportion of breast in relation to BW was 1.7 times greater in the 2001 vs the 1957 strains fed the same diet (19.5 and 11.3%, respectively) [3].

Given the large, rapid improvement in the genetic potential for growth and feed efficiency, as well as the change in muscle mass, it is not surprising that metabolic problems have been exacerbated. Metabolic problems in poultry production cause morbidity, mortality, or both, but are not related to infectious diseases and appear to be due to disorders in metabolic processes. Because these disorders tend to affect poultry that have the greatest productivity, they can be ameliorated by implementing changes in diet, management, or both, that decrease production rates (e.g., growth and egg production). Metabolic disorders have been covered in depth previously [4, 5, 6, 7, 8]. Numerous metabolic disorders have been identified, and their close association with productivity has been proven [4, 5, 6, 9]. The metabolic disorders of greatest economic importance, at least in broiler production, are skeletal disorders, ascites, and sudden death syndrome. Ascites and sudden death syndrome are both metabolic diseases associated with insufficiencies of the cardiovascular system [4, 5, 7, 9]. These disorders will not be addressed in this paper.

The focus of this paper will be on the metabolic disorders of the skeletal system. Issues related to the negative effect of how we have addressed limiting metabolic diseases (reduce growth rate) will be addressed in the context of macro- and micromineral availability of the embryo, the physical growth of the skeleton early after hatch, and its quantitative deposition of macro- and microminerals and how this relates to feed nutrient concentrations and availabilities. Implications of early access to minerals and correct structural growth of the skeletal system in the neonatal broilers on leg problems and their costs in latter growth phases will also be addressed.

Description of Skeletal Disorders
There are numerous skeletal disorders that have been described and assigned generalized causes [4, 5, 7]. Skeletal problems can be as follows: related to nutritional deficiencies; infections of the bone, joints, or both; intestinal diseases that lead to malabsorption; mechanically-or trauma-induced; related to gender; have a genetic component; associated with fast growth rates; and composed of interactions among the above factors [4, 7, 8, 10]. The most prevalent skeletal problems in broilers have been identified as tibial dyschondroplasia (TD), chronic painful lameness in older broilers or roasters, chondrodystrophy or angular bone deformities, valgusvarus deformities (commonly known as twisted leg), spondylolisthesis or kinky back, rickets, femoral head necrosis, curled toes, and ruptured gastrocnemious tendon. Clinical signs and potential causes of these skeletal problems, as well as methods to decrease or eliminate them, have been extensively described [4, 5, 7]. There can be numerous causes for each of the mentioned skeletal problems. Lameness, for example, can be related to deformity, trauma, infection, severe TD, or to no specific gross or histological cause [5]. During the last couple of weeks in the broiler production cycle, healthy birds spend most of their time sitting down (73 to 76%) [11, 12] even though they are not considered lame. Of importance when defining skeletal abnormalities related to metabolic disease is not what the specific skeletal problem is per se, but identification of underlying causes.

Defining Skeletal Abnormalities as They Relate to Metabolic Disease
The hypothesis behind the definition of skeletal abnormalities related to metabolic disease is that the early rapid growth of the genetic broiler strains of today leads to skeletal abnormalities exhibited primarily, but not always, after the bird reaches BW greater than 1 kg. Of the diseases mentioned previously, most can result from metabolic disease.

Chronic lameness can be described as impaired walking ability, difficulty standing, hobbled movement when walking, frequent and prolonged squatting, and it is most often seen in heavier birds [5, 13]. The lameness observed in the absence of either gross or histological causes (deformity, trauma, infection) can be reduced by management programs that slow growth rates in the first 2 wk of life [5]. Lameness, therefore, can be caused by metabolic disease associated with rapid growth early in life.

Twisted legs or angular bone deformity is possibly the most common skeletal problem among broilers that does not appear to be associated with a nutritional deficiency [5]. Of the skeletal abnormalities, angular bone deformities seem to be the most clearly associated with rapid growth and appear to be related to limitations in time for remodeling of bone during growth and proper bone alignment. Researchers have shown the poor ability of fast-growing broiler strains to respond to mechanical load bearing or insensitivity to load, which would suggest that they are unable to adapt the skeletal system as rapidly as BW increases [14]. This phenomenon may be related to the incidence of twisted legs in broilers. Reducing growth during the first and second weeks of life, as well as increasing dark periods, seems to reduce the incidence of angular bone deformities [5]. Specifically, the use of light-dark cycles with prolonged dark periods has been shown to increase the overall activity of chicks [15, 16], reduce gait problems [16], and reduce the incidence of angular bone deformities [5].

Rickets is most often associated with a nutritional deficiency or imbalance. These imbalances or deficiencies may occur due to mixing errors; inaccurate ingredient nutrient estimates; variable content of Ca, P, or both, when formulating diets; and vitamin deficiencies due to loss, primarily of vitamin D activity in vitamin premixes. Deficiencies may also occur as a result of transient or chronic intestinal disease that impairs absorption (malabsorption syndrome, coccidiosis, etc.). Because it relates to metabolic disease, the incidence of rickets is not as frequent as for other skeletal problems but can result from management changes that reduce feed consumption as a means to reduce growth, with no adjustment in the concentrations of nutrients that are required for skeletal development.

Tibial dyschondroplasia has been studied extensively. It has been related closely to vitamin D status of the bird [16]: The addition of vitamin D₃ alleviates the clinical signs of this disease primarily by inducing maturation of chondrocytes [17]. The concentration and ratio of Ca and P in the diet have also been implicated in affecting chondrocyte differentiation [18] and thus in the incidence and severity of TD. The influence of P may be related, in part, to its contribution to acid-base balance. Electrolyte imbalances have been related to the incidence of TD. It may be chloride in particular that exerts the most influence, and it may have an independent effect on TD [4]. It has been reported that rapid growth may cause metabolic acidosis, which in turn contributes to the incidence of TD [5]. Tibial dyschondroplasia appears to be most prevalent in rapidly growing birds [4, 5, 7], and this may be related to transient deficiencies during the rapid growth phase of long bones, specifically the tibia, because the proximal tibia is the site of the fastest-growing growth plate. Ultimately, the approaches that are used to decrease metabolic disease, such as lighting programs that limit feed consumption and thus growth, may lead to transient deficiencies unless applied correctly.

Spondylolisthesis, or kinky back, is a lesion seen frequently in broilers and is associated with rapid growth, but it occurs most frequently in females [7]. The most likely cause is poor ligament strength, a weak ligament attachment associated with the heavy weight of the breast, or both. The incidence of this disease is low and is highly influenced by genetics, but with no known nutritional deficiency associated with it [4].

It is important from a field standpoint to separate the term "leg problems" or "skeletal abnormalities" into specific types and potential causes if any progress is to be made in decreasing the losses due to problems related to the skeleton. Usually, when mortality causes are identified in the field, all losses caused by skeletal abnormalities are pooled together, whether they are related to field losses or processing losses. This practice limits our ability to determine the economic loss associated with skeletal abnormalities that are related to metabolic disease, which in turn makes it difficult to implement management strategies to decrease their incidence.

	SKELETAL GROWTH AND MINERAL AVAILABILITY

TOP SUMMARY DESCRIPTION OF PROBLEM SKELETAL GROWTH AND MINERAL... ECONOMIC LOSSES DUE TO... CONCLUSIONS AND APPLICATIONS REFERENCES AND NOTES

 
The fastest growth of the skeletal system, both in terms of bone length and width and mineral deposition, occurs in the first 2 wk of life. At hatch, mineralization of the skeleton is poor at best. This means that a high proportion of the consumed and available minerals during the first few days after hatch are needed for bone mineralization and growth. Yet feed consumption during that period is low and highly variable among birds. This presents a challenge for delivery of critical nutrients for skeletal growth, especially when the situation is compounded by management programs to reduce metabolic challenges. These strategies often involve lighting programs that reduce feed consumption and thus growth, but minimal or no changes in diet nutrient concentration are made.

Embryo Mineral Content
There are excellent articles that review mineral metabolism in avian embryos, discuss mineral stores in the egg, the location of these stores, amounts present, and how they are mobilized and utilized by the embryo [19, 20]. There has been little research in recent years on the effect of maternal nutrition on egg mineral stores. Most of the minerals in the egg are in the yolk, and a few of them can be heavily influenced by their concentration in the maternal diet (Table 1) [19, 21, 22, 23, 24, 25]. In recent years, work has focused not so much on the effect of maternal nutrition on the concentration of egg minerals but on the chemical form of the mineral and its ease of mobilization and use by the embryo [19, 20, 24, 26].

In the case of Ca and to some extent Mg, the eggshell provides a large store. It is estimated that 70 to 90% of the Ca and 20 to 30% of the Mg used by the embryo comes from the shell [19, 27]. Phosphorus stores are more problematic given that the shell contains minimal P, and thus the P available for all functions, including bone mineralization, is found primarily in the yolk. Of importance is that some of that P is retained in the residual yolk at hatch and conceptually serves, at least in part, an important developmental function for phospholipid synthesis. Thus, a large proportion of that residual P is not available for bone growth and mineralization. As incubation proceeds, concentrations of P and Mg decrease in the yolk, whereas Ca concentrations in the yolk increase as mobilized eggshell Ca is stored [19].

The chick at hatch contains 117.08 mg of total P (1.81 mg/100 mg of DM), of which 59% is inorganic P, 11% is lipid-associated P, 18% is protein-associated P, and 3% is associated with phosphagen and sphingomyelin [28]. Hatchling mineral content is as follows: Ca, 129.31 mg (2 mg/100 mg of DM); Mg, 0.83 mg (0.015 mg/100 mg of DM); K, 38.37 mg (0.59 mg/100 mg of DM); Na, 41.38 mg (0.64 mg/ 100 mg of DM); Mn, 9.0 µg (0.14 µg/100 mg of DM); Cu, 48.4 µg (0.75 µg/100 mg of DM); Fe, 1.51 µg (0.02 µg/100 mg of DM); and ash, 508.9 mg (7.86 mg/100 mg of DM) [28]. The whole skeleton at hatch contains 362.8 mg of total ash (32.41 mg/100 mg of DM), 98 mg of Ca (8.75 mg/100 mg of DM), and 71.5 mg of total P (6.36 mg/100 mg of DM), of which 65% is inorganic P and 2.9% is lipid-associated P [28]. Thus, the skeletal system accounts for 71% of the ash in the embryo, 76% of the Ca, and 61% of the total P.

Skeletal Growth for the First Two Weeks After Hatch
Several studies have reported the physical size (weight, length, width) and ash Ca and P content of specific components of the broiler skeleton at different ages [10, 29, 30, 31]. None of the information available provides an insight into the changes that occur specifically in the first 1 to 2 wk of life or how the absolute macro-and micromineral amounts present in part or all of the skeleton change from hatch to 14 d of age. Information about this process would allow us to determine the amounts of minerals deposited in the skeleton during the neonatal phase and thus what needs to be delivered to the chick. Correlating deposition information with feed consumption data, nutrient concentrations, and nutrient availabilities may allow us to better formulate broiler neonatal feeds, especially when feed restriction is used as a way to decrease growth and the incidence of metabolic diseases. The effect of other minerals such as Cu and Zn on bone development and bone strength has been illustrated [26, 32]. No data were found in the literature on the absolute micromineral contents of any poultry skeletal components during the first 14 d following hatch.

A study was done in which 10 Ross 308 broilers (5 per sex) were sampled at random from a pen of 200 broilers at hatch and 2, 4, 6, 10, and 14 d of age [33]. Broilers were sexed at the hatchery and females marked on arrival. This was part of a larger, long-term experiment lasting to 85 d of age, but given the focus of this paper, only data from the first 14 d will be presented here. Broilers were raised on pine shavings in a floor pen facility that simulated commercial practices. The following lighting program was used: 24 h of light from hatch to 4 d of age, followed by 10 h of dark from 5 to 10 d of age, and then 8 h of dark from 11 to 14 d of age. This is a lighting program used commercially to reduce early growth as a means to decrease the incidence of metabolic diseases. Room temperature was maintained at 30°C for wk 1 and then dropped to 28°C during wk 2; brooder lamps were left on for the first 10 d of life. Corn and soybean meal diets, formulated to exceed broiler requirements [34] (Table 2), and water were available for ad libitum consumption. All guidelines of the University of Maryland Animal Care and Use Committee were followed.

All bones were fat-extracted with petroleum ether, dried at 100°C for 24 h, weighed, then ashed in a muffle furnace at 550°C for 24 h and reweighed, enabling the calculation of total mineral content (ash) as milligrams per gram of the dry, fat-free sample. Samples from the tibia, humerus, and pelvis of 3 males and 3 females (selected randomly) from each age group were resuspended in 6 M HCl, diluted to enable the measurement of total P by colorimetric means [35] and Ca by atomic absorption spectrophotometry, and reported as a proportion of ash (mg/ g). All bones, including the neck, were pooled from 2 birds per sex per age group for analyses of macrominerals (K, Mg, Na) and microminerals (Fe, Mn, Zn, Cu, Se) by inductively coupled plasma source mass spectrometry.

Feed consumption data are presented as arithmetic means with no associated error, because all birds were housed and fed together. This will be an average value that is presented mainly to provide an idea of feed consumption in these birds and average consumption of the different minerals. When using the feed consumption averages and any values derived from it (mineral consumption concentrations), care must be taken, because it is only an arithmetic average and feed consumption will vary greatly among individual broilers, especially early in life. For skeletal data, the experimental unit was the individual bird. Pair-wise mean comparisons were performed using Tukey’s method [36] when the model was significant (P < 0.05). All analyses were performed using SAS Version 8.2 [37].

Body weight increases in a quadratic manner for the first 14 d of age (Table 3). Similarly, growth of the skeleton, both on a wet and a dry defatted basis, and weight of ash follow a quadratic pattern. During the first 2 d after hatch, there is no significant change in the wet or dry defatted weight of the skeleton or in ash weight and ash percentage (Table 3). Overall, the skeleton is poorly mineralized at hatch (19.87% ash), and despite rapid mineralization to 10 d, whole skeletal ash content was only 27.74%, compared to 38% at 85 d [33]. Others have reported tibia dry defatted ash values of 27.44, 36.52, and 39.30% at 1, 7, and 14 d of age in male broilers [31]. This suggests that the tibia is one of the more mineralized bones in the skeleton, at least early in the life of the broiler. Yet it has been reported repeatedly that tibia mineralization is a good indicator of overall skeletal mineralization [38, 39]. Tibia length in broilers was 1.8 times greater at 15 d of age compared to hatch and only 2 times longer at 43 d of age compared to the length at 15 d of age, showing that length increases proportionately faster in the first 15 d of life [29]. Similar trends have been reported for tibia width [29, 31] and femur length and width [29]. Specific mineral deposition to the skeleton (Tables 4 and 5) during the first 2 wk of life in the broiler follows a quadratic pattern, as observed with growth of the body, skeletal weight, and skeletal ash increases. No significant change occurred in specific mineral deposition during the first 4 d of life, followed by a subsequent rapid increase from 4 to 14 d (Tables 4 and 5).

If one considers some of the mineral retention values, especially those at the lower end, in the context of the data presented in Tables 4 and 5, it is clear that any yolk and liver stores of minerals are being used quickly in the first 2 d of life. For example, if one assumes an apparent Ca retention of 25.7% [43], apparent P and Cu retentions of 52.6 and 39.8% [42], and apparent Mn and Zn retentions of 14.1 and 14.1%, then apparent retention of the minerals consumed was, on average, 31.8, 46.8, 0.1, 0.2, and 0.3 mg of Ca, P, Cu, Mn, and Zn, respectively. Skeletal deposition during these first 2 d of life was 28.2 and 16.2 mg of Ca and P and 3.1, 68.8, and 1.5 µg of Cu, Zn, and Mn, respectively. It appears that a large proportion of the retained minerals could be used for bone growth and mineralization, with considrable variation in proportions deposited among minerals.

As nutritionists formulating diets that will be used in programs designed to limit feed consumption early in the life of the broilers as a means to reduce growth and thus incidence of metabolic diseases, we need to ask, "Should we increase dietary mineral concentration of those diets?" In most cases, starter diets are not modified when feed consumption limits are implemented in the young chick. The focus of these limited consumption programs is to reduce growth, but they should not curtail growth of all body components by creating borderline mineral deficiencies. It appears that, under normal growth conditions, skeletal growth does not keep up with BW gain. Curtailing growth based on changes in energy to protein ratios should be explored more fully. Also increasing mineral concentrations, use of highly available sources of minerals in prestarter diets, or both, could allow for optimal skeletal growth without risking mineral deficiencies at a time when requirements are high.

	ECONOMIC LOSSES DUE TO SKELETAL ABNORMALITIES RESULTING FROM METABOLIC DISEASE

TOP SUMMARY DESCRIPTION OF PROBLEM SKELETAL GROWTH AND MINERAL... ECONOMIC LOSSES DUE TO... CONCLUSIONS AND APPLICATIONS REFERENCES AND NOTES

 
There is very sparse information published that addresses issues of costs associated with losses due to skeletal problems, much less on costs of the portion of those losses that can be attributed to metabolic disease. Work published in 1994 estimated that leg problems cost the US broiler industry from $80 to $120 million, but little if any partitioning of costs due to cause of the leg problem was done [44]. A survey conducted by Morris [45] in 1993, in which approximately 55% of the poultry industry was represented in the responses, estimated that 1.1% of the live production mortality was due to leg problems and that 2.1% of the birds reaching processing were either downgraded or condemned because of leg or bone disorders. This survey ranked in the following order the causes of the losses due to leg problems: nutrition, followed by infectious causes, TD, toxins, and conformational problems. Since the 1990s, it appears that breeding companies have included skeletal soundness in their multiple trait selection approach, because decreases in the incidence and severity of leg problems have been reported [46, 47]. One of the goals of broiler breeders is to reduce overall mortality and reduce susceptibility to leg problems and cardiovascular disorders [47]. A British survey by Flock et al. [47] showed a decrease in the prevalence of leg defects (gait alterations) from 3 to 1.9% incidence from 1994 to 2000. It is evident that there is no recent detailed information source that documents the incidence of leg problems and that tries to categorize them by cause and type. Without this information, it is impossible to calculate economic losses related to leg problems of metabolic disease origin. More importantly, without a clearer understanding of the causes for the losses, change cannot be implemented to ameliorate the costs associated with metabolic disease in broiler production.

	CONCLUSIONS AND APPLICATIONS

TOP SUMMARY DESCRIPTION OF PROBLEM SKELETAL GROWTH AND MINERAL... ECONOMIC LOSSES DUE TO... CONCLUSIONS AND APPLICATIONS REFERENCES AND NOTES

 

1. Metabolic diseases are caused by rapid early growth rate in broilers, and their incidence can be decreased by slowing early broiler growth.
   
2. Leg problems observed in the absence of infectious agents are usually a result of rapid early growth.
   
3. The embryo has limited access to minerals, except Ca. Most are contained in the yolk, and their concentration in general cannot be greatly influenced by maternal diet. Access, however, can be improved by dietary mineral source selection.
   
4. At hatch, the broiler skeleton is poorly mineralized; growth and mineralization occurs most rapidly in the first 2 wk of life.
   
5. Use of management methods to reduce metabolic diseases that rely primarily on decreasing feed consumption, without increasing mineral concentration in the prestarter phase (hatch to 8 or 14 d), may have negative unintended consequences on the sound development of the skeletal system.
   
6. The incidence of actual losses due to leg problems, during growout and at processing, have decreased since the early 1990s, possibly due to breeding focus that includes decreasing metabolic diseases.
   
7. Economic losses that can be attributed to metabolic disease are unknown currently. This lack of information makes general metabolic disease or any of the specific metabolic disorders less likely to be candidates to be decreased in future breeding or management programs.
   

	REFERENCES AND NOTES

TOP SUMMARY DESCRIPTION OF PROBLEM SKELETAL GROWTH AND MINERAL... ECONOMIC LOSSES DUE TO... CONCLUSIONS AND APPLICATIONS REFERENCES AND NOTES

 

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