Why are young broiler chickens fatter than layer-strain chicks?

Camp. Biochem.

Physiol.

Vol. lOOA,No. I, pp. 205-210, 1991

0300-9629/9153.00+ 0.00 0 1991Pergamon Press plc

Printed in Great Britain

WHY ARE YOUNG BROILER CHICKENS FATTER LAYER-STRAIN CHICKS?

THAN

H. D. GRIFFIN,* D. WINDSOR and C. GODDARD Department of Cellular and Molecular Biology, AFRC Institute of Animal Physiology and Genetics Research, Edinburgh Research Station, Roslin, Midlothian, EH25 9PS, U.K. Telephone: 031440 2726, Fax: 03 I-440-0434 (Received 3 January 1991) Abstract-l.

The abdominal fat pads of 5 week-old broiler and layer chicks incorporated 6.0 and 3.9% of intravenously-injected 14C-labelled very low density lipoproteins respectively. 2. These proportions of total plasma lipoprotein flux were sufficient to account for about 65-70% of the rate of fat deposition in broilers, but were more than 4-fold greater than that the rate of fat deposition in layers. 3. [i4C]Palmitate taken up into adipose tissue of layer chicks had a t,,2 of 2-3 days. 4. There was no significant turnover of adipose tissue triglycerides in broilers and this appears to be a major reason for their relative fatness.

INTRODUCTION

fat in broilers was due to the very high LPL activity

Excessive fatness is a problem in modern strains of rapidly growing broiler chicken that are reared for meat production. Broiler carcasses at commercial killing ages in the U.K. typically contain 130-160 g of ether-extractable fat/kg and higher levels are often reported from the U.S. In contrast, chicks of similar ages from strains selected for egg laying performance contain less than half that proportion of fat. Differences in the abdominal fat pad of broilers and layers are even greater (Griffin et al., 1987). The reason for the deposition of such relatively large amounts of fat in broiler strains is not clear. The intense selection of broilers for rapid growth for 30 or more generations is often suspected to have played a part, although the evidence that an increase in fatness is an inevitable consequence of selection for growth is not conclusive (see McCarthy and Seigel, 1983). The feeding of diets with high energy: protein ratios and better regulation of poultry house environment may encourage fattening in broilers, but cannot explain the very large difference in body composition between broiler and layer strains. Avian adipose tissue has a very limited capacity for fatty acid synthesis and most of the fat accumulating in growing birds is derived from the diet or synthesized in the liver (Griffin and Hermier, 1988). Dietary fat is transported from the avian intestine as portomicrons and non-esterified fatty acids, whereas fatty acids that are synthesized in the liver are transported to other tissues in the form of very low density lipoproteins (VLDL). The portomicrons and VLDL are hydrolysed in the peripheral circulation by lipoprotein lipase (LPL) and the fatty acids released are taken up into the surrounding tissues to be oxidised or re-esterified. Previous comparisons of broiler- and layer-strain chicks suggested that the large amount of abdominal

in the depot. This in turn appeared to be due to both a greater number of adipocytesjfat pad and to a greater LPL activity/fat cell (Griffin ef al., 1987). A greater ability of the abdominal fat pad of broilers to hydrolyse circulating triglyceride-rich lipoproteins can only increase fat deposition if it is accompanied by an increased supply of lipoproteins and/or a decrease in the uptake of lipoprotein triglyceride by muscle and other tissues. The aim of the present investigations was to define the role of plasma lipoprotein metabolism in determining the body composition of young broiler and layer chicks. Our studies led to some unexpected results.

*Please address all correspondence to: Dr H. D. Griffin.

MATERIALS AND METHODS Materials

[r4C]Palmitic acid was bought from Amersham International, Amersham, England, and used at the specific activity supplied (2 MBct/~mole). Heparin (172 units/mg, from porcine intestinal mucosa) ias bought from the Sigma Chemical Co. and Nonidet-P40 from BDH Ltd.. both of Poole, England. Chicks, diets and husbandry conditions

Female day old chicks of commercial strains were obtained from local hatcheries. The layer strain chicks were ISA Browns from ISA Poultry Services, Peterborough, England, and broiler chicks were from D. B. Marshall, Newbridge, Scotland. Birds were initially reared in brooder cages on conventional starter diets appropriate for each strain. They were transferred at about 24 days of age to smaller cages and a 23 hr light: I hr dark photoperiod. Comparisons between lines were made at about 5 weeks of age, and feed and water were available ad lib. Measurement of rates of lipoprotein secretion

The rate of secretion of triglyceride rich-lipoproteins (TGR-lipoproteins) into the circulation was determined by measuring the rate of accumulation of triglyceride in the plasma after intravenous injection of sufficient anti-LPL 205

H. D. GRIFFIN et al.

206

antiserum to block lipoprotein clearance. Details of the experimental protocol used are described by Griffin et al. (1989). Plasma triglyceride concentrations were measured using a commercial kit (Sigma) and converted to mg TG by assuming an average molecular weight of TG of 860. Plasma volume was calculated from the dilution of Evans blue dye (in 0.154 M NaCl) 3 min after its injection into the wing vein. Both broilers and layers reared on a 23 hr light: 1 hr dark photoperiod eat continually (Savory, 1980) and measurements of rate of TGR-lipoprotein secretion were assumed to be representative of the rate of secretion throughout the day. Merabolic fare of radioacriviry labelled VLDL

Biologically-labelled VLDL were prepared by intravenous injection of a 6 week old broiler chicken with 7.4MBq of [“Clpalmitic acid and subsequent recovery of labelled VLDL from the plasma, as described by Griffin et af. (1989). Labelled VLDL were used within 6 hr of isolation. Individual birds were injected via the wing vein with either 1 x 10’ Ba (broilers) or 3 x 10’ Ba (laversl of labelled VLDL in 01154M NiCl. Blood s&p& were removed from the opposite wing vein at appropriate intervals to determine the rate of VLDL clearance. Birds were then killed by cervical dislocation and the abdominal fat pad (including the fat surrounding the gizzard) was rapidly removed, rinsed in ice-cold 0.154 M NaCl and frozen in liquid nitrogen. Frozen tissue was crushed and duplicate 1 g samples extracted according to Folch et al. (1957). Solvent was evaporated under vacuum and the lipid residue dissolved in 5ml of scintillation fluid (Optiphase X, Fisons, Loughborough, U.K.) for determination of radioactivity. The extent of oxidation of lipoprotein triglyceride was measured by transferring individual birds to metabolism chambers immediately after intravenous injection of “Clabelled VLDL. Air was drawn through the chambers at a rate of 5 l/min and expired CO, recovered by passing through a Drescher bottle containing 150 ml of ethanolamine; 2-methoxymethanol (1: 2 v/v). Fresh trapping solution was used every 2 hr and duplicate 0.8 ml samples removed hourly for determination of expired radioactivity. The efficiency of trapping was assessed by measuring the recovery of radioactivity after intravenous injection of 3.7 x 10’ Bq of [“C]NaHCO, in saline. Recovery from three broilers was 90 & 3.9%. Measuremenr of lipoprorein lipase

Lipoprotein lipase (LPL) was measured using Intralipid (KabiVitrum, Stockholm, Sweden) as substrate, as described by Guo et al. (1988). LPL activity in tissues was measured in homogenates prepared in 0.233 M Tris/HCl, pH 8.5 containing 0.25 M sucrose and 10 mg bovine serum albumin, 1 mg sodium deoxycholate, 40 pg-Nonidet P.40, 20 pg of heparin and 20 pg phenylmethylsulphonylfluoride/ml (Iverius and Brunzell, 1985). The homogenates were centrifuged at 3000g for 5 min and activity assayed in the supematant. The proportion of lipase activity that was Table

attributable to LPL was determined by immunoprecipitation with an anti-LPL antiserum (Guo et al., 1988) and found to be greater than 95% in all tissues examined. Plasma hormone concentrations

Plasma samples were stored frozen at - 70°C and thawed only once. Plasma immunoreactive glucagon was measured by radioimmunoassay using a heterologous RIA kit (Cambridge Medical Diagnostics, Inc., MA, U.S.A.). Plasma GH concentrations were measured by enzyme-linked immunosorbent assay (Houston et al., 1991) based on two monoclonal antibodies against chicken growth hormone (GH) (Goddard et al., 1987). Plasma IGF-I concentrations were measured by heterologous radioimmunoassay (Armstrong et al., 1990). RESULTS

Comparison of broiler and layer strain chicks clearly needs to take account their very different rates of growth and in the present paper this has been achieved by expressing much of the data relative to body weight (Table 1). Five-week-old broiler chicks were much fatter than layer-strain chicks of the same age, but the overall rate of secretion of triglyceride into the plasma in the two strains was not very different (4.84 vs 3.43 g TG/d/kg body weight, Table 1). The overall rate of fat deposition can be calculated from the data for body composition (since this was unlikely to be changing in either strain at this age, Griffin et al., 1987) and daily weight gain. This produced estimates of about 4.7 and 1.9 g of triglyceride (TG) deposited/d/kg body weight for broilers and layers respectively. Plasma lipoprotein flux in broilers appears therefore to be just sufficient to account for all the total fat being deposited in broilers at 5 weeks of age. In contrast, plasma lipoprotein metabolism in layer-strain chicks appears to provide TG at about 1.8 times the rate that fat is actually accumulating. Intravenously-injected [14C]VLDL was cleared from the circulation more rapidly in layers than in broilers. A greater proportion was oxidised to [“C]C02 in layers than in broilers and a greater proportion of [14C]VLDL triglyceride was incorporated into the abdominal fat pad of broilers than of layers (Table 2). Uptake of the same proportions of endogenous lipoprotein flux into the abdominal fat pad (i.e. of 4.8 and 3.4 g of TG/kg body weight/day) is equivalent to the incorporation of about 280 and 140 mg of TG/kg body weight/day. Calculations from the data in Table 1 show that the daily growth of broilers and layers at 5 weeks of age involves the

I. Comparison of fattening and plasma lipoprotein metabolism in 5 week old broiler and layer chicks N

Body weight (g) Mean BW gain, 30-35 d (g/kg BW/d) Body lipid content (g/kg BW) Abdo&al fat (g/kgBw) Lipid in abdominal fast(mg/g) Plasma volume (ml/kg BW) Rate of lipoprotein secretion @moles TG/hr/ml of plasma) (g TG/d/kg BW)

Broilers

14 8 8 14 14 6

1231 k 38.2 f 123 f 16.2 f 710 f 47 +

234$ 3.6 12t 3.0t 78t 5.

16

4.84 * 1.91t 4.84 f 1.9lt

Layers 387 + 30.3 * 61 f 2.6 f 403 f 59 f

22 7.3 II I .6 153 6

2.71 +_0.98 3.43 f 1.24

Results are the means f SD of data from the number of birds/line indicated. Values for broilers that are significantly ditTerent(r-test) from those of layers are shown by: *P < 0.05; tP c 0.01; $P < 0.001.

Fattening

in broiler

and layer-strain

chickens

207

Table 2. Lipoprotein lipase activities and fate of [“qVLDL in broiler and layer chicks N LPL activity: -post-heparin plasma (units/ml) -leg muscle (units/g) -breast muscle (units/g) -thigh muscle (units/g) -heart (units/g) -abdominal fat pad (units/fat pad) (units/fat pad/kg BW) (units/g of tissue) I,,~ of VLDL clearance (mm) % oxidised to CO, after 8 hr % taken up by AFP

Broilers

8 8 8 8 8

53.9 + 10.5 f 5.0 f 9.0 f 82.9 f

8

4480 * 7431 3124 f 583t 189%31 5.0 * 1.0’ 21.4f4.3’ 5.9 * I .o*

5 3 6

12.6 4.6 3.2 3.7 12.8

Layers 46.1 f 8.7 k 7.5 f 10.2 + 58.8 +

23.4 3.0 1.6 4.8 23.5

274 + 185 699 k 475 192k60 3.3 f 0.3 28.9 f 0.8 4.1 * 1.9

Comparisons were made at 5 weeks of age as described in Materials and Methods. Values are the mean f SD of assays from the number of birds indicated/strain. Those for broilers that are significantly different (r-test) from those for layers are indicated by: *P
accumulation of about 440 and 35 mg of lipid per kg body weight by the abdominal fat pad. Plasma lipoprotein metabolism appears therefore to account for only about 65% of the total rate of lipid accumulation in the abdominal fat pad of broilers. In contrast, the rate of uptake of VLDL-TG by the abdominal fat pad of layers appeared to be about 4-fold greater than the net rate of lipid accumulation in the depot. There were no significant differences between strains in the specific activity of lipoprotein lipase in muscle and adipose tissue, but total LPL activity was much greater in the abdominal fat pad of broilers than in layers (Table 2), as reported previously (Griffin et al., 1987). The fates of [r4C]palmitate that had been incorporated into the abdominal fat pad of broilers and layers after intravenous injection of ‘*C-labelled VLDL are compared in Table 3. The first birds were killed after 1 day in this experiment to allow label that had been initially taken up by the liver (typically about 20% of that injected) to be cleared to other tissues. No significant fall in radioactivity was found in broiler adipose tissue between 1 and 7 days, but a rapid and significant decrease in labelling was observed in the fat pad of layers indicating a half life of adipose tissue TG of about 2-3 days. Mean plasma GH concentration and pulse amplitude was greater in layer strain chicks than in broilers (Fig. 1). The GH concentration in all samples taken from six broilers and six layers was 2.42 + 1.95 and 18.97 + 12,30 ng/ml respectively (P < 0.0001). There was no difference between strains in plasma insulinlike growth factor-I (IGF-I) concentration (42.5 + 10.7 and 40.5 f 11.3 ng/ml in broiler and Table 3. Turnover of adipose tissue triglycerides in the abdominal fat pad of broiler- and layer-strain chicks Radioactivity recovered (% of injected dose) Day 1 Day 2 Day 3 Broilers Layers

8.8 k I .6 3.4 + 1.3

7.8 & 1.9 1.8 + 0.9.

8.8 * 2.2 1.4 f 1.ot

Birds were injected intravenously with “C-1abelled VLDL and the proportion of injected radioactivity taken up and retained by the abdominal fat pad determined 1, 3 and 7 days later. Results are the means*SD of data from IO-12 birds/group. Values for birds killed after 3 and 7 days that are significantly different (r-test) from those for birds killed after 1 day are indicated by: lP < 0.01; tP < 0.001.

layer plasma respectively) or in plasma immunoreactive glucagon concentration (1.54 + 0.6 ng/ml for broilers and 1.68 f 0.27 ng/ml for layers).

DISCUSSION

In considering the role of plasma lipoprotein metabolism in supplying fatty acids for deposition in adipose tissue, it is important to appreciate that (1) a relatively high proportion of VLDL-triglyceride may be synthesized from pre-formed fatty acids (derived from the diet or from other tissues) and (2) a significant proportion of fatty acids available to the liver are oxidised rather than exported as VLDL (Fukoda and Ontko, 1984; Griffin et al., 1989). In vivo measurement of the rate of secretion of plasma TGR-lipoproteins into the circulation is therefore a much more useful indicator of the importance of lipoprotein metabolism in control of fat deposition than, for example, measurement of hepatic lipogenesis. The rate of TGR-lipoprotein secretion into the circulation of young layer chicks was surprisingly high and apparently sufficient to sustain a rate of accumulation of triglyceride almost 2-fold greater than the actual rate of accumulation of body fat. In contrast, the rate of TGR-secretion in broilers was hardly sufficient to account for the overall rate of accumulation of fat. The difference in fatness between broilers and layers could have been due, however, to differences in partitioning of plasma TG between oxidation in muscle and storage in adipose tissue. Layers are more active than broilers and they contain a significantly greater proportion of the oxidative type of muscle fibre rich in LPL (Linder et al., 1976; Aberle et al., 1979). However, there was no significant difference between strains in the specific activity of LPL in muscle (Table 2) and although a greater proportion of intravenously-injected [“CIVLDL was oxidised to CO, in layers than in broilers, the difference between strains (29 vs 21%) was too small to have a major effect on fat deposition. The relatively high proportion of [“C]VLDL taken up into the abdominal fat pad of layer chicks was surprising in view of the low LPL activity in the depot (Table 2). The partitioning of circulating TG between

H. D. GR~P~N et al.

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Fig. I. Growth hormone concentrations in the plasma of broiler- and layer-strain chicks at 4 weeks of age, Blood samples were taken from the wing vein of each bird every 12 min for between 1 and 3 hr. Panels depict patterns over time in three typical birds from each strain.

storage and oxidation is thought to be determined by the dist~bution of functional LPL activity between tissues (i.e. that proportion of total tissue activity present at the capillary bed, see Cryer, 1981). The results of the present study suggest avian adipose tissue is particularly effective in sequestering plasma TG, irrespective of the total activity of

LPL in the tissue. It may be that functional LPL activity is a particularly high proportion of total LPL activity in layer adipose tissue or that the fate of TGR-lipoproteins in chicken plasma is influenced more by other factors (e.g. the surface density of LPL at the capillary bed or blood flow).

Fattening in broiler and layer-strain chickens

The estimates of daily rates of uptake of VLDLTG into the abdominal fat pad and comparison with the actual rate of fat deposition in the depot are clearly subject to substantial error. Nevertheless they appear to show that the uptake of lipoprotein TG into the abdominal fat pad of 5 week old layers is very much greater than the net rate of accumulation of fat in the depot. It follows therefore that there must be a rapid turnover of adipose tissue TG in layer-strain chicks and this was confirmed by the rapid turnover of [‘4C]palmitate after its incorporation into the abdominal fat pad from [‘4C]-labelled VLDL. The rapid turnover of adipose tissue triglyceride in layers occurred even through the birds were maintained on a 23 hr light: 1 hr dark photoperiod. Under these conditions both broilers and layers feed continually (Savory, 1980) and the turnover of adipose tissue triglyceride in layers is therefore not dependent on feeding behaviour. Glucagon is the major lipolytic hormone in birds (Langslow and Hales, 1971) but plasma concentrations of immunoreactive glucagon were very similar in broiler and layer plasma. Growth hormone has been shown to have both lipolytic (Campbell and Scanes, 1985) and anti-lipolytic effects (Campbell and Scanes, 1987) on avian adipose tissue in vitro. The anti-lipolytic effect of GH is seen only as a transitory inhibition of glucagon-stimulated lipolysis and its role in vivo is not clear. Increases in body fat content of chickens following hypophysectomy have been used to support the view that the lipolytic effect of GH is important in vivo, but the responses to hypophysectomy appear to vary with strain and age. Hypophysectomy of White Leghorn chicks at 3 weeks of age is followed by a decrease in the circulating concentrations of non-esterified fatty acids (measured at 6 weeks of age) which are restored to normal by administration of chicken GH (Scanes et al., 1986). However, neither hypophysectomy or subsequent administration of GH had any significant effect on carcass fat content at this age (see Scanes, 1987). In contrast, hypophysectomy of chickens between 6 and 9 weeks of age produced a large increase in fat deposition that was accompanied by both a decrease in basal lipolysis (as measured in vitro) and an increase in hepatic fatty acid synthesis (Nalbandov and Card, 1943; Gibson and Nalbandov, 1966a,b). The effects of hypophysectomy on body composition could be due to the combined absence of other pituitary hormones but the available evidence suggests that GH is the most likely candidate (see Scanes, 1987). Pulsatile (but not continuous) administration of GH to 8 week old broilers decreases body fat content and hepatic lipogenesis and increases feed efficiency (Vasilatos-Younken et al., 1988; Rosebrough et al., 1990). The results in the present paper clearly show that the turnover of adipose tissue triglyceride in adipose tissue of layers makes a key contribution to their leanness and the association of such turnover with high and pulsatile plasma GH levels suggests it may be a direct or indirect effect of GH. Broiler strains that have continued to be selected for growth have lower plasma growth hormone concentrations that strains in which selection has been relaxed (Burke and Marks, 1982; Goddard et al., 1988) and this suggests

209

that the low plasma GH concentration in all broiler strains is a consequence of their selection for growth. In summary, the results of this study show that the relative fatness of broilers is due to (1) a higher rate of secretion of triglyceride-rich secretion into the circulation (2) an uptake of a greater proportion of secreted TG into adipose tissue, most probably because of a high adipose tissue LPL activity but in particular to (3) the absence of any significant turnover of adipose tissue TG. The latter characteristic may be the consequence of low plasma GH concentrations, since adipose tissue TG in 5 week old layer strain chicks (which have much higher plasma concentrations of growth hormone) has a half-life of about 2-3 days. REFERENCES Aberle E. D., Addis P. B. and Shoffner R. N. (1979) Fibre types in skeletal muscle of broiler and layer chickens. Poult. Sci. 58, 1210-1212. Armstrong D. G., Duclos M. J. and Goddard C. (1990). Biological activity of insulin-like growth factor I purified from chicken serum. Dam. An. Endocrin. 7, 383-393. Burke W. H. and Marks H. L. (1982) Growth hormone and prolactin levels in nonselected and selected broiler lines of chickens from hatch to eight weeks of age. Growth 46, 283-295. Campbell R. M. and Scanes C. G. (1985) Lipolytic activity of purified and bacterially derived growth hormone on chicken adipose tissue in vitro. Proc. Sot. Exp. Biol. Med. 180, 513-517. Campbell R. M. and Scanes C. G. (1987) Growth hormone inhibition of glucagon- and CAMP-induced lipolysis by chicken adipose tissue in vitro. Proc. Sot. Exp. Biol. Med. 184,456-460. Cryer A. (1981) Tissue lipoprotein lipase activity and its action in lipoprotein metabolism. Int. J. Biochem. 13, 525-541.

Folch J., Lees M. and Sloan Stanley G. H. (1957) A simple method for the isolation and purification of total lipids from animal tissues. J. Biol. Chem. 226, 497-509. Fukoda N. and Ontko J. A. (1984) Interactions between fatty acid synthesis, oxidation and esterification in the production of triglyceride-rich lipoproteins by the liver. J. Lipid Res. 25, 831-842.

Gibson W. R. and Nalbandov A. V. (1966a) Lipid mobilization in obese hypophysectomized cockerels. Am. J. Exp. 2001. 211, 1345-1351. Gibson W. R. and Nalbandov A. V. (1966b) Lipolysis and lipogenesis in liver and adipose tissue of hypophysectomized cockerels. Am. J. Expo. Zool. 211, 1352-1358. Goddard C., Houston B. and Gray C. (1987) Monoclonal antibody to chicken growth hormone. J. Endocr. 112, supplement, abstract 125. Goddard C., Wilkie R. and Dunn I. C. (1988) The relationship between insulin-like growth factor, growth hormone, thyroid hormone and insulin in chickens selected for growth. Dom. An. Endocrin. 5, 165-176. Griffin H. D. and Hermier D. (1988) Plasma lipoprotein metabolism and fattening in poultry. In Leanness in Domestic Birds (Edited by Leclercq B. and Whitehead C. C.) pp. 175-201. Butterworths, London. Griffin H. D., Acamovic F., Guo K. and Peddie J. (1989) Plasma lipoprotein metabolism in lean and fat chickens produced by divergent selection for plasma very low density lipoprotein concentration. J. Lipid Rex 30, 1243-1250.

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H. D. GRIN

Guo K., Griffin H. D. and Butterwith S. C. (1988) Biochemical indicators of fatness in meat-tye chickens: lack of correlation between lipoprotein lipase activity in postheparin plasma and body fat. Br. Poult. Sci. 29, 351-358. Houston B., Peddie C. D. and Goddard C. A monoclonal antibody-based enzyme-linked immunosorbent assay for chicken growth hormone. Br. Poulf. Sci. 32, 63344. Iverius P.-H. and Brunzell J. D. (1985) Human adipose tissue lipoprotein lipase: changes with feeding and relation to post-heparin plasma enzyme. Am. J. Physiol. 249, El 107-114. Langslow D. R. and Hales C. N. (1971) The role of the exocrine pancreas and catecholamines in the control of carbohydrate and lipid metabolism. In Physiology and Biochemistry of the Domestic Fowl (Edited by Bell D. J. and Freeman B. M.) Vol. 1, pp. 521-548. Academic Press, London. Linder C., Chemik S. S., Fleck T. R. and Scow R. 0. (1976) Lipoprotein lipase and uptake of chylomicron triglyceride by skeletal muscle of rats. Am. J. Physiol. 231, 860-864. McCarthy J. C. and Siegel P. B. (1983) A review of genetical and physiological effects of selection in meat-type poultry. Animal Breeding Abstracts 51, 87-94.

ef al.

Nalbandov A. V. and Card L. E. (1943) Effect of hypophysectomy on growing chicks. J. Exp. Zoo/. 94, 387-394.

Rosebrough R. W., McMurtry J. P. and Vasilatos-Younken R. (1990). Effect of pulsatile (P) or continuous (C) administration of pituitary-derived chicken growth hormone (pcGH) on lipid metabolism in broiler pullets. PO&. Sci. 69, supplement 1, 114. Savory C. J. (1980) Diurnal feeding patterns in domestic fowl: a review. Appl. An. Ethol. 6, 71-82. Scanes C. G. (1987) The physiology of growth, growth hormone, and other growth factors in poultry. CRC Crit. Revs. in Poulf. Biol. 1, 51-105. Scanes C. G., Duyka D. R., Lauterio T. J., Bowen S. J., Huybrechts L. M., Bacon W. L. and King D. B. (1986) Effects of chicken growth hormone, triiodothyronine and hypophysectomy in growing domestic fowl. Growth SO, 12-31. Vasilatos-Younken R., Cravener T. L., Cogbum L. A., Mast M. G. and Wellenreiter R. H. (1988) Effect of pattern of administration on the response to exogenous, pituitary derived chicken growth hormone by broilerstrain pullets. Gen. Comp. Endo. 71, 268-283.