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The Cellular Basis for Growth of the Abdominal Fat Pad in Broiler-Type Chickens
PHYSIOLOGY AND REPRODUCTION The Cellular Basis for Growth of the Abdominal Fat Pad in Broiler-Type Chickens ROSS L. HOOD CSIRO Division of Food Research, Food Research Laboratory, P.O. Box 52, North Ryde, New South Wales 2113, Australia (Received for publication July 14, 1980)
1982 Poultry Science 61:117-121
INTRODUCTION
Broiler chickens from selected genetic lines are fed high energy grain diets to achieve a greater monetary return. Carcasses from these chickens often have excessive fat in the abdominal and visceral region, which is considered undesirable to both the processor and the consumer. This fat must be removed and reprocessed as a component of poultry byproduct meal at a greatly reduced value when compared to the value of the carcass. The relative size of these fat deposits is influenced by nutritional factors (Farrell, 1974; Griffiths et al., 1977a,b) and genetic background (Littlefield, 1972; Pym and Solvyns, 1979). The mass of the abdominal fat pad is determined by the number and volume of adipose cells in the depot. Numerous studies with animals used for the production of meat have indicated tiiat in pigs (Anderson and Kauffman, 1973; Enser et al, 1976; Hood and Allen, 1977), cattle (Hood and Allen, 1973), and sheep (Haugebak etal., 1974; Hood and Thornton, 1979) both adipose cell number and volume increase for the first 5, 14, and 11 months of life, respectively. Beyond these respective physiological ages, further changes in adiposity are due to changes in adipose cell size. Comparatively few reports have been made on the cellularity of avian adipose tissue. A ninefold increase in adipose cell volume was observed in subcutaneous adipose tissue of ducks
during growth from day-old to 8 weeks (Evans, 1972). White Leghorn chickens were found to have smaller adipose cells in the abdominal fat pad than broiler-type chickens, and this difference was independent of nutrient intake (March and Hansen, 1977). When White Leghorn pullets were fed a low energy diet for the first 20 weeks, Pfaff and Austic (1976) found that the reduced size of the fat pad was associated with smaller adipose cells and not with a decrease in cell number. Ballam and March (1979) found that adipose cell size increased between 18 and 42 weeks of age and that dietary restriction from day-old to 12 and 14 weeks suppressed adipose cell enlargement; this effect remained until the birds were 42 weeks of age. This communication describes the application of the technique of Hirsch and Gallian (1968) to study the cellular development of avian adipose tissue and to determine the physiological age at which a fixed number of adipose cells is attained in the abdominal fat pad. MATERIALS AND METHODS
Tegel TM70 white broiler chickens were used in this study. The chickens were transferred from the incubator to battery brooders and then moved to larger cages as necessary. The chickens were fed a commercial starter (22.7% crude protein, 2950 kcal/kg) for the
117
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
ABSTRACT Cellular growth of the abdominal fat pads from Tegel TM70 white broiler chickens was characterized by both hyperplasia and hypertrophy of adipose cells until the chickens were approximately 14 weeks old, after which hypertrophy of existing adipose cells was solely responsible for increases in the mass of these fat deposits. The percent body fat was linearly and positively correlated with the weight of abdominal fat. However, at a constant percent body fat, male birds had a larger deposit of fat in the abdominal region than did females. Thus, a different relationship to predict body fat would be required for each sex. In mature birds the mass of an adipose tissue deposit is generally reflected in the size of adipose cells rather than the number of cells in an adipose organ. (Key words.- adipose cells, hypertrophy, hyperplasia, adiposity, abdominal fat pad, chickens)
HOOD
118
screening and the cells sized with a Coulter electronic counter by the method of Hirsch and Gallian (1968) as detailed by Hood and Allen (1977). The number of cells per abdominal fat pad is the product of the number of cells per gram of fat and the weight of the fat pad. RESULTS Liveweight gains were greater for male than for female chickens at all ages (Fig. 1). At 9 weeks, mean weights of 3.05 and 2.35 kg were achieved for male and female birds, respectively. This growth rate is similar to that achieved in commercial operations. The accumulation of fat in the body with increasing age is shown in Figure 2. Although the female birds were lighter than the males, they had a higher percent body fat at all ages. The relationship between the weight of abdominal fat pad and percent body fat is shown in Figure 3. At the same level of fatness male birds had a greater amount of lipid in their abdominal fat pad, as indicated by a significant difference (P<.01) in the shape of the curves given by the quadratic equations (Fig. 3) calculated for males and females. Growth of the fat deposits in the chicken was accompanied by an increase in the number (hyperplasia) and size (hypertrophy) of the adipose cells (Fig. 4). The number of adipose cells in the abdominal fat pad increased until about 14 weeks; beyond this time it remained constant at about 270 X 10 cells per fat pad. For the first 14 weeks, the mean size of adipose cells increased slowly due to the presence of increasing numbers of small cells. However, after 14 weeks adipose cell volume increased rapidly, since beyond this age growth of the
6-1
50^
40-
NP
2
30
"
in
10
S 2 °H
n O
10-
Age(weeks)
FIG. 1. Effect of age on the liveweight of male and female chickens.
Age(weeks)
FIG. 2. Relationship between age and percent carcass fat of male and female chickens.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
first 5 weeks and then the diet was changed to a commercial finisher (21.0% crude protein, 3120 kcal/kg). Both feeds were supplied by Allied Feeds, Sydney. The birds were weighed weekly during the experiment and at predetermined ages the birds (3 to 5 per age group) were killed by cervical fracture for body composition studies and cellularity measurements in the abdominal fat pad. After the birds had been plucked, the abdominal fat pad (adipose tissue surrounding the gizzard and between the intestines and abdominal muscles) was removed, weighed, and a small sample taken for adipose cell counting. Adipose tissue not used for cell counting was combined with the body and abdominal fat pad for body composition analysis. Each body was frozen and stored in a sealed plastic bag at —20 C prior to subsequent analysis. The frozen body was cut into small pieces (ca. 30 cm 3 ) with a band-saw and ground through a 5 mm screen with a Nolex No. 51 mincer. The ground body was passed through the mincer on two further occasions to obtain uniform mixing. The mixture was frozen and cut into thick slices (4 X 4 X .5 cm). The slices (8 to 10 g) were placed in folded filter papers, dried to constant weight in an oven for 18 hr at 105 C, and then extracted for 36 hr by repeated flushings with diethyl ether in a large soxhlet extractor capable of holding 40 samples. The water and lipid contents were determined in triplicate. Fresh adipose tissue slices (ca. 200 mg; < 1 mm thick) were cut and fixed with osmium tetroxide. The adipose cells were isolated by
ABDOMINAL FAT PAD GROWTH 200n
9
3)
100-
—I20
1
15
10
Body
fat
25
(%)
FIG. 3. Relationship between body fat and the weight of the abdominal fat pad in chickens less than 14 weeks of age. Males, Y = -9.2 - 2.07X + .39X1; Females Y = 7.2 - 3.1X + .32X2.
abdominal fat pad was due solely to the filling of existing adipose cells with lipid. Data relating to the cellularity and body composition of male chickens are listed in Table 1. These data refer only to birds older than 17 weeks of age, since at this age changes in the size of adipose tissue deposits were due to alterations in cell volume (Fig. 4). Unlike the female birds of this age, whose cellularity data were predictable from the size of the abdominal fat pad, the data for the male birds were more variable. The nine females in this age group had 278 ± 31 X 10 6 adipose cells in their fat
pads. Although the majority of males investigated had the expected number of cells in their fat pads, 4 birds (the last 4 listed in Table 1) produced unexpected results. Three birds had very small fat pads and were leaner than chickens of comparable age and weight. In fact, in these 3 birds the number of adipose cells was probably overestimated, since much of the fat pad was composed of connective tissue rather than lipid. The cellularity of the abdominal fat pad of the 4th bird was also unusual in that it was composed of a small number of very large adipose cells. The disparity in the results for older male chickens is also shown in Figure 5, which depicts the relationship between adipose cell volume and the weight of the abdominal fat pad. There was a significant linear relationship (r = .926, P<.01) between these two parameters for females, whereas the data for males were spread and no significant relationship was calculated. The lack of correlation confirms the variability of the cellularity data listed in Table 1.
DISCUSSION Growth was accompanied by an increased percent body fat and a concomitant increase in the weight of the abdominal fat pad. Significant correlation coefficients between these two parameters suggest that the weight of the fat pad could be a useful indicator of body fatness. However, a different relationship would be required for each sex, since at constant
TABLE 1. Body composition and cellularity data for male broiler chickens with ages greater than 17 weeks Adipose cells Live weight (kg)
Body fat
(%)a
Abdominal fat pad (g)
Average cell volume (nl)
Number' 3
4.9 5.1 6.5 6.3 4.9 6.3 5.4 5.1 5.9
18.7 19.0 17.6 17.6 19.1 19.4 12.1 13.1 ND
110 110 140 135 145 132 30 30 28
.481 .405 .559 .724 .641 1.102 .216 .457 .492
256 301 278 207 251 133 154 72 63
a
The percent body fat was not determined on one bird. These figures represent the numbers of cells (X 10"6) per abdominal fat pad.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
-**£-
119
120
HOOD
il
percent body fat the older male birds had larger deposits of fat in the abdominal region than females. This relationship does not hold for older male birds (greater than 17 weeks of age), since several of these birds were found to have very small fat pads. Considerable variation in the quantity of visceral fat has been demonstrated in 4-week-old birds (Griffiths et al, 1978). However, Griffiths et al. (1978) found that carcass fat at 8 weeks bore little relationship to abdominal fat at 4 weeks, suggesting that young birds may not provide meaningful estimates of excess fat in older birds. Growth of adipose tissue at the cellular level can occur by hyperplasia, hypertrophy, or a combination of these two mechanisms. In this study with broiler-type chickens, growth of the abdominal fat pad was achieved by both hypertrophy and hyperplasia of adipose cells until about 14 weeks of life. At 14 weeks adipose tissue reached physiological maturity and further growth was due solely to hypertrophy of existing cells. Pfaff and Austic (1976) found that the total DNA-deoxyribose content of adipose tissue of pullets increased for the first 12 to 15 weeks of life. The pattern of development in the chicken is similar to that of animals of economic importance to the meat industry. However, the time at which hyperplasia is complete varies among species and is probably related to the age at which physiological maturity is attained. Hood and Allen (1977) have reported that the final adipose cell number is a function of the true body size (weight of the fat-free carcass) of an animal. True body size is primarily dependent on heredity.
Research groups (Oscai et al, 1972; Miller and Wise, 1975) have shown that nutritional manipulation of the diet before rats are weaned can influence the number of adipose cells in their adipose tissue deposits. However, this nutritional restriction is often severe and is not a feasible practice for commercial broiler chicken operations. Also a decreased number of adipose cells does not necessarily imply that an animal or bird will have less fat at a given liveweight. For example, adiposity .in the pig is a function of cellular hypertrophy rather than cellular hyperplasia; during growth, adipose tissue from a lean strain of pigs (30.6% extramuscular fat) contained more adipose cells than in a fat strain of pigs (46.6% extramuscular fat) (Hood and Allen, 1977). Within a
Adipose cell volume ( n l )
FIG. 5. of adipose fat pad of Females Y =
Relationship between average volume cells and the weight of the abdominal chickens older than 17 weeks of age. 306X-11.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
FIG. 4. Effect of age on volume and number of adipose cells in the abdominal fat pad of the chicken. The data are averaged across sexes.
At maturity the abdominal fat pad contained about 270 X 10 6 adipose cells, which contrasts with the value of 349 X 10 6 for Hubbard chickens obtained by Ballam and March (1979) using a microscopic method to measure cellularity. In response to feed restriction from day-old to 12 and 14 weeks of age, these authors also reported an increase in adipose cell number in this depot due to the presence of many small cells. March and Hansen (1977) determined from the lipid/DNA ratio that cell multiplication was active in 6-week-old chicks and that this multiplication proceeded when nutrient intake was restricted, although the cells remained small. Unlike a study on rat epididymal fat pads (Knittle and Hirsch, 1968), Pfaff and Austic (1976) were not able to demonstrate a permanent effect of early diet on the cellularity of the adbominal fat pad of White Leghorn pullets.
ABDOMINAL FAT PAD GROWTH
ACKNOWLEDGMENTS The author would like to thank P. E. Walton for his technical assistance, A. A. Tegel Pry. Limited for the supply of chickens, and Allied Mills for the preparation of the diets. This work was supported in part by a grant from the Australian Chicken Meat Research Committee.
REFERENCES Anderson, D. B., and R. G. Kauffman, 1973. Cellular and enzymatic changes in porcine adipose tissue during growth. J. Lipid Res. 14:160—168. Ballam, G. C , and B. E. March, 1979. Adipocyte size and number in mature broiler-type female chickens subjected to dietary restriction during the growing period. Poultry Sci. 58:940-948. Enser, M. B., J. D. Wood, D. J. Restall, and H.J.H. MacFie, 1976. The cellularity of adipose tissue from pigs of different weights. J. Agr. Sci. 86:633-638. Evans, A. J., 1972. Changes in adipocyte size during postembryonic growth in the female Aylesbury duck. Brit. Poultry Sci. 13:615-618. Farrell, D. J., 1974. Effects of dietary energy con-
centration on utilisation of energy by broiler chickens and on body composition determined by carcass analysis and predicted using tritium. Brit. Poultry Sci. 1 5 : 2 5 - 4 1 . Griffiths, L., S. Leeson, and J. D. Summers, 1977a. Fat deposition in broilers: Effect of dietary energy to protein balance, and early life caloric restriction on productive performance and abdominal fat pad size. Poultry Sci. 56:638—646. Griffiths, L., S. Leeson, and J. D. Summers, ^L977b. Influence of energy system and level of various fat sources on performance and carcass composition of broilers. Poultry Sci. 56:1018-1026. Griffiths, L., S. Leeson, and J. D. Summers, 1978. Studies on abdominal fat with four commercial strains of male broiler chicken. Poultry Sci. 57:1198-1203. Haugebak, C. D., H. B. Hedrick, and J. M. Asplund, 1974. Adipose tissue accumulation and cellularity in growing and fattening lambs. J. Anim. Sci. 39:1016-1024. Hirsch, J., and E. Gallian, 1968. Methods for the determination of adipose cell size in man and animals. J. Lipid Res. 9:110-119. Hood, R. L., and C. E. Allen, 1973. Cellularity of bovine adipose tissue. J. Lipid Res. 14:605—610. Hood, R. L. and C. E. Allen, 1977. Cellularity of porcine adipose tissue: effects of growth and adiposity. J. Lipid Res. 18:275-284. Hood, R. L., and R. F. Thornton, 1979. The cellularity of ovine adipose tissue. Australia J. Agric. Res. 30:153-161. Knittle, J. L., and J. Hirsch, 1968. Effect of early nutrition on the development of rat epididymal fat pads: cellularity and metabolism. J. Clin. Invest. 47:2091-2098. Littlefield, L. H., 1972. Strain differnece in quantity of abdominal fat in broilers. Poultry Sci. 51: 1829. March, B. E., and G. Hansen, 1977. Lipid accumulation and cell multiplication in adipose bodies in White Leghorn and broiler-type chicks. Poultry Sci. 56:886-894. Miller, D. S., and A. Wise, 1975. Maintenance requirement and adipocyte count of rats from large and small litters at the same weight. Proc. Nutr. Soc. 34:105A. Oscai, L. B., C. N. Spirakis, C. A. Wolff, and R. J. Beck, 1972. Effects of exercise and of food restriction on adipose tissue cellularity. J. Lipid Res. 13:588-592. Pfaff, F. E., Jr., and R. E. Austic, 1976. Influence of diet on development of the abdominal fat pad in the pullet. J. Nutr. 106:443-450. Pym, R.A.E., and A. J. Solvyns, 1979. Selection for food conversion in broilers: Body composition of birds selected for increased bodyweight gain, food consumption and food conversion ratio. Brit. Poultry Sci. 20:87-97.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
breed and at constant liveweight, Hood and Allen (1977) found that adiposity was positively correlated with adipose cell volume and not cell number. There are differences in the cellularity of the abdominal fat pads of male birds (Table 1), although the importance of this observation in relation to body fat content is not yet clear. Although some of these birds were lean and had small fat pads this may not necessarily be a consequence of adipose cell number but rather due to metabolic differences in the utilization of dietary energy. Perhaps a full "bed" of cells was laid down, were present as pre-adipose cells, and were not measured, since only cells greater than 25 nm in diameter are counted with this technique. The relevance of adipose cell number in the determination of adiposity is still not understood. Rather than select birds with a reduced adipose cell number, it would be more desirable to select parents of birds with small fat pads for a breeding program to reduce body fat. Selection for this criterion is made on a metabolic basis, which is probably genetic in origin, and not on a cellular basis.
121
1982 Poultry Science 61:117-121
INTRODUCTION
Broiler chickens from selected genetic lines are fed high energy grain diets to achieve a greater monetary return. Carcasses from these chickens often have excessive fat in the abdominal and visceral region, which is considered undesirable to both the processor and the consumer. This fat must be removed and reprocessed as a component of poultry byproduct meal at a greatly reduced value when compared to the value of the carcass. The relative size of these fat deposits is influenced by nutritional factors (Farrell, 1974; Griffiths et al., 1977a,b) and genetic background (Littlefield, 1972; Pym and Solvyns, 1979). The mass of the abdominal fat pad is determined by the number and volume of adipose cells in the depot. Numerous studies with animals used for the production of meat have indicated tiiat in pigs (Anderson and Kauffman, 1973; Enser et al, 1976; Hood and Allen, 1977), cattle (Hood and Allen, 1973), and sheep (Haugebak etal., 1974; Hood and Thornton, 1979) both adipose cell number and volume increase for the first 5, 14, and 11 months of life, respectively. Beyond these respective physiological ages, further changes in adiposity are due to changes in adipose cell size. Comparatively few reports have been made on the cellularity of avian adipose tissue. A ninefold increase in adipose cell volume was observed in subcutaneous adipose tissue of ducks
during growth from day-old to 8 weeks (Evans, 1972). White Leghorn chickens were found to have smaller adipose cells in the abdominal fat pad than broiler-type chickens, and this difference was independent of nutrient intake (March and Hansen, 1977). When White Leghorn pullets were fed a low energy diet for the first 20 weeks, Pfaff and Austic (1976) found that the reduced size of the fat pad was associated with smaller adipose cells and not with a decrease in cell number. Ballam and March (1979) found that adipose cell size increased between 18 and 42 weeks of age and that dietary restriction from day-old to 12 and 14 weeks suppressed adipose cell enlargement; this effect remained until the birds were 42 weeks of age. This communication describes the application of the technique of Hirsch and Gallian (1968) to study the cellular development of avian adipose tissue and to determine the physiological age at which a fixed number of adipose cells is attained in the abdominal fat pad. MATERIALS AND METHODS
Tegel TM70 white broiler chickens were used in this study. The chickens were transferred from the incubator to battery brooders and then moved to larger cages as necessary. The chickens were fed a commercial starter (22.7% crude protein, 2950 kcal/kg) for the
117
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
ABSTRACT Cellular growth of the abdominal fat pads from Tegel TM70 white broiler chickens was characterized by both hyperplasia and hypertrophy of adipose cells until the chickens were approximately 14 weeks old, after which hypertrophy of existing adipose cells was solely responsible for increases in the mass of these fat deposits. The percent body fat was linearly and positively correlated with the weight of abdominal fat. However, at a constant percent body fat, male birds had a larger deposit of fat in the abdominal region than did females. Thus, a different relationship to predict body fat would be required for each sex. In mature birds the mass of an adipose tissue deposit is generally reflected in the size of adipose cells rather than the number of cells in an adipose organ. (Key words.- adipose cells, hypertrophy, hyperplasia, adiposity, abdominal fat pad, chickens)
HOOD
118
screening and the cells sized with a Coulter electronic counter by the method of Hirsch and Gallian (1968) as detailed by Hood and Allen (1977). The number of cells per abdominal fat pad is the product of the number of cells per gram of fat and the weight of the fat pad. RESULTS Liveweight gains were greater for male than for female chickens at all ages (Fig. 1). At 9 weeks, mean weights of 3.05 and 2.35 kg were achieved for male and female birds, respectively. This growth rate is similar to that achieved in commercial operations. The accumulation of fat in the body with increasing age is shown in Figure 2. Although the female birds were lighter than the males, they had a higher percent body fat at all ages. The relationship between the weight of abdominal fat pad and percent body fat is shown in Figure 3. At the same level of fatness male birds had a greater amount of lipid in their abdominal fat pad, as indicated by a significant difference (P<.01) in the shape of the curves given by the quadratic equations (Fig. 3) calculated for males and females. Growth of the fat deposits in the chicken was accompanied by an increase in the number (hyperplasia) and size (hypertrophy) of the adipose cells (Fig. 4). The number of adipose cells in the abdominal fat pad increased until about 14 weeks; beyond this time it remained constant at about 270 X 10 cells per fat pad. For the first 14 weeks, the mean size of adipose cells increased slowly due to the presence of increasing numbers of small cells. However, after 14 weeks adipose cell volume increased rapidly, since beyond this age growth of the
6-1
50^
40-
NP
2
30
"
in
10
S 2 °H
n O
10-
Age(weeks)
FIG. 1. Effect of age on the liveweight of male and female chickens.
Age(weeks)
FIG. 2. Relationship between age and percent carcass fat of male and female chickens.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
first 5 weeks and then the diet was changed to a commercial finisher (21.0% crude protein, 3120 kcal/kg). Both feeds were supplied by Allied Feeds, Sydney. The birds were weighed weekly during the experiment and at predetermined ages the birds (3 to 5 per age group) were killed by cervical fracture for body composition studies and cellularity measurements in the abdominal fat pad. After the birds had been plucked, the abdominal fat pad (adipose tissue surrounding the gizzard and between the intestines and abdominal muscles) was removed, weighed, and a small sample taken for adipose cell counting. Adipose tissue not used for cell counting was combined with the body and abdominal fat pad for body composition analysis. Each body was frozen and stored in a sealed plastic bag at —20 C prior to subsequent analysis. The frozen body was cut into small pieces (ca. 30 cm 3 ) with a band-saw and ground through a 5 mm screen with a Nolex No. 51 mincer. The ground body was passed through the mincer on two further occasions to obtain uniform mixing. The mixture was frozen and cut into thick slices (4 X 4 X .5 cm). The slices (8 to 10 g) were placed in folded filter papers, dried to constant weight in an oven for 18 hr at 105 C, and then extracted for 36 hr by repeated flushings with diethyl ether in a large soxhlet extractor capable of holding 40 samples. The water and lipid contents were determined in triplicate. Fresh adipose tissue slices (ca. 200 mg; < 1 mm thick) were cut and fixed with osmium tetroxide. The adipose cells were isolated by
ABDOMINAL FAT PAD GROWTH 200n
9
3)
100-
—I20
1
15
10
Body
fat
25
(%)
FIG. 3. Relationship between body fat and the weight of the abdominal fat pad in chickens less than 14 weeks of age. Males, Y = -9.2 - 2.07X + .39X1; Females Y = 7.2 - 3.1X + .32X2.
abdominal fat pad was due solely to the filling of existing adipose cells with lipid. Data relating to the cellularity and body composition of male chickens are listed in Table 1. These data refer only to birds older than 17 weeks of age, since at this age changes in the size of adipose tissue deposits were due to alterations in cell volume (Fig. 4). Unlike the female birds of this age, whose cellularity data were predictable from the size of the abdominal fat pad, the data for the male birds were more variable. The nine females in this age group had 278 ± 31 X 10 6 adipose cells in their fat
pads. Although the majority of males investigated had the expected number of cells in their fat pads, 4 birds (the last 4 listed in Table 1) produced unexpected results. Three birds had very small fat pads and were leaner than chickens of comparable age and weight. In fact, in these 3 birds the number of adipose cells was probably overestimated, since much of the fat pad was composed of connective tissue rather than lipid. The cellularity of the abdominal fat pad of the 4th bird was also unusual in that it was composed of a small number of very large adipose cells. The disparity in the results for older male chickens is also shown in Figure 5, which depicts the relationship between adipose cell volume and the weight of the abdominal fat pad. There was a significant linear relationship (r = .926, P<.01) between these two parameters for females, whereas the data for males were spread and no significant relationship was calculated. The lack of correlation confirms the variability of the cellularity data listed in Table 1.
DISCUSSION Growth was accompanied by an increased percent body fat and a concomitant increase in the weight of the abdominal fat pad. Significant correlation coefficients between these two parameters suggest that the weight of the fat pad could be a useful indicator of body fatness. However, a different relationship would be required for each sex, since at constant
TABLE 1. Body composition and cellularity data for male broiler chickens with ages greater than 17 weeks Adipose cells Live weight (kg)
Body fat
(%)a
Abdominal fat pad (g)
Average cell volume (nl)
Number' 3
4.9 5.1 6.5 6.3 4.9 6.3 5.4 5.1 5.9
18.7 19.0 17.6 17.6 19.1 19.4 12.1 13.1 ND
110 110 140 135 145 132 30 30 28
.481 .405 .559 .724 .641 1.102 .216 .457 .492
256 301 278 207 251 133 154 72 63
a
The percent body fat was not determined on one bird. These figures represent the numbers of cells (X 10"6) per abdominal fat pad.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
-**£-
119
120
HOOD
il
percent body fat the older male birds had larger deposits of fat in the abdominal region than females. This relationship does not hold for older male birds (greater than 17 weeks of age), since several of these birds were found to have very small fat pads. Considerable variation in the quantity of visceral fat has been demonstrated in 4-week-old birds (Griffiths et al, 1978). However, Griffiths et al. (1978) found that carcass fat at 8 weeks bore little relationship to abdominal fat at 4 weeks, suggesting that young birds may not provide meaningful estimates of excess fat in older birds. Growth of adipose tissue at the cellular level can occur by hyperplasia, hypertrophy, or a combination of these two mechanisms. In this study with broiler-type chickens, growth of the abdominal fat pad was achieved by both hypertrophy and hyperplasia of adipose cells until about 14 weeks of life. At 14 weeks adipose tissue reached physiological maturity and further growth was due solely to hypertrophy of existing cells. Pfaff and Austic (1976) found that the total DNA-deoxyribose content of adipose tissue of pullets increased for the first 12 to 15 weeks of life. The pattern of development in the chicken is similar to that of animals of economic importance to the meat industry. However, the time at which hyperplasia is complete varies among species and is probably related to the age at which physiological maturity is attained. Hood and Allen (1977) have reported that the final adipose cell number is a function of the true body size (weight of the fat-free carcass) of an animal. True body size is primarily dependent on heredity.
Research groups (Oscai et al, 1972; Miller and Wise, 1975) have shown that nutritional manipulation of the diet before rats are weaned can influence the number of adipose cells in their adipose tissue deposits. However, this nutritional restriction is often severe and is not a feasible practice for commercial broiler chicken operations. Also a decreased number of adipose cells does not necessarily imply that an animal or bird will have less fat at a given liveweight. For example, adiposity .in the pig is a function of cellular hypertrophy rather than cellular hyperplasia; during growth, adipose tissue from a lean strain of pigs (30.6% extramuscular fat) contained more adipose cells than in a fat strain of pigs (46.6% extramuscular fat) (Hood and Allen, 1977). Within a
Adipose cell volume ( n l )
FIG. 5. of adipose fat pad of Females Y =
Relationship between average volume cells and the weight of the abdominal chickens older than 17 weeks of age. 306X-11.
Downloaded from http://ps.oxfordjournals.org/ at Universitat Autònoma de Barcelona on October 29, 2014
FIG. 4. Effect of age on volume and number of adipose cells in the abdominal fat pad of the chicken. The data are averaged across sexes.
At maturity the abdominal fat pad contained about 270 X 10 6 adipose cells, which contrasts with the value of 349 X 10 6 for Hubbard chickens obtained by Ballam and March (1979) using a microscopic method to measure cellularity. In response to feed restriction from day-old to 12 and 14 weeks of age, these authors also reported an increase in adipose cell number in this depot due to the presence of many small cells. March and Hansen (1977) determined from the lipid/DNA ratio that cell multiplication was active in 6-week-old chicks and that this multiplication proceeded when nutrient intake was restricted, although the cells remained small. Unlike a study on rat epididymal fat pads (Knittle and Hirsch, 1968), Pfaff and Austic (1976) were not able to demonstrate a permanent effect of early diet on the cellularity of the adbominal fat pad of White Leghorn pullets.
ABDOMINAL FAT PAD GROWTH
ACKNOWLEDGMENTS The author would like to thank P. E. Walton for his technical assistance, A. A. Tegel Pry. Limited for the supply of chickens, and Allied Mills for the preparation of the diets. This work was supported in part by a grant from the Australian Chicken Meat Research Committee.
REFERENCES Anderson, D. B., and R. G. Kauffman, 1973. Cellular and enzymatic changes in porcine adipose tissue during growth. J. Lipid Res. 14:160—168. Ballam, G. C , and B. E. March, 1979. Adipocyte size and number in mature broiler-type female chickens subjected to dietary restriction during the growing period. Poultry Sci. 58:940-948. Enser, M. B., J. D. Wood, D. J. Restall, and H.J.H. MacFie, 1976. The cellularity of adipose tissue from pigs of different weights. J. Agr. Sci. 86:633-638. Evans, A. J., 1972. Changes in adipocyte size during postembryonic growth in the female Aylesbury duck. Brit. Poultry Sci. 13:615-618. Farrell, D. J., 1974. Effects of dietary energy con-
centration on utilisation of energy by broiler chickens and on body composition determined by carcass analysis and predicted using tritium. Brit. Poultry Sci. 1 5 : 2 5 - 4 1 . Griffiths, L., S. Leeson, and J. D. Summers, 1977a. Fat deposition in broilers: Effect of dietary energy to protein balance, and early life caloric restriction on productive performance and abdominal fat pad size. Poultry Sci. 56:638—646. Griffiths, L., S. Leeson, and J. D. Summers, ^L977b. Influence of energy system and level of various fat sources on performance and carcass composition of broilers. Poultry Sci. 56:1018-1026. Griffiths, L., S. Leeson, and J. D. Summers, 1978. Studies on abdominal fat with four commercial strains of male broiler chicken. Poultry Sci. 57:1198-1203. Haugebak, C. D., H. B. Hedrick, and J. M. Asplund, 1974. Adipose tissue accumulation and cellularity in growing and fattening lambs. J. Anim. Sci. 39:1016-1024. Hirsch, J., and E. Gallian, 1968. Methods for the determination of adipose cell size in man and animals. J. Lipid Res. 9:110-119. Hood, R. L., and C. E. Allen, 1973. Cellularity of bovine adipose tissue. J. Lipid Res. 14:605—610. Hood, R. L. and C. E. Allen, 1977. Cellularity of porcine adipose tissue: effects of growth and adiposity. J. Lipid Res. 18:275-284. Hood, R. L., and R. F. Thornton, 1979. The cellularity of ovine adipose tissue. Australia J. Agric. Res. 30:153-161. Knittle, J. L., and J. Hirsch, 1968. Effect of early nutrition on the development of rat epididymal fat pads: cellularity and metabolism. J. Clin. Invest. 47:2091-2098. Littlefield, L. H., 1972. Strain differnece in quantity of abdominal fat in broilers. Poultry Sci. 51: 1829. March, B. E., and G. Hansen, 1977. Lipid accumulation and cell multiplication in adipose bodies in White Leghorn and broiler-type chicks. Poultry Sci. 56:886-894. Miller, D. S., and A. Wise, 1975. Maintenance requirement and adipocyte count of rats from large and small litters at the same weight. Proc. Nutr. Soc. 34:105A. Oscai, L. B., C. N. Spirakis, C. A. Wolff, and R. J. Beck, 1972. Effects of exercise and of food restriction on adipose tissue cellularity. J. Lipid Res. 13:588-592. Pfaff, F. E., Jr., and R. E. Austic, 1976. Influence of diet on development of the abdominal fat pad in the pullet. J. Nutr. 106:443-450. Pym, R.A.E., and A. J. Solvyns, 1979. Selection for food conversion in broilers: Body composition of birds selected for increased bodyweight gain, food consumption and food conversion ratio. Brit. Poultry Sci. 20:87-97.
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breed and at constant liveweight, Hood and Allen (1977) found that adiposity was positively correlated with adipose cell volume and not cell number. There are differences in the cellularity of the abdominal fat pads of male birds (Table 1), although the importance of this observation in relation to body fat content is not yet clear. Although some of these birds were lean and had small fat pads this may not necessarily be a consequence of adipose cell number but rather due to metabolic differences in the utilization of dietary energy. Perhaps a full "bed" of cells was laid down, were present as pre-adipose cells, and were not measured, since only cells greater than 25 nm in diameter are counted with this technique. The relevance of adipose cell number in the determination of adiposity is still not understood. Rather than select birds with a reduced adipose cell number, it would be more desirable to select parents of birds with small fat pads for a breeding program to reduce body fat. Selection for this criterion is made on a metabolic basis, which is probably genetic in origin, and not on a cellular basis.
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