Caponization Effects on Growth Performance and Lipid Metabolism in Taiwan Country Chicken Cockerels

This trial was designed to study the caponization effects on the appearance, carcass characteristics, blood constituents and lipid metabolism of Taiwan country chicken cockerels. Cockerels were caponized at 8 weeks of age. Sixteen-week-old chickens, including 10 capons, 5 slips (incomplete caponized male chickens) and 20 normal chickens of equal sexes were selected for a 10 week ad libitum feeding trial. Results showed that the testosterone concentrations in the capons and females were lower (p<0.05) than that of intact males. The comb length, height and weights were also lower (p<0.05). The weight of the slips was between that of the capons and intact males, but was heavier (p<0.05) than that of the capon. The live-weight, carcass weight and shank perimeter in the capons were higher than those of the other groups (p<0.05). Hepatic lipogenic enzyme activity analyses showed that NADP-malic dehydrogenase (MDH) activity in the capons and female chickens was higher than that in intact male chickens (p<0.05). The MDH activity in the slips was between that for the capon and intact male chickens (p>0.05). The abdominal fat weight and relative abdominal fat weight of the capons and females were heavier than that for intact males (p<0.05); the slips were between the capons and intact males. The blood lipid content results showed that the triacylglycerol and cholesterol in the capons were higher than that for intact males (p<0.05). However, the percentage of low-density lipoprotein (LDL) was lower than that in intact male chickens (p<0.05). It appears that the increase in lipid accumulation in caponized male chickens is attributed mainly to an increase in MDH activity and the changes in lipid transportation in the capons. (Asian-Aust. J. Anim. Sci. 2006. Vol 19, No. 3 : 438-443)


INTRODUCTION
Capons are defined as having the testis artificially removed via a surgical operation on 6 to 12-week old male chickens.The secondary male sexual characteristics then degenerate (including comb, wattle, colour, fighting behavior and sound production etc.).Capons experience fat accumulation upon sexual maturity, have enhanced flavor, texture and juicy muscle meat compared with intact cockerels (Chen et al., 2000a, b;Chang, 2001).In Taiwan, 4.3 million capons were consumed each year (Hsieh, 2002).
Literatures showed the caponization effects on carcass characteristics in male chickens (Rath et al., 1996), but results were discrepant due to strains, age on caponization and feeding period.The caponization effect on muscle formation is still not well understood.Some researchers regard it as a promoter (Ono et al., 1979(Ono et al., , 1982;;Cason et al., 1988), while others regard it as a depressor on muscle growth (Fennell and Scanes, 1992;Morgan et al., 1993;Burke and Edwards, 1994).Although most researchers agree on the promotion effect of caponization on lipid accumulation and regard it as the testosterone inhibitory effect on lipid accumulation (Deyhim et al., 1992;Fennell and Scanes, 1992), the lipogenesis mechanism after caponization has not been described in the literature and is still unclear.Therefore, further research is required on the lipid lipogenesis and metabolism in capons.
In general, 5 to 20% of incompletely caponized chickens (slip) are detected even when the surgical operation is conducted by an experienced technician.These slips present more prominent secondary sexual characteristics, compared with the capon, but less prominent compared with intact birds, especially the comb and wattle.Occurrence of these slips probably due to regeneration from the residual testis cells that could not be detected from visual inspection.Slips are not favored or accepted as capons by consumers, resulting in a huge loss in revenue.Moreover, the shape and body fat accumulation trend toward feminization after caponization in male chickens require using female chickens as negative controls.
The aim of this trial was to study the capon and slip effect on the appearance, growth performance, carcass characteristics, blood constituents and lipid metabolism in Taiwan country chickens by the commercial production model.

Experimental animal and management
Taiwan Country chickens line D×L2 bred by National Chung-Hsing University were housed in individual 40×30 cm, 38 cm high cages.Water was provided using a water trough and commercial growing diet of 16% CP and 11.72 MJ/kg ME with water was provided ad libitum for the chickens.Cockerels were caponized at 8 weeks of age.Thirty-five sixteen-week-old chickens, including 10 capons, 5 slips (incomplete caponized male chickens) and 20 normal intact birds of equal sexes were selected for 10 weeks feeding.

Testectomy
The procedure of testectomy is according to Chen et al. (2005a).Restricted to feed and water for 12 h before surgical operation, intact male chickens were then restrained and the site of incision was sterilized with iodinealcohol.A 1 cm lateral incision was made at the second to last rib, and the testes were removed.Iodine-alcohol again was applied to the site of incision.

Measurements and analyses
Growth performance and appearances : During the feeding period, feed intake and live-weight were measured weekly.The appearance, including length, height and weight of comb and perimeter of shank were measured at the end of the feeding trial.
Carcass characteristics : The abdominal fat was stripped off immediately after the livers, gizzard, and testicles were removed and weighed.The abdominal fat included the fat surrounding gizzard and fat pad in the abdominal cavity.Fat located in the intestinal mesenteries was included in the intestinal tract.
Blood constituents : Blood samples, 10 ml each, were taken from the ulner-vein after birds were withdrawn from feed and water for 12 h before sacrifice at the end of the trial.Blood sera were obtained as supernatants after centrifugation at 1,500×g for 15 min.and stored at -40°C for further analysis.Blood serum glucose, triacylglycerol and total cholesterol concentrations were analyzed using an automatic blood chemical analyzer with Roche testing kits (Roche COBAS MIRA PLUS).Non-esterified fatty acid (NEFA) was determined using a spectrophotometer according to the modified method of Chromy et al. (1977).Lipoproteins were analyzed according to Houstmuller (1969) and using Helena titian gel electrophoresis.Electrophoresis data center scanning densitometry (Helena Laboratories, USA) was used to estimate the area of each fraction (Lien et al., 2005).Testosterone concentration was measured according to Li et al. (1987).

Statistical analysis
Analyses of variance were calculated using the general linear model procedure of the SAS (1985).Duncan's new multiple-range test was used to compare the means according to Steel and Torrie (1960).The correlation between the blood constituents, carcass characteristics and performance was analyzed using the PROC CORR of the SAS (1985) and Pearson's correlation analysis.

Growth performance and appearances
Table 1 presents the caponization effect on the testosterone, performance and appearance of Taiwan country chickens.Caponization increased the live-weight as the capons became heavier (p<0.05)than the slips and intact males.The smallest (p<0.05)comb length, height and weight were in capons and females, followed by the slips and males.This reflected that caponization decreased the secondary sexual characteristics as the slips were partially affected.The perimeter of the shank was longest in the capon (p<0.05)followed by the slips, intact males and females with the shortest (p<0.05).The testosterone concentration was highest in the intact males (p<0.05).
The heavier live-weight in the capons compared with intact males in this trial agreed with the results of Chen et al. (2000a, b).The capons gained weight faster in the late growing phase (Chen et al., 2000b;Kuo, 2002).Farmers use the shank perimeter as the fatness indicator for capons.However, in this trial that the longest shank perimeter was not significantly correlated with fat deposition in the capon.
Caponization decreased the serum testosterone concentration (Mashaly, 1984;Burke and Edwards, 1994), hence the secondary male sexual characteristics, comb weight, were significantly decreased (Fennell and Scanes, 1992;Wang, 2001).This agreed with significantly increased comb weight produced by exogenous testosterone implantation in chickens (Fennell and Scanes, 1992;Astiningsih and Rogers, 1996).The testosterone concentration of capons was only 5% (32.9 pg/ml) of the intact males.The slips, however, with some remaining testicle tissue, approximately 26% of the weight of the intact bird, showed a trend toward secreting more testosterone than the capon (p<0.10).Hence, slips showed significant secondary male sexual characteristics as compared with the capon.However, these characteristics were less prominent than those in intact males.From appearance observations, the comb and wattle in the capons degenerated to female size with a pale colour.The slips possessed large red combs, that were longer in length, taller in height and heavier in weight (p<0.05)compared with the capons.These male secondary sexual characteristics were significantly correlated with the serum testosterone concentration, as shown in Table 4.The serum testosterone concentration (pg/ml) can be predicted from the comb length regression equation (=-563.18+10.492X, in mm), height (=-358.95+16.256X, in mm) and the comb weight (= 32.649+14.195X, in g) (p<0.001).Therefore, success of surgical caponization can be evaluated from the chicken appearance.

Carcass characteristics
Table 2 presents the caponization effect on the carcass traits of Taiwan country chickens.The carcass weight was heaviest (p<0.05) in the capon, but not different in dressing percentage from the slip and male.Caponization increased the lipid deposition as the subcutaneous fat and relative subcutaneous fat weight were lightest (p<0.05) in intact males.The abdominal fat and relative abdominal fat weight were heaviest (p<0.05) in the capon and females compared with the intact males (p<0.05).Caponization also increased the weight of gizzard, intestine and relative intestine weight (p<0.05)compared with intact males.The females also showed a trend toward heavier intestine weight and relative intestine weight compared with the slips and intact males.The testicle weight and relative testicle weight were lighter (p<0.05) in the slip compared with intact males.
Maturity of Taiwan country chickens occurs at around 16 weeks of age.The male has fighting behavior, probably due to the androgen effect after maturity, and depressed growth afterward (Wang, 2001).In this trial, the capons consumed more feed and gain with less fighting behavior compared with the intact males.The dressing percentage did not differ (p>0.05)among capons, slips and intact males.Caponization resulted in the heavier abdominal fat and intestine weight, but showed no effects on relative weights of liver, gizzard and subcutaneous fat weight, which resulted in the unmarked difference on dressing percent.
In the lipid deposition, the weight of subcutaneous fat in the breast and relative weight of the abdominal fat in the capon were similar to that in the females.However, both were greater (p<0.05)than that in intact males.The weight and relative weight of the subcutaneous fat in the breast of slips did not differ from that of females (p>0.05).However, the weight was heavier than that in intact males (p<0.05).Caponization influenced the testosterone concentration in intact males (p<0.05)(Deyhim et al., 1992;Fennell et al., 1996;Chen et al., 2000a).In this trial, the testosterone concentration was negatively correlated with the fat deposition (r = 0.44; p<0.05,Table 4) and reflected the influence of testosterone on the fat deposition.Lack of testosterone in capons caused fat deposits similar to that in females.The liver is the major site for lipogenesis in poultry (Leveille et al., 1975;Donaldson, 1990;Griffin et al., 1992).In this trial, caponization did not influence the weight and relative weight of the liver as there were no differences among the capon, slip and intact males without fatty liver syndrome.The female, on the other hand, possessed the heaviest liver (p<0.05) with fatty liver appearance.When females are in the egg laying period, extra amounts of energy are required.This triggers oestrogen secretion and induces hepatic lipogenesis (Polin and Wolford, 1977;Squires and Lesson, 1988;Hermier et al., 1996).

Lipogenesis and metabolism
Table 3 presents the caponization effect on the blood traits and lipogenic enzymes of Taiwan country chickens.Females and capons showed a higher (p<0.05)MDH (NADP-malic dehydrogenase) activity than intact males.The slip fell in the middle.The other hepatic lipogenic enzymes, CCE (ATP-citrate cleavage enzyme) and G-6-PDH (Glucose-6-phosphate dehydrogenase) were not different (p>0.05)among the capon, slip and intact male.Conversely, the capon showed a higher triacylglycerol and total cholesterol concentration with lower (p<0.05)LDL ratio than intact males, while the slip was in between the two (p>0.05).
The hepatic CCE and MDH activity are positively correlated to fatty acid synthesis (Yeh et al., 1970;Yeh and Leveille 1971).Higher hepatic MDH activity and abdominal fat in females reflected more active lipogenesis in the females (Grunder et al., 1987).The hepatic lipogenic enzyme activity can therefore be an indicator for lipid synthesis in chickens.MDH is the major source of hydrogen from NADPH (Legrand et al., 1987).In this trial, the capon was close to the female in MDH activity (p>0.05) and both were higher than that for intact males (p<0.05).Females, however, showed a lower CCE activity than the other groups (p<0.05).This result agreed with Jiang (1989) in his comparison of female and male Taiwan country chickens, indicating that females showed significantly higher MDH activity with no significant difference with slightly lower trend in CCE activity than intact males.As shown in Table 4, the MDH activity was positively correlated to the abdominal fat deposition (r = 0.582; p<0.01).The serum testosterone concentration influenced MDH synthesis and is negatively correlated with MDH activity (r = -0.43;p<0.01).Caponization decreased the   (Chen et al., 2005b).Hence, the elevated MDH activity was resulted from the lower androgen concentration, or which cooperated to other hormones need further study.Capons showed a higher (p<0.05)triacylglycerol and total cholesterol concentration in their blood constituents over intact males, with the slip in between (p>0.05).The higher MDH activity in capons may be attributed to the increase in hepatic lipogenic activity, leading to higher blood lipid concentrations, i.e., triacylglycerol and total cholesterol, especially extremely high triacylglycerol concentration (as much as three times that in intact males).Because lipoproteins play a major role in lipid transportation and females depend on VLDL (very low density lipoprotein) to transport lipids to the ovary for egg production, hence females showed a higher VLDL concentration (Schneider, 1992(Schneider, , 1995;;Walzem et al., 1994).There are species that show differences in the lipoprotein ratio, higher LDL ratios occur in human beings and higher HDL ratios occur in cockerels and immature female chickens (Chapman, 1980;Hermier et al., 1984;Hermier, 1997).Hermier et al. (1984) indicated that the VLDL and HDL concentrations increased as the body lipid deposition increased.This VLDL concentration is utilized as the fatness selection index in chicken breeding (Whitehead et al., 1984).In this trial, the LDL ratio was lower in capons than in intact males and female (p<0.05).Generally, LDL is derived from VLDL hydrolysation by lipoprotein lipase (LPL) accompanied with a large amount of triacylglycerol from the VLDL content, triacylglycerol is hydrolyzed into NEFA and glycerol is the end product for energy.The lower LDL ratio in capons meant less VLDL was hydrolyzed, and leading to abdominal fat accumulation.

Table 1 .
Caponization effects on the testosterone, performance and appearance of Taiwan country chickens 1

Table 2 .
Caponization effects on carcass traits of Taiwan country chickens 1

Table 3 .
Caponization effects on the blood traits and hepatic lipogenic enzymes of Taiwan country chickens 1 Means of the same row with different superscripts were significantly different (p<0.05).

Table 4 .
Correlation coefficient for comb traits, fat accumulation, the hepatic lipogenic enzymes and testosterone in Taiwan country chickens