Livestock Research for Rural Development 31 (7) 2019 Guide for preparation of papers LRRD Newsletter

Citation of this paper

Growth performance and lipid profile of broilers fed different levels of purple sweet potato extract and raised under different stocking densities

Maulana Hamonangan Nasoetion, Umiyati Atmomarsono, Dwi Sunarti and Nyoman Suthama

Faculty of Animal and Agricultural Sciences, Diponegoro University, Tembalang Campus, Semarang 50275, Central Java - Indonesia
dwisunarti@gmail.com

Abstract

The study was conducted to investigate the effect of feeding different levels of purple sweet potato extract (PSPE) on growth performance and lipid profile of broilers raised under different stocking densities. A total of 288 broiler chicks were used in the study arranged as 3 × 2 factorial design with PSPE inclusion levels (at 0, 25 and 50 ml/kg) and stocking densities (8 and 16 chicks/m2) as main factors. Each treatment consisted of 4 replications with 12 chicks in each. Body weight, feed intake and feed conversion ratio (FCR) was determined at a weekly basis. At day 35, one male and one female chick from each replicate of the treatments were blood sampled, and from which the meat sample was obtained. The interaction between the levels of PSPE and different stocking densities was not observed in respect to all the measured parameters. Dietary incorporation of PSPE particularly at the level of 25 ml/kg improved the growth rate, feed intake and feed efficiency of broiler chickens. Increasing stocking of density decreased low-density lipoprotein (LDL), cholesterol, but increased high-density lipoprotein (HDL) on blood, liver and carcass. Increasing PSPE levels decreased LDL, cholesterol, fat, but increased HDL on blood, liver and carcass. In conclusion, the addition of PSPE in broiler feed improved the growth performance and fatness of broilers rising in low and high stocking densities.

Keywords: broiler, growth, lipid profiles, purple sweet potatoes extract, stocking densities


Introduction

There has been a recent trend that consumers avoid broiler meat in their daily menu. Several issues may bear such trend, some of which are antibiotic residues and high lipid content in broiler meat. With regard to lipid content, consumers believe that broiler meat may pose to coronary heart disease and arteriosclerosis. If not responded appropriately, the latter issue may negatively affect the sustainability of broiler production. Of the efforts to improve the fatness in broiler chickens, nutritional intervention such as feeding selected amino acids (Jiao et al 2010; Andi 2012; Fouad et al 2013), fatty acids (Azman et al 2005; Zhang et al 2007; Zhou 2008) and minerals (Lu et al 2007) as well as increasing the ratio of protein to energy in the diets (Rosa et al 2007) have been conducted. However, the documented data are less consistent since several factors may also influence the lipid profile in broilers such as the environmental factors. Other than nutritional approach, avoiding broilers from stress seems beneficial in reducing the lipid content in broilers (Sugiharto et al 2017a,b). It is generally known that high stocking density is attributable to the compromised growth performance in broiler chickens (Simitzis et al 2012). The high stocking density is also associated with stress and less locomotion of broilers during rearing, resulting in high abdominal fat deposition (Beg et al 2011). Yet, the data reported by the latter authors disagreed with Simitzis et al (2012) showing no effect of stocking density on meat quality and fatness of broilers. Hence, it was essential to confirm the effect of stocking density on the fatness of broilers. Indeed, applying an optimum stocking density is crucial in broiler production as the high stocking density could reduce the space required and thus cost of housing, equipment, and labor (Estevez 2007).

Anthocyanins are the pigments (in glycosylated forms) found in plants belonging to the phenolic group. In poultry, this phytochemical has been exploited to improve the growth performance. Recent study showed that feeding grape pomace (Vitis vinifera) rich in anthocyanins improved the growth performance of broilers (Aditya et al 2018). Feeding such phytochemical also improved nutrient digestibility in broiler chickens (Saputra et al 2016; Aditya et al 2018). In addition to the effect on performance, there has been an increasing interest to use anthocyanins as lipid-improving agents. Liu et al (2016) found that anthocyanins significantly reduced serum triglyceride, total cholesterol, low-density lipoprotein (LDL) cholesterol and increased high-density lipoprotein (HDL) cholesterol in humans with dyslipidemia. Likewise, Khoo et al (2017) documented that feeding anthocyanins reduced the fat content both in humans and animals. Owing to this, it was therefore interesting to include anthocyanins in broiler rations in order to improve the lipid profile of chicks. Among the plants, purple sweet potato is rich in anthocyanins. Study by Hwang et al (2011) showed that treatment with anthocyanin fraction from purple sweet potato was capable of decreasing hepatic triglyceride accumulation in mice. However, to best of our knowledge the study using anthocyanin fraction from purple sweet potato to improve the fatness in broilers remains scarce. This present study aimed to investigate the effect of feeding different levels of PSPE on growth performance and lipid profile of broilers raised under different stocking densities.


Materials and methods

Production of purple sweet potato extract and anthocyanins determination

The fresh tubers of purple sweet potatoes (Figure 1) were purchased from the local market in Semarang city, Central Java Province, Indonesia. The extraction of anthocyanin pigment was done by maceration method in the temperature of 25ºC for 24 hours (Dwiyanti et al 2018). One kg of the purple sweet potato was scraped and added with 0.5 L of water. The mixture was then extorted using two layers of cheesecloth to obtain 1.0 L of PSPE. The concentration of anthocyanins in the PSPE was subsequently determined using UV-Vis Spectrophotometer at 510 nm of wave length. Total anthocyanin concentration measurement was performed by the method according to the pH difference, pH 1.0 using KCl-HCl buffer (0.025 M) and the second solution was for pH 4.5 using Na-Acetate-HCl buffer (0.4 M). Absorbance measurement at a wavelength of 530 nm and 700 nm was done on diluted samples (Dwiyanti et al 2018). In this study, PSPE contained 250 mg/L anthocyanins.

Figure 1. Fresh tubers of purple sweet potatoes
Dietary treatment

Commercial starter feed containing 21.6% crude protein, 6.36% crude fat, 2.98 crude fibers and 4.36% crude ash was provided to broiler chicks during the first week of life. From week-2 onward, the birds were provided with diet containing crude protein of 21 g/kg and metabolizable energy of 3,000 kcal/kg (Table 1). PSPE was added in the expense of feeds.

Table 1. Ingredient and proximate analysis of the experimental diet (as-fed basis)
Feed ingredients %
Maize 54.0
Fish Meal 5.00
Poultry Meat Meal 4.00
Meat Bone Meal 7.00
Rice Bran 9.00
Soybean Meal 20.0
Premix1 1.00
Total 100
Proximate analysis
Crude protein 21.0
Crude fiber 7.93
Metabolism energy (kcal/kg) 3,000
Calcium 1.84
Total phosphorus 0.96
1 The premix provided the following per kilogram of diet: lysine (100 mg), methionine (2,500 mg), sodium salicylate (50,000 IU), vitamin A (5,000 IU), vitamin D3 (5,000 IU), vitamin E (25 IU), vitamin K3 (1 mg), vitamin B1 (20 mg), vitamin B2 (40 mg), vitamin B6 (6 mg), vitamin B12 (20 µg), vitamin C (100 mg), nicotinic acid (150 mg), calcium-D-pantothenic (50 mg), manganese (20 mg), zinc (20 mg), magnesium (50 mg), copper (4 mg), and cobalt (2 mg)
Birds and experimental design

A total of 288 broiler strain Lohmann unsexed chicks were used in the present study. The birds were raised from week-2 to week-5 in a stage house in a tropical zone at temperatures of 25.5-33.7°C and humidity of 61-89%. The study was arranged as 3 × 2 factorial design with PSPE inclusion levels (at 0, 25 and 50 ml/kg) and stocking densities (8 and 16 chicks/m2) as main factors. Each treatment consisted of 4 replications with 12 chicks in each. In the present study, PSPE inclusion at the levels of 0, 25 and 50 ml/kg corresponded to the anthocyanins contents of 0, 6.25 and 12.5 mg/kg feed.

Data collection

The birds were weighed weekly. Likewise, feed intake and feed conversion ratio (FCR) was determined at a weekly basis. At day 35, one male and one female broiler were randomly obtained from each replicate of the treatments. Blood was collected from the jugular vein of each chick and stored in vacuumed capillary tubes to determine the serum HDL and LDL levels. After coagulation, blood samples were centrifuged at 2,000 rpm and then serum was collected and stored at −20°C for later analysis. Blood HDL and LDL levels were determined spectrophotometrically by using commercial kits.

The same birds as blood sampled were subsequently slaughtered, de-feathered, processed (removal of the head and feet), and eviscerated (removal of gastrointestinal tract). Livers and carcasses were stored at 4°C for approximately 6 hours. The carcasses were dissected, and samples from the different portions were collected including breast meat plus the attached skin and thigh meat plus the attached skin. Meat samples were homogenized using a blender with horizontal blades, and samples were frozen and stored in a freezer at −20°C until further analysis. Cholesterol, HDL, and LDL levels were determined spectrophotometrically by using commercial kits. Fat was extracted with ethyl ether using a Soxhlet apparatus (AOAC 1990). Data were analyzed according to factorial ANOVA (with two factors). Differences among means were determined with Duncan’s multiple-range test with 5% level of significance.


Results and discussion

In this study, it was found that dietary incorporation of PSPE particularly at the level of 25 ml/kg improved the growth rate, feed intake and feed efficiency of broiler chickens (Table 2). This present finding was in accordance with Aditya et al (2018) showing a positive impact of feeding grape pomace (Vitis vinifera) rich in anthocyanins on the growth performance of broiler chickens. The reason for the improved growth performance in broiler chickens with feeding PSPE was not definitely known, but the increase in protein intake, protein digestibility and meat protein mass might be responsible for the improvement effect of PSPE on the growth performance of broiler chicks in the present study (Saputra et al 2016). The latter authors also confirmed that feeding of PSPE at the level of 25 ml/kg resulted in better protein digestibility and meat protein mass in broiler chicks as compared to feeding of 50 ml/kg of PSPE. This condition may partly explain why feeding 25 ml/kg PSPE resulted in better growth performance as compared to that of 50 ml/kg PSPE. In this study we did not analyze the anti-nutritional factor contents of PSPE. According to Dako et al (2016) and Mitiku and Teka (2017), PSPE contain anti-nutrition factors such as tannin and phytic acid. This condition may therefore explain the lower growth performance in broiler chicks fed PSPE 50 ml/ kg diets as compared to that of PSPE 25 ml/kg diets.

Table 2. Performance and lipid profile in broilers fed purple sweet potato extract (PSPE) in diets at low and high stocking densities
Variable Purple sweet potato extract (P) Stocking density (D) p
0 25 50 8 16 P D P × D
Performance
Daily gain g, d 47.9 ± 0.542b 50.7 ± 0.65a 48.1 ± 1.31b 48.9 ± 1.40 48.9 ± 1.72 <0.0000 0.9210 0.9827
Feed intake, g/d 79.5 ± 0.951b 81.0 ± 0.453a 81.2 ± 1.28a 80.4 ± 1.08 80.8 ± 1.26 0.0054 0.2621 0.2733
Feed conversion 1.66 ± 0.0302a 1.60 ± 0.0254b 1.69 ± 0.0541a 1.64 ± 0.0433 1.66 ± 0.0632 0.0011 0.6200 0.6628
Blood

LDL, mg/dl

40.9 ± 1.15a 36.2 ± 2.81b 33.9 ± 1.34c 38.3 ± 3.38x 35.7 ± 3.25y <0.0000 0.0002 0.2295

HDL, mg/dl

85.0 ± 1.98c 88.3 ± 2.33b 93.0 ± 2.36a 87.3 ± 4.00y 90.3 ± 3.49x <0.0000 0.0004 0.6105
Abdominal Fat, g/100 g 1.53 ± 0.0703a 1.13 ± 0.119b 1.13±0.0834b 1.30±0.216 1.23±0.212 <0.0000 0.0786 0.1597
Liver

LDL, mg/dl

95.5 ± 2.66a 91.7 ± 2.78b 86.0 ± 2.21c 92.3 ± 4.72x 89.8 ± 4.56y <0.0000 0.0204 0.7133

HDL, mg/dl

104 ± 4.51c 122 ± 4.40b 128 ± 4.00a 116 ± 11.2y 120 ± 11.7x <0.0000 0.0504 0.9119

Fat, g/100 g

3.29 ± 0.159a 3.13 ± 0.143b 3.04 ± 0.124c 3.28 ± 0.134x 3.03 ± 0.108y <0.0000 0.0000 0.3898
Carcass
Cholesterol, mg/100 g 106 ± 5.75a 93.2 ± 6.22b 85.5 ± 6.92c 100 ± 9.18x 89.7 ± 9.43y <0.0000 <.0000 0.8439

LDL, mg/dl

28.9 ± 0.677a 28.0 ± 0.707b 26.6 ± 0.620c 28.14 ± 1.14x 27.5 ± 1.16y <0.0000 0.0157 0.5326

HDL, mg/dl

62.8 ± 1.12c 67.3 ± 1.13b 69.1 ± 0.954a 66.0 ± 2.88y 66.8 ± 2.96x <0.0000 0.0477 0.9487

Fat, g/100 g

5.74 ± 0.214a 5.56 ± 0.190b 5.22 ± 0.178c 5.68 ± 0.244x 5.34 ± 0.228y <0.0000 <0.0000 0.6998
a-c, x,y Means in PSPE and stocking density within rows differ (P<0.05). LDL: low-density lipoprotein, high-density lipoprotein (HDL)

It was apparent in the present study that abdominal fat weight of broilers decreased with administering of PSPE in the diets of broilers (Table 2). Likewise, higher PSPE in feed resulted in decrease in LDL, fat and total cholesterol in the liver and carcass, but increased the HDL levels in the blood, liver, and carcass (Table 2). In line with our data, Liu et al (2014) revealed that anthocyanin from black wolfberry increased the concentration of HDL and effectively reduced the levels of total cholesterol and LDL in the blood of rats. The mechanism by which anthocyanins decreased the body fatness has actually been described in detail by Shah and Shah (2018). They pointed out that anthocyanins down-regulated the HMG-CoA reductase gene activation causing reduced synthesis of cholesterol. Anthocyanins also inhibited the cholesteryl ester transfer protein (CEPT) that may result in reduced concentration of LDL. Moreover, anthocyanins indirectly reduced the apolipoprotein B and apolipoprotein C-III–lipoprotein levels which are prime transporters of TG resulting in lower TG content. Anthocyanin also facilitated the excretion of cholesterol through faeces.

Furthermore, anthocyanins reduced the hepatic lipid metabolism and hence reduce the deposition of fat in the body.

Our present result did not show any effect of stocking density on the growth performance of broilers. This was different from that of reported by Simitzis et al (2012), in which high stocking density alleviated the growth performance in broilers. The exact reason for such discrepancy remains unclear, but the differences in trial conditions such as the environmental condition (temperature and humidity), energy density in diets and body weight of each chick seemed to be responsible.

Data in the present study further demonstrated that higher stocking density decreased the LDL, but increased the HDL concentration in blood, liver and carcass (Table 23). The results of this current study disagreed with Park et al (2018), in which high stocking density increased total cholesterol, triacylglycerol and LDL, while decreased HDL level in the blood of broilers. With regard to HDL, Simsek et al (2009a) reported that high stocking density was attributed to the high level of HDL, which corresponded to our present data. To date, the exact reason for the decreased LDL level with the increased stocking density remains unclear. It has widely been known that high stocking density induces stress responses in broilers (Al-Benna et al 2006). Indeed, stress increased lipid peroxidation resulting in the increased production of malondialdehyde (MDA) (Simsek et al 2009b). In human study, Parthasarathy et al (2010) confirmed that the increased level of MDA may be associated with the increased oxidation ofLDL cholesterol. In light with these above studies, stress-induced by high stocking density may therefore reduce LDL, total cholesterol and fat contents in broiler chickens. It is generally accepted that stress may stimulate lipolysis resulting in less fatness (Rabasa and Dickson 2016). In this basis, it is therefore accepted that stress-induced by high stocking density may be responsible for the increase lipolysis and hence reduce the fatness in broiler chickens. With regard to HDL, the increased level of HDL in broilers raised under high stocking density may reflect the increased need of HDL in transporting cholesterol from the peripherals to the liver to be oxidized for producing the energy (Han et al 2007). The latter condition explained the increased HDL level in broilers raised under higher stocking density.


Conclusions


Acknowledgments

The research was supported by Doctoral Research grants by the Ministry of Research, Technology and Higher Education of the Republic of Indonesia through the Domestic Graduate Scholarship program.


References

Aditya S, Ohh S J, Ahammed M and Lohakare J 2018 Supplementation of grape pomace (Vitis vinifera) in broiler diets and its effect on growth performance, apparent total tract digestibility of nutrients, blood profile, and meat quality. Anim Nutr 4: 210-214, https://doi.org/10.1016/j.aninu.2018.01.004

Al-Benna S, Hamilton C A, Mcclure J D, Rogers P N, Berg G A, Ford I, Delles C and Dominiczak A F 2006 Low-density lipoprotein cholesterol determines oxidative stress and endothelial dysfunction in saphenous veins from patients with coronary artery disease. Arterioscler Thromb Vasc Biol 26(1): 218-223. DOI: 10.1161/01.ATV.0000193626.22269.45 ; PMID: 16254199.

Andi M A 2012 Effects of additional DL-methionine in broiler starter diet on blood lipids and abdominal fat. Afric J Biotechnol, 11: 7579-7581, http://www.academicjournals.org/article/article1380875314_Andi.pdf.

AOAC 1990 Official methods of analysis. 15th ed. Association Official Analytical Chemists, Washington, DC.

Azman M E, Cerci I H and Birben N 2005 Effects of various dietary fat sources on performance and body fatty acid composition of broiler chickens. Turk J Vet Anim Sci, 29: 811-819, https://www.researchgate.net/publication/286654914_Effects_of_different_dietary_fat_sources_on_growth_performances_and_carcass_fatty_acid_composition_of_broiler_chickens

Beg M A H, Baqui M A, Sarker N R and Hossain M M 2011 Effect of stocking density and feeding regime on performance of broiler chicken in summer season. International J Poult Sci 10 (5): 365-375. DOI: 10.3923/ijps.2011.365.375

Dako E, Retta N and Desse G 2016 Comparison of three sweet potato (Ipomoea batatas (l.) Lam) varieties on nutritional and anti-nutritional factors. Global J Sci Frontier Res: D Agric and Vet 16 (4): 63-72. https://pdfs.semanticscholar.org/61c8/0293d9cc811632c40ad096d0d59ebaa9433c.pdf

Dwiyanti G, Siswaningsih W and Febrianti A 2018 Production of purple sweet potato (Ipomoea batatas L.) juice having high anthocyanin content and antioxidant activity. J. Phys.: Conf. Ser. 1013 012194. https://iopscience.iop.org/article/10.1088/1742-6596/1013/1/012194/pdf.

Estevez I 2007 Density allowances for broilers: where to set the limits? Poult Sci 86: 265-272, https://doi.org/10.1093/ps/86.6.1265.

Fouad M, El-Senousey H K, Yang X J and Yao J H 2013 Dietary L-arginine supplementation reduces abdominal fat content by modulating lipid metabolism in broiler chickens. Animal 7:1239-1245. DOI: 10.1017/S1751731113000347. PMID: 23472611.

Han K H, Shimada K, Sekikawa M and Fukushima M 2007 Anthocyanin-rich red potato flakes affect serum lipid peroxidation and hepatic SOD mRNA level in rats. Biosci Biotechnol Biochem 71: 1356–1359. DOI: 10.1271/bbb.70060; PMID: 17485834.

Hwang Y P, Choi J H, Han E H, Kim H G, Wee J H, Jung K O, Jung K H, Kwon K, Jeong T C, Chung Y C and Jeong H G 2011 Purple sweet potato anthocyanins attenuate hepatic lipid accumulation through activating adenosine monophosphate–activated protein kinase in human HepG2 cells and obese mice. Nutrition Research 31:896–906. DOI: 10.1016/j.nutres.2011.09.026 ; PMID: 22153515.

Jiao P, Guo Y, Yang X and Long F 2010 Effect of dietary arginine and methionine levels on broiler carcass traits and meat quality. J Anim Vet Adv 9:1546-1551. DOI: 10.3923/javaa.2010.1546.1551

Khoo H E, Azlan A, Tang S T and Lim S M 2017 Anthocyanidins and anthocyanins: colored pigments as food, pharmaceutical ingredients, and the potential health benefits. Food Nutr Res 61: 1361779. DOI:

Liu C, Sun J, Lu Y and Bo Y 2016 Effects of Anthocyanin on Serum Lipids in Dyslipidemia Patients: A Systematic Review and Meta-Analysis. PLoS ONE 11(9): e0162089. DOI: 10.1371/journal.pone.0162089; PMID: 27589062 PMCID: PMC5010219.

Liu Y, Li D, Zhang Y, Sun R and Xia M 2014 Anthocyanin increases adiponectin secretion and protects against diabetes-related endothelial dysfunction. Am J Physiol Endocrinol Metab 306: E975–E988, https://doi.org/10.1152/ajpendo.00699.2013

Lu L, Luo , Ji C, Liu B and Yu S X 2007 Effect of manganese supplementation and source on carcass traits, meat quality and lipid oxidation in broilers. J Anim Sci 85: 812-822. DOI: 10.2527/jas.2006-229 ; PMID: 17040939.

Mitiku D H and Teka T A 2017 Nutrient and antinutrient composition of improved sweet potato (Ipomea batatas (L) Lam) varieties grown in eastern Ethiopia.  Nutrition & Food Science 47(3): 369-380, DOI: 10.1108/NFS-07-2016-0098

Park B S, Um K H, Park S O and Zammit V A 2018 Effect of stocking density on behavioral traits, blood biochemical parameters and immune responses in meat ducks exposed to heat stress. Arch Anim Breed 61: 425–432, https://www.arch-anim-breed.net/61/425/2018/aab-61-425-2018.pdf

Parthasarathy S, Raghavamenon A, Garelnabi M O and Santanam N 2010 Oxidized Low-Density Lipoprotein. Methods Mol Biol 610: 403–417, DOI: 10.1007/978-1-60327-029-8_24

Rabasa C and Dickson S L 2016 Impact of stress on metabolism and energy balance. Current Opinion in Behavioral Sci 9: 71–77, https://doi.org/10.1016/j.cobeha.2016.01.011

Rosa P S, Faria F D E, Dahlke F, Vieira B S, Macari M and Furlan R l 2007 Effect of energy intake on performance and carcass composition of broiler chickens from two different genetic groups. Braz. J. Poult Sci 9:117-122, http://dx.doi.org/10.1590/S1516-635X2007000200007

Saputra Y, Suthama N and Sukamto B 2016 Supplementation of Purple Sweet Potato Extract on Protein Digestibility and Meat Protein Mass in Broiler Reared Under Different Cage Density, http://dx.doi.org/10.14334/Proc.Intsem.LPVT-2016-p.378-384.

Shah K and Shah P 2018 Effect of Anthocyanin Supplementations on Lipid Profile and Inflammatory Markers: A Systematic Review and Meta-Analysis of Randomized Controlled Trials. Cholesterol Volume 2018, Article ID 8450793, 12 pages https://doi.org/10.1155/2018/8450793

Simitzis P E, Kalogeraki E, Goliomytis M, Charismiadou M A, Triantaphyllopoulos K, Ayoutanti A, Niforou K, Hager-Theodorides A L and Deligeorgis S G 2012 Impact of stocking density on broiler growth performance, meat characteristics, behavioural components and indicators of physiological and oxidative stress. Brit Poult Sci 53(6):721-730. DOI: 10.1080/00071668.2012.745930 ; PMID: 23398415.

Simsek U G, Cerci I H, Dalkilic B, Yilmaz O, and Ciftci M 2009a Impact of stocking density and feeding regimen on broilers: Chicken meat composition, fatty acids, and serum cholesterol levels. J Appl Poult Res 18: 514 – 520, https://doi.org/10.3382/japr.2008-00141

Simsek U G, Dalkilic B, Mehmet D, Mehmet C and Yuce C A 2009b The influences of different stocking densities on some welfare indicators, lipid peroxidation (MDA) and antioxidant enzyme activities (GSH, GSH-Px, CAT) in broiler chickens. J Anim Vet Adv 8(8): 1568-1572, http://medwelljournals.com/abstract/?doi=javaa.2009.1568.1572

Sugiharto S, Yudiarti T, Isroli I, Widiastuti E and Putra F D 2017a Effect of dietary supplementation with Rhizopus oryzae or Chrysonilia crassa on growth performance, blood profile, intestinal microbial population, and carcass traits in broilers exposed to heat stress. Arch Anim Breed 60: 347–356, https://www.arch-anim-breed.net/60/347/2017/aab-60-347-2017.pdf

Sugiharto S, Yudiarti T, Isroli I, Widiastuti E and Kusumanti E 2017b Dietary supplementation of probiotics in poultry exposed to heat stress – a review. Ann Anim Sci (17): 591–604, DOI: 10.1515/aoas-2016-0062, http://eprints.undip.ac.id/64759/1/Ann._Anim.Sci_-_17(3)_591-604__2017.pdf

Zhang G M, Wen J, Chen J L, Zhao G P, Zheng M Q and Li W J 2007 Effect of conjugated linoleic acid on growth performances, carcass composition, plasma lipoprotein lipase activity and meat traits of chickens. Br Poult Sci 48:217-223. DOI: 10.1080/00071660701255841 ; PMID: 17453815.

Zhou J 2008 Effect of dietary conjugated linoleic acid (CLA) on abdominal fat deposition in yellow-feather broiler chickens and its possible mechanism. Asian Australian J Anim Sci 21:1760-1765. DOI: 10.1080/00071660701255841; PMID: 17453815.


Received 8 March 2019; Accepted 22 March 2019; Published 2 July 2019

Go to top