Effects of zinc oxide nanoparticles on growth performance and concentrations of malondialdehyde, zinc in tissues, and corticosterone in broiler chickens under heat stress conditions

Effects of zinc oxide nanoparticles on growth performance and concentrations of malondialdehyde, zinc in tissues, and corticosterone in broiler chickens under heat stress conditions

∗

Institute of Tropical Agriculture and Food Security, Universiti Putra Malaysia, 43400 Serdang, Selangor, Malaysia; † Department of Poultry Production, University of Khartoum, 13314 Khartoum North, Sudan; and ‡ Malaysian Palm Oil Board (MPOB), No. 6 Persiaran Instituti, Bandar Baru Bangi, 43000, Kajang, Selangor, Malaysia ± 1◦ C throughout) or heat stress conditions (34 ± 1◦ C daily for 6 h from 10:00 am until 4:00 pm). From 1 to 42 D of age, the broiler chickens fed 100 mg/kg ZnONPs exhibited lower feed intake and feed conversion ratio than the control. The accumulation of Zn in the liver of broilers was significantly higher among all treatment groups compared to breast and thigh muscle tissues regardless of the temperature conditions. At 40 and 60 mg/kg ZnONPs, the malondialdehyde content increased in thigh muscle of broilers at 7 D postmortem, indicating that ZnONPs potentially inhibited the antioxidant system in muscle tissues. The control and ZnONPs at 40 mg/kg and 60 mg/kg led to low serum corticosterone levels that may be attributed to the antioxidant and antistress properties of Zn. Taken together, although supplementation with ZnONPs at 40 mg/kg and 60 mg/kg alleviated the negative results of heat stress, further research is needed to determine the optimal level of dietary ZnONPs supplementation.

ABSTRACT The use of nanominerals, such as nanozinc, represents a promising and emerging technology in the animal farming industry. Due to the small particle size and bioavailability of nano-zinc, it can be easily assimilated in the digestive system, thereby reducing excretion and environmental pollution. The present study was conducted to assess the effects of zinc oxide nanoparticles (ZnONPs) on the growth performance, zinc (Zn) concentration in edible tissues, thiobarbituric acid reactive substance, and corticosterone concentrations in broilers reared under normal or heat stress environmental conditions. The experiment was performed with a completely randomized design based on a 4 × 2 factorial arrangement consisting of 4 diets (basal diet + 60 mg/kg conventional zinc oxide as control diet; basal diet + 40 mg/kg of ZnONPs; basal diet + 60 mg/kg of ZnONPs; and basal diet + 100 mg/kg of ZnONPs) and 2 environmental conditions (normal and heat stress). On day 22, birds from each dietary group were divided equally to normal temperature (23

Key words: broiler chicken, nanoparticles, TBARS, serum corticosterone, zinc oxide 2019 Poultry Science 0:1–11 http://dx.doi.org/10.3382/ps/pez093

INTRODUCTION

Zinc (Zn) is an important trace element for humans and animals that is involved in numerous metabolic pathways (Salim et al., 2008). Zn cannot be stored in an animal’s body; hence, there is a need for daily supplementation of Zn through the diet (Bao and Choct, 2009). According to NRC (1994), the requirement for Zn in poultry diets ranges between 40 and 75 mg/kg of Zn. Zinc deficiency in animals is characterized by reduced feed intake (FI) and feed utilization, which leads to growth retardation (Ensminger et al., 1990). Zinc supplementation is required in poultry diets during heat stress (Sahin and Kucuk, 2003). However, previously published studies on the effect of dietary Zn supplementation on performance of heat-stressed birds have been inconsistent. Zinc supplementation exhibits a positive effect on growth performance of heat-stressed broiler chickens (Rao et al., 2016) and Japanese quail (Sahin

Chickens are highly susceptible to heat stress and have a narrow thermal comfort zone. The difficulty chickens experience in balancing heat loss and production is due to the lack of sweat glands and feathering (Sahin et al., 2009) In tropical regions, such as Malaysia, high environmental temperatures cause heat stress in poultry that leads to detrimental effects on growth rate, feed consumption, feed efficiency, and mortality, subsequently resulting in a large economical loss in commercial poultry farms (Rossi et al., 2007; Rao et al., 2016).

 C 2019 Poultry Science Association Inc. Received October 29, 2018. Accepted February 8, 2019. 1 Corresponding author: s [email protected]

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Suriya Kumari Ramiah,∗,1 Elmutaz Atta Awad,∗,† Saminathan Mookiah,‡ and Zulkifli Idrus∗

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RAMIAH ET AL.

MATERIALS AND METHODS Chickens, Housing, Diets, and Experimental Design A total of 240 1-day-old male broiler chicks (Cobb 500) were obtained from a commercial hatchery and randomly allotted to 48 battery cages (120 × 60 × 45 cm; length × width × height) with wire floors in six identical environmentally controlled chambers. Each chamber measured 9.10 × 3.80 × 2.30 m, and the temperature of the chambers were maintained at 32 ± 1◦ C on day 1 followed by a gradual reduction to approximately 23 ± 1◦ C on day 21. On day 1, 48 cages were randomly assigned to 4 dietary groups: a basal diet with 60 mg/kg ZnO (Peterlabs, Malaysia) based on the recommended amount stated in the (NRC, 1994) (control); basal diet +40 mg/kg ZnONPs (ZnONPs 40); basal diet +60 mg/kg ZnONPs (ZnONPs 60), and basal diet +100 mg/kg ZnONPs (ZnONPs 100). From days 1 to 21 (starter period), there were 2 replicates per diet in each chamber, resulting in a total of 12 replicates (5 birds each) during the starter period. The basal diet was formulated to maintain the nutrient requirements of broilers during the starter and finisher (day 22 to 42) periods (Table 1). Feed (mash form) and drinking water were provided ad libitum. NanoZnO was purchased from the US Research Nanomaterials, Inc. (Houston, USA). The purity of ZnONP was 99%. Heat treatment started on day 22 when birds from each dietary group were either subjected to normal or heat stress environmental conditions. Thus, during the finisher period, there were 4 diets × 2 temperatures with 6 replicates of 5 chickens per diet-temperature subgroup. The experimental animals received humane care as outlined in the Guide for the Care and Use of Experimental Animals (Research Policy, University Putra Malaysia) under Animal Ethical Code number UPM/AICUC/AUP-R040/2017.

Heat Challenge To elicit heat stress from days 22 to 42, 6 cages from each dietary treatment (3 chambers) were randomly assigned to heat stressed (34 ± 1◦ C) daily for 6 h from 10:00 am until 4:00 pm, whereas the temperature in the remaining chambers was maintained at 23 ± 1◦ C (normal temperature) throughout the experiment, resulting in 8 treatment subgroups (4 diets × 2 temperatures) from day 22 until 42. The time required for the temperature to increase from 23 to 34◦ C was approximately 30 min. Throughout the experiment, the relative humidity ranged from 75 to 90%.

Growth Performance and Sample Collection Average body weights and FI were recorded for the starter (day 1 to 21), finisher (day 22 to 42), and

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et al., 2005; SM and Gh, 2014). In contrast, dietary Zn supplementation had no effect on the performance of heat-stressed broilers (Smith, 2003). High dietary zinc oxide (ZnO) exhibits reduced digestibility; hence, high amounts of Zn are excreted into the manure causing environmental pollution (Swain et al., 2016; Wang et al., 2017). Zinc oxide nanoparticles (ZnONPs), as an alternative to the conventional zinc sources, represent a good alternative in livestock feeding. The usage of ZnONPs has gained attention due to the larger surface area, higher surface activity and catalytic efficiency, and stronger adsorbing quality compared with the conventional use of Zn (Safaei-Ghomi et al., 2013). ZnONPs at levels of 30 to 90 mg per kg improved broilers’ growth performance (Ahmadi et al., 2013). Zhao et al. (2014) reported that supplementation of nano-zinc in broilers at 20, 60, and 100 ppm significantly improved the feed conversion and growth rate compared with the control group (60 mg/kg ZnO). The distribution of nanominerals in the body is greater than inorganic and organic minerals due to its high bioavailability that allows nanominerals to pass through the small intestine (Hillyer and Albrecht, 2001). Tissue mineral bio distribution can be used as an index of mineral storage in the body (Wedekind et al., 1992). The predominant deposition site for Zn is in legs and breast chicken meat as reported by Stef and Gergen (2012). In addition, the liver is also known as a deposit site for trace minerals, including Zn (EKMEKCI˙ et al., 2003) in chickens. ZnONPs introduced by oral exposure in mice were retained in the liver after 14 D of subacute exposure (Sharma et al., 2012). Kikusato and Toyomizu (2013) and Mujahid et al. (2005) reported that the production of reactive oxygen species from the mitochondria resulted in skeletal muscle oxidative damage in meat-type chickens in response to acute heat stress. Heat challenge caused increased excretion of minerals, such as Zn, which act as cofactors for antioxidant enzymes (Sahin and Kucuk, 2003). Metallothionein (MT), a Zn binding protein, is an effective scavenger of hydroxyl radicals that protect against immune-mediated free radical attack (Shaheen and El-Fattah, 1995). The hypothalamicpituitary-adrenal (HPA) axis mediates secretion and release of corticosteroids from the adrenal gland in response to stressful stimuli or homeostatic disturbances (McEwen, 2000; Ritchie, 2014). Extensive research has shown that the elevation of plasma corticosterone levels is a reliable indicator of stress in avian species as reported by Najafi et al. (2015) and Zulkifli et al. (2003). Hence, this study was designed in an attempt to examine the effects of ZnONPs on the growth performance, Zn content in tissues, malondialdehyde (MDA), and serum corticosterone concentrations in broiler chickens reared under normal or heat stress conditions.

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NANO ZINC OXIDE, BROILERS, AND HEAT STRESS Table 1. Composition of the basal diet during the starter and finisher periods. Item

Finisher (day 22 to 42)

54.05 2.70 32.9 3.30 3.10 1.81 0.95 0.42 0.07 0.10 0.25 0.24 0.04 0.07

58.21 2.50 30.4 0.00 5.20 1.47 0.82 0.40 0.05 0.10 0.21 0.05 0.55 0.04

Nutrient composition (%DM, unless stated otherwise)2 Crude protein 22.00 Metabolizable energy (kcal/kg) 3080 Crude fat 7.27 Phosphorus 0.45 Calcium 1.00 Methionine 0.55 Lysine 1.20 Na 0.20

20.5 3150 7.50 0.42 0.90 0.50 1.00 0.15

1 Premixes contributed the following nutrients per kilogram of complete feed: Vitamin A, 2300 IU; vitamin D3 , 400 IU; vitamin E, 1.8 mg; vitamin B12 , 3.5 mg; Riboflavin, 1.4 mg; Panthotenic Acid, 2 mg; Nicotinic Acid, 7 mg; Pyridoxine, 0.25 mg; Folic Acid, 0.15 mg; Menadione, 0.3 mg; Thiamin, 0.15 mg; Manganese Oxide, 35 mg; Ferrous Sulfate 35 mg; Copper Sulfate, 60 mg; Cobalt Carbonate, 5 mg; Potassium Iodine, 0.6 mg; Selenium Vanadate, 0.09 mg. Mineral premix was free of zinc. 2 Calculated values.

overall (day 1 to 42) experimental periods. Weight gain (WG) and feed conversion ratios (FCR) (feed/gain) of each group of birds were calculated accordingly. The FI data were corrected for mortalities. At the end of the experiment (day 42), 10 birds from each group were randomly selected and slaughtered for blood, liver, breast, and thigh samples collection, and samples were stored at −80◦ C until further analysis. The birds were slaughtered according to the halal slaughter method (Farouk et al., 2014), which was performed by severing the jugular veins, carotid arteries, trachea, and the esophagus.

Zinc Concentration The technique to obtain zinc concentrations in the liver, breast, and thigh samples was adapted from Stef and Gergen (2012). A total of 10 samples of each tissue (liver, breast, and thigh) from each treatment subgroup were obtained. Briefly, samples were dried in an oven at 105◦ C for 24 h and then digested in the Muffle furnace. The temperature was increased to 550◦ C until white ash formed. The ash was dissolved in 0.5 N nitric acid (HNO3 ) and filtered through ash-free filter paper. Each sample solution was comprised of dilute HNO3 (0.5 N) to a final volume of 50 ml and analyzed using flame atomic absorption spectrometry.

Thiobarbituric Acid Reactive Substance Assay Immediately after slaughter and processing, iliotibialis lateralis muscle (thigh muscle) was collected from 10 birds of each treatment group for the determination of lipid peroxidation or MDA content. The muscle samples were stored in a 4◦ C refrigerator before being snap frozen in liquid nitrogen and stored in −80◦ C for 2-thiobarbituric acid reactive substance (TBARS) evaluation to determine the MDA concentration at 0, 1, 3, and 7 D post storage. The MDA determination was based on a method adapted by Abdulla et al. (2015) and revised by Kumari Ramiah et al. (2014). One gram of thigh sample was homogenized in 4 ml 0.15 M KCl (potassium chloride) + 0.1 mM butylated hydroxytoluene. Then, 200 μl of the homogenized sample was extracted and mixed with 2 ml of thiobarbituric acid solution. Then, the mixed samples were placed in a water bath at 95◦ C for 60 min until pale red pigment developed. Then, the samples were cooled to room temperature under running water. Next, 3 ml of n-butanol was added, and the sample was vortexed for 60 s. The mixture was then centrifuged at 4000 rpm for 15 min, and the supernatant was extracted. MDA levels were determined colorimetrically using a spectrophotometer against pure n-butanol.

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Ingredient composition (%) Corn Wheat bran Soybean meal Gluten meal Palm oil Dicalcium phosphate Limestone Salt (NaCl) Vitamin premix1 Mineral premix1 DL-Methionine L-Lysine HCl L-Threorine Choline CI (70%)

Starter (day 1 to 21)

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RAMIAH ET AL.

Corticosterone Assay

Statistical Analysis All the data were analyzed using the general linear model (GLM) procedure of Statistical Analysis System (SAS Institute, Inc., Cary, NC, USA) software (SAS, 2005). Growth parameters (FI, WG, and FCR) during the starter period were subjected to 1-way ANOVA using PROC GLM, and the diet was fixed as the main effect. Mortality rate data were subjected to chisquare analysis. The data of growth performance during the finisher and overall periods, Zn content in tissues, TBARS, and corticosterone concentrations were analyzed using diet, heat treatment, and their interaction as main effects. When interactions between main effects were significant, comparisons were made within each experimental variable. Separate statistical analyses were performed to investigate the effect aging on TBARS and the effect of tissue sample (liver, breast, and thigh) on Zn concentration. Tukey’s test was used for comparisons between the means. The results were considered statistically significant at P ≤ 0.05.

RESULTS Data on the effects of dietary supplementation with ZnONPs on growth-performance parameters and mortality rates of broilers raised at normal temperature or heat stress condition are presented in Table 2. ZnONPs supplementation had no effect (P > 0.05) on WG, FI, or FCR during the starter period. No significant interaction (P > 0.05) was noted between diet and temperature for WG, FI, or FCR during the finisher and overall periods. Regardless of temperature, ZnONPs supplementation at 100 mg/kg significantly decreased FI during the finisher (P < 0.001) and overall (P = 0.003) periods compared with the control diet without affecting the WG. ZnONPs supplementation at 100 mg/kg exhibited a strong trend in improving the FCR during the overall period (P = 0.051) but not during the finisher period (P > 0.05). Regardless of diet, heat stress significantly (P < 0.01) reduced the FI and WG and increased the FCR during both the finisher and overall periods. Neither diet nor temperature had a significant effect on the mortality rate of broiler chickens. Data on Zn concentrations in breast and thigh muscles and liver tissues of broilers as affected by feeding with ZnONP-supplemented diets under normal or heat stress conditions are presented in Table 3. Regardless of dietary group and temperature, liver tissues retained the highest (P < 0.001) Zn concentration compared with thigh and breast muscles. Significant diet

DISCUSSION The role of the micronutrients zinc in animal health is well documented (El-Masry and Nasr, 2010; Liu et al., 2011). This nutrient cannot be stored in the body; therefore, regular dietary intake of Zn is required to meet functionality requirements (Swain et al., 2016). According to Sandoval et al. (1998), high utilization of Zn is the largest issue in animal diets given that high Zn deposition in the stool severely contaminates the

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Corticosterone concentration was determined using a commercial high-sensitivity EIA kit (IDS Ltd., Bolton, UK). The intra- and inter-assay variations for corticosterone measurements were <7% and <9%, respectively, and the sensitivity was 0.17 ng/mL. The assay was performed according to the manufacturer’s information.

× temperature interactions were noted for Zn concentrations in thigh muscle (P = 0.041) and liver (P = 0.029). Diet had no effect (P = 0.646) on Zn concentration in the liver under normal temperature (Table 4). Under heat stress conditions, feeding birds with the ZnONP 40 diet resulted in significantly (P = 0.007) lower Zn concentrations in liver tissues compared with other diets. Nevertheless, in those birds fed ZnONPsupplemented diets, the zinc concentrations in thigh muscle were significantly (P < 0.05) increased under normal temperatures compared with heat stress conditions. However, the zinc concentration in thigh muscle was reduced with 100 mg/kg ZnONP compared with lower levels of ZnONPs. The effects of different levels of ZnONPs at different temperatures on MDA concentration in thigh muscle are presented in Table 5. The MDA concentrations were low on day 7 in the 100-mg/kg ZnONPs (P < 0.05) group. MDA concentrations in thigh muscle of broiler chickens are significantly increased under heat stress compared with normal temperature on day 1 and 7. Significant interactions were noted between diet × temperature on ZnONPs of MDA concentration in thigh muscles on day 0 and 7 as shown in Table 6. On day zero, the MDA concentrations were significantly reduced in heat-stressed birds compared with birds maintained at normal temperature and fed 60 mg/kg ZnONPs. However, at 0 day, the ZnO groups exhibited higher MDA concentrations in heat-challenged birds compared with unchallenged counterparts. On day 7, the MDA concentrations in the control group and 100-mg/kg ZnONPs group exhibited no difference regardless of temperature. Chickens fed diets with 40 and 60 mg/kg ZnONPs under heat stress condition had higher MDA concentrations compared to those kept at normal temperature. However, the MDA concentrations were significantly and gradually reduced with 40 and 60 mg/kg ZnONPs on day 7 in both conditions (P < 0.05). Table 7 presents the effects of dietary supplementation with ZnONPs on circulating corticosterone levels of broilers subjected to normal temperature or heat stress conditions. Significant diet × temperature interactions (P < 0.001) were noted for corticosterone as diet affected corticosterone concentration under heat stress but not under normal temperature (P = 0.215) (Table 8). Under heat stress conditions, the corticosterone level of birds fed a diet with 100 mg/kg ZnONPs was significantly increased (P < 0.001) compared with birds fed other diets.

Diet1 Control ZnONPs 40 ZnONPs 60 ZnONPs 100 SEM2

NA

0.734 NA 0.342

< 0.001 0.002

3,520a 3,297b 276

3,561a 3,519a 3,391a 3,162b 258

Finisher (day 22 to 42)

Feed intake (g/bird)

0.526

0.003 0.002

4,768a 4,529b 285

4,807a 4,747a 4,624a,b 4,417b 276

Overall (day 1 to 42)

NA

0.178 NA

NA NA –

918 946 960 914 60

Starter (day 1 to 21)

0.488

0.917 < 0.001

1,724a 1,477b 146

1,615 1,601 1,611 1,575 197

Finisher (day 22 to 42)

Weight gain (g/bird)

0.509

0.549 < 0.001

2,672a 2,398b 139

2,533 2,547 2,571 2,489 199

Overall (day 1 to 42)

NA

0.091 NA

NA NA –

1.29 1.24 1.23 1.30 0.09

Starter (day 1 to 21)

0.368

0.128 0.008

2.06b 2.24a 0.21

2.23 2.23 2.11 2.03 0.26

Finisher (day 22 to 42)

FCR (feed/gain)

0.197

0.052 0.009

1.76b 1.86a 0.11

1.87a 1.84a,b 1.77a,b 1.75b 0.12

Overall (day 1 to 42)

1

a,b

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> 0.05 > 0.05

10.0 16.7 6.80

16.7 16.7 11.7 8.30 8.16

Finisher (day 22 to 42)

Mortality (%)

Means within a column-subgroup with no common superscripts are significantly different at P < 0.05. Control (zinc oxide, ZnO): basal diet without ZnONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZnONPs 40: basal diet + 40 mg/kg of ZnONPs; ZnONPs 60: basal diet + 60 mg/kg of ZnONPs; ZnONPs 100: basal diet + 100 mg/kg of ZNONPs. 2 SEM = Standard error of the mean for diet effect (n = 12). 3 Equal numbers of birds from each diet were subjected to either 23±1◦ C throughout (normal temperature) or 34±1◦ C for 6 h per day (heat stress) from 22 to 42 days of age. 4 SEM = Standard error of the mean for temperature effect (n = 24). NA = not applicable.

ANOVA (P-value) Diet Temperature (Temp) Diet × Temp

NA NA –

1,246 1,227 1,233 1,255 64

Treatment

Temperature3 Normal Heat stress SEM4

Starter (day to 21)

Table 2. Effects of dietary zinc oxide nanoparticles (ZnONPs) supplementation and temperature on feed intake, weight gain, feed conversion ratios (FCR), and mortality in broiler chickens from 1 to 42 D of age.

NANO ZINC OXIDE, BROILERS, AND HEAT STRESS

5

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RAMIAH ET AL. Table 3. Effects of dietary ZnONPs supplementation and temperature on zinc concentrations (mg/kg) in breast, thigh, and liver of broiler chickens at 42 D of age. Treatment

Thigh

Liver

SEM

P-value

2.78B 2.53B 2.65B 2.55B 0.74

2.46B 2.66B 2.78B 2.42B 0.92

9.01A 7.23A 8.23A 9.01A 3.19

1.69 1.75 1.74 2.56

< 0.001 < 0.001 < 0.001 < 0.001

2.82a,B 2.44b,B 0.71

2.18b,B 2.97a,B 0.83

8.67A 7.85A 3.20

1.87 2.03

< 0.001 < 0.001

0.662 0.019 0.257

0.448 < 0.001 0.041

0.308 0.233 0.029

a,b Means within a column-subgroup with no common superscripts are significantly different at P < 0.05. A,B Means within a row with no common superscripts are significantly different at P < 0.05. 1 Control (ZnO): basal diet without ZnONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZnONPs 40: basal diet + 40 mg/kg of ZnONPs; ZnONPs 60: basal diet + 60 mg/kg of ZnONPs; ZnONPs 100: basal diet + 100 mg/kg of ZnONPs. 2 SEM = Standard error of the mean for diet effect (n = 20). 3 Equal numbers of birds from each diet were subjected to either 23 ± 1◦ C throughout (normal temperature) or 34 ± 1◦ C for 6 h per day (heat stress) from 22 to 42 D of age. 4 SEM = Standard error of the mean for temperature effect (n = 40).

Table 4. Zinc concentration (mg/kg) in thigh muscle and liver at 42 D of age when interactions between diet and temperature were significant. Diet1 Temperature

2

Thigh muscle Heat stress Normal SEM3 P-value Liver Heat stress Normal SEM3 P-value

Control (ZnO)

ZnONP40

ZnONPs 60

ZnONPs 100

SEM3

P-value

2.49 2.42 0.94 0.8542

1.99y 3.32x 1.04 0.0107

2.25y 3.31x 0.68 0.0025

1.99y 2.85x 0.42 0.0002

0.67 0.91

0.307 0.098

10.24a,x 6.89y 2.14 0.003

5.98b,y 8.48x 2.37 0.029

8.96a 7.50 2.78 0.254

9.50a 8.52 4.41 0.627

2.71 3.37

0.007 0.646

Means within a row with no common superscripts are significantly different at P < 0.05. Means within a column with no common superscripts are significantly different at P < 0.05. 1 Control (ZnO): basal diet without ZnONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZnONPs 40: basal diet + 40 mg/kg of ZnONPs; ZnONPs 60: basal diet + 60 mg/kg of ZnONPs; ZnONPs 100: basal diet + 100 mg/kg of ZnONPs. 2 Equal numbers of birds from each diet were subjected to either 23±1◦ C throughout (normal temperature) or 34 ± 1◦ C for 6 h per day (heat stress) from 22 to 42 D of age. 3 SEM = Standard error of the mean for diet × temperature effect (n = 10). a,b x,y

environment. There is a growing interest in the application of nanotechnology to improve the utilization efficiency of trace elements in diets (Ahmadi and Rahimi, 2011; Al-Beitawi et al., 2017). The application of ZnONPs can be a good alternative in animal livestock feeding as a substitute to conventional Zn sources. However, the efficacy of ZnONPs in broiler growth under high ambient temperature is rarely reported. The current study showed that the body weight gain of broiler chickens fed ZnONPs exhibited no statistical changes from 1 to 42 D of age. Fathi et al. (2016) reported that 20 mg/kg ZnONPs exhibited an effect on body weight gain and provided a better FCR compared with other groups. In the same study, no significant effects were observed in body weight and

the FCR of broiler chickens fed 40 mg/kg ZnONPs. Although studies have demonstrated that appropriate concentrations of ZnONPs are better than conventional organic ZnO for improving the efficiency of feed utilization and growth performance in broilers, excess ZnONPs may have a toxic effect and thus inhibit broiler growth (Zhao et al., 2014). In the present study, FI was substantially reduced with decreased ZnONP feeding dose during the finisher and overall periods. Our study is consistent with Ahmadi et al. (2013), who reported that the FI was significantly decreased with 60 and 90 mg/kg ZnONPs. In this study, the absence of a response in body weight or FI in ZnONP diets may be due to increased synthesis of intestinal metallothionein (Jahanian et al., 2008). Zn intake induced the

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Diet1 Control ZnONPs 40 ZnONPs 60 ZnONPs 100 SEM2 Temperature3 Normal Heat stress SEM4 ANOVA (P-value) Diet Temperature (Temp) Diet × Temp

Breast

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NANO ZINC OXIDE, BROILERS, AND HEAT STRESS Table 5. Effects of dietary ZnONPs supplementation and temperature on concentrations of malondialdehyde in thigh of broiler chickens at 42 D of age. TBARS (mg MDA5 /kg thigh meat) Treatment

Day 0

Day 7

SEM

P-value

4.52b,c,B 4.06c,B 5.77a,b 6.30a,B 2.33

7.12a,b,A 8.18a,b,A 6.51b 8.64a,A 3.43

7.67a,A 7.61a,A 4.81b 4.33b,C 2.88

3.30 3.03 2.45 2.64

0.009 < 0.001 0.195 < 0.001

4.94C 5.33B 2.46

9.19a,A 6.04b,A,B 3.11

6.96a,B 5.32b,B 3.14

2.93 2.90

< 0.001 0.029

0.006 0.386 0.002

< 0.001 0.009 0.046

0.111 < 0.001 0.253

a–c Means within a column-subgroup with no common superscripts are significantly different at P < 0.05. A–C Means within a row with no common superscripts are significantly different at P < 0.05. 1 Control (ZnO): basal diet without ZnONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZnONPs 40: basal diet + 40 mg/kg of ZnONPs; ZnONPs 60: basal diet + 60 mg/kg of ZnONPs; ZnONPs 100: basal diet + 100 mg/kg of ZnONPs. 2 SEM = Standard error of the mean for diet effect (n = 20). 3 Equal numbers of birds from each diet were subjected to either 23 ± 1◦ C throughout (normal temperature) or 34 ± 1◦ C for 6 h per day (heat stress) from 22 to 42 D of age. 4 SEM = Standard error of the mean for temperature effect (n = 40). 5 MDA = malondialdehyde

Table 6. Thiobarbituric acid reactive substances (TBARS, mg MDA5 /kg thigh meat) in thigh at 42 D of age when interactions between diet and temperature were significant. Diet1 Temperature2 Day 0 Heat stress Normal SEM3 P-value Day 7 Heat stress Normal SEM3 P-value

Control (ZnO)

ZNONPs 40

ZNONPs 60

ZNONPs 100

SEM3

P-value

5.79x 3.26b,y 2.33 0.0258

4.10 4.01b 1.72 0.9083

4.61y 6.94a,x 1.63 0.0049

5.31 7.29a 2.79 0.1507

2.22 2.08

0.356 < ..001

8.12a,b 7.23a 3.56 0.582

9.52a,x 5.69a,b,y 2.53 0.003

6.15b,c,x 3.47c,y 2.69 0.051

3.96c 4.71b,c 1.51 0.277

3.11 2.15

0.002 0.004

Means within a row with no common superscripts are significantly different at P < 0.05. Means within a column with no common superscripts are significantly different at P < 0.05. 1 Control (ZnO): basal diet without ZNONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZNONPs 40: basal diet + 40 mg/kg of ZNONPs; ZNONPs 60: basal diet + 60 mg/kg of ZNONPs; ZNONPs 100: basal diet + 100 mg/kg of ZNONPs. 2 Equal numbers of birds from each diet were subjected to either 23 ± 1◦ C throughout (normal temperature) or 34 ± 1◦ C for 6 h per day (heat stress) from 22 to 42 D of age. 3 SEM = Standard error of the mean for diet × temperature effect (n = 10). a–c x,y

intestinal metallothionein synthesis (Sandoval et al., 1998). The increased synthesis of intestinal metallothionein is associated with reduced zinc absorption (Jahanian et al., 2008). Our results are consistent with the general trend observed in heat-stressed broilers ¨ on decreased FI (Ozkan et al., 2003; Aljubori et al., 2017). To increase the survival rate under high ambient temperature, reduced FI is associated with lower metabolic heat production in broiler chickens (Li et al., 1992). The low FCR of chickens fed 100 mg/kg ZnONP may be attributed to increased metabolic efficiency associated with maintaining a smaller body weight

compared with control and other dietary ZnONPs groups. Supplementing ZnONP trace elements into animals’ diets could modify mineral deposition given their high bioavailability compared with inorganic sources (Ibrahim et al., 2017). Zn levels of the breast, thigh muscles, and liver in chickens were significantly increased by dietary inclusion of Zn (Akbari Moghaddam Kakhki et al., 2017). Liu et al. (2011) reported increased Zn concentrations in the liver, muscle, and breast supplemented with Zn in broiler chickens regardless of Zn source. In our study, regardless of temperature, the

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Diet1 Control (ZnO) ZnONPs 40 ZnONPs 60 ZnONPs 100 SEM2 Temperature3 Heat stress Normal SEM4 ANOVA (P-value) Diet Temperature (Temp) Diet × Temp

Day 1

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RAMIAH ET AL.

Table 7. Effects of dietary ZNONPs supplementation and temperature on serum corticosterone concentration (ng/mL) of broiler chickens at 42 D of age. Treatment

Corticosterone

1

2.63b 3.96b 2.86b 6.44a 3.88 6.15a 1.79b 3.49 < .001 < .001 < .001

a,b Means within a column-subgroup with no common superscripts are significantly different at P < 0.05. 1 Control (ZnO): basal diet without ZNONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZNONPs 40: basal diet + 40 mg/kg of ZNONPs; ZNONPs 60: basal diet + 60 mg/kg of ZNONPs; ZNONPs 100: basal diet + 100 mg/kg of ZNONPs. 2 SEM = Standard error of the mean for diet effect (n = 20). 3 Equal numbers of birds from each diet were subjected to either 23 ± 1◦ C throughout (normal temperature) or 34 ± 1◦ C for 6 h per day (heat stress) from 22 to 42 D of age. 4 SEM = Standard error of the mean for temperature effect (n = 40).

accumulation of Zn in the liver of broiler chickens was significantly higher among all treatment groups compared with breast and thigh muscle. This observation is supported by the accumulation of Zn in liver of chickens supplemented with graded levels of Zn sulfate (range 0 to 320 ppm; Sunder et al., 2008). Similarly, Wang et al. (2017) demonstrated increased Zn concentrations in the livers of piglets fed ZnONPs (1,200 mg/kg) and ZnO (3,000 mg/kg) with colistin sulfate. Regarding Zn, the results are consistent with the model for aquatic animals, which demonstrates that muscle tissues exhibit low metabolic activities, whereas the liver is an organ in the body that processes blood and helps to remove unwanted substances (Gundo˘ gdu et al., 2009). In addition, another theory that supports the differences in the accumulation of Zn in the liver may be the activity of metallothionein, a cysteine-rich protein with the ability to bind divalent cations and control the pool

Table 8. Corticosterone concentration (ng/mL) in serum of broilers at 42 D of age when interactions between diet and temperature were significant. Diet1 Temperature2

Control

ZnONPs 40

ZnONPs 60

ZnONPs 100

SEM3

P-value

Heat stress Normal SEM3 P-value

3.86b,x 1.39y 1.14 < 0.001

6.56b,x 1.36y 1.98 < 0.001

3.44b 2.28 1.65 0.133

10.74a,x 2.14y 5.05 0.001

3.90 1.23

< 0.001 0.215

Means within a row with no common superscripts are significantly different at P < 0.05. Means within a column with no common superscripts are significantly different at P < 0.05. Control (ZnO): basal diet without ZnONPs supplementation but with inclusion of 60 mg/kg conventional ZnO; ZnONPs 40: basal diet + 40 mg/kg of ZnONPs; ZnONPs 60: basal diet + 60 mg/kg of ZnONPs; ZnONPs 100: basal diet + 100 mg/kg of ZnONPs. 2 Equal numbers of birds from each diet were subjected to either 23 ± 1◦ C throughout (normal temperature) or 34 ± 1◦ C for 6 h per day (heat stress) from 22 to 42 D of age. 3 SEM = Standard error of the mean for diet × temperature effect (n = 10). a–b x,y 1

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Diet Control ZNONPs 40 ZNONPs 60 ZNONPs 100 SEM2 Temperature3 Heat stress Normal SEM4 ANOVA (P-value) Diet Temperature (Temp) Diet × Temp

and turnover of the microelements (Coyle et al., 2002). Another theory that may support the above results indicates that Zn in the form of nanoparticles is able to penetrate into the hepatic cells via blood or interstitial space. The increased uptake and interaction with biological tissues due to the size of the nanoparticles was reduced in the transitional zone between individual atoms or molecules and the corresponding bulk materials (Nel et al., 2006). In the present study, we observed that Zn concentrations were increased in breast muscle but decreased in thigh muscle during heat stress. Saleh et al. (2018) illustrated that the breast muscle Zn concentration in chickens fed with Zinc-methionine increased during heat stress, which is similar to our study. Akbari Moghaddam Kakhki et al. (2017) postulated that compared with breast muscle, the thigh muscle responded positively to dietary Zn supplementation, which is comparable to our study. Nevertheless, the differences of Zn concentrations in both muscle tissues are difficult to explain because Zn muscle concentrations vary based on morphology, biochemical status, and functionality, especially during heat stress. Variations are noted in muscle tissues that mainly consist of a large amount of mitochondria and altered the actions of oxidative and degradative enzymes that affect protein synthesis (J´ o´zwik et al., 2018). Chickens fed 100 mg/kg ZnONPs exhibited a higher Zn concentration in their diet but reduced deposition of Zn in the thigh muscle compared with lower level of ZnONPs. This finding may be attributed to a decrease in FI in chicken fed 100 mg/kg ZnONPs (Wedekind et al., 1992). In response to acute heat stress in broiler chickens, the elevated glutathione peroxidase (GSH-Px) but decreased superoxide ismutase (SOD) and catalase (CAT) activities in thigh muscle and decreased SOD and CAT activities with unchanged GSH-Px in breast muscle indicated a tissue-specific response in the antioxidative enzymatic system (Huang et al., 2007). Increased GSH-Px activities may be an adaptive mechanism secondary to the increase of oxidative stress (Zhu et al., 2006). Consistent with this notion, the thigh muscle was significantly different on TBARS analysis in the present study. In the current study, at day 0, the

NANO ZINC OXIDE, BROILERS, AND HEAT STRESS

tal in broiler production, especially under heat stress conditions. The relationship between diet and serum corticosterone levels has received considerable attention given that ZnONPs reduced serum corticosterone levels under heat stress conditions in chickens fed 40 to 60 mg/kg ZnONPs compared with 100 mg/kg ZnONPs. The impact of zinc on growth performance is not completely understood; hence, further research should be conducted to identify the optimal levels of ZnONPs that can provide better performance and economic benefits.

ACKNOWLEDGMENTS The authors would like to express gratitude to all staff from Laboratory of Animal Production and Sustainable Biodiversity, Institute of Tropical Agriculture and Food Security (ITAFoS) for their support.

AUTHORS’ CONTRIBUTIONS All authors contributed equally to this work.

FUNDING This research is supported by the Ministry of Higher Education Malaysia through Higher Institutions Centres of Excellence (HiCoE) grant and Universiti Putra Malaysia.

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lower MDA content at 60 mg/kg ZnONPs is may be due to high Zn content in the thigh muscle. MT synthesis is promoted by Zn, acts in detoxifying and antioxidant systems, such as SOD, and subsequently reduces the usage of GSH-Px (Akbari Moghaddam Kakhki et al., 2017). In contrast, MDA levels in serum and hepatic tissues were significantly reduced in birds fed 20 to 100 mg/kg ZnONPs compared with the control group (60 mg/kg ZnO; Zhao et al., 2014). Consistent with our data, as MDA increased by day, exposure of ZnONPs at 40 and 60 mg/kg in the thigh muscle at 7 D may have led to a reduction of antioxidant enzymes, such as SOD, CAT, and GSH-Px. These findings indicate that ZnONPs may impede the antioxidant system in the muscle tissue (Saddick et al., 2017; Attia et al., 2018). The current results were consistent with the findings of Al-Aqil and Zulkifli (2009) and Garriga et al. (2006), who indicated that corticosterone concentrations were increased in heat-challenged chickens compared with unchallenged chickens. Under normal temperatures, the ZnONP diet did not change the concentration of serum corticosterone in broiler chickens regardless of diet. An explanation for this phenomenon may be that heat stress activates the HPA axis and leads to increased plasma corticosterone concentrations (Song et al., 2012). In addition, alterations in the HPA axis that functions by released corticosterone during heat stress could impair chicken production by reducing feed consumption and consequently reducing body weight gain as observed in this study (Quinteiro-Filho et al., 2010; Lara and Rostagno, 2013). Previous studies (Sahin and Kucuk, 2003; Sahin et al., 2005) reported that 30 or 60 mg Zn/kg in the feed of quails reduced corticosterone levels under heat stress. The control and 40 mg/kg and 60 mg/kg ZnONP diets produced low serum corticosterone levels that may be attributed to the antioxidant and antistress properties of Zn, which also inhibits nicotinamide adenine dinucleotide phosphate-dependent lipid peroxidation (Bozakova, 2010). In addition, Zn may play a key role in the suppression of free radicals due to its ability to replace Fe and Cu from binding sites, thus contributing to reduced free radical production as a result of heat stress (Prasad and Kucuk, 2002). However, in this study, we found that 100 mg/kg dietary ZnONPs increased corticosterone levels in serum compared with control group and 40 mg/kg ZnONPs, indicating that a low level of Zn is absorbed due to low FI at 100 mg/kg. In conclusion, heat stress plays a vital role on the physiology of broilers and influences their performance. ZnONPs used in this study did not influence the body weight of the broiler chickens; however, ZnONPs numerically reduced the FCR of broilers, increased Zn retention in the liver regardless of source and level and alleviated the negative effects of heat stress via maximizing the antioxidant defense system and minimizing lipid peroxidation. These beneficial results are vi-

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