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. 2022 Oct 13;102(1):102244. doi: 10.1016/j.psj.2022.102244

Impacts of synthetic androgen and estrogenic antagonist administration on growth performance, sex steroids hormones, and immune markers of male and female broilers

Mona EM Younis *, Fatima A Jaber †, Kamlah Ali Majrashi ‡, Hanan A Ghoneim §,ǁ, Mustafa Shukry #,, Manal E Shafi ǁ, Najah M Albaqami ǁ, Mohamed E Abd El-Hack #,¶,1, Mahmoud M Abo Ghanima *
PMCID: PMC9640317  PMID: 36335738

Abstract

The influence of synthetic androgen and estrogenic antagonists (Tamoxifen) on body characteristics and immune response of male and female broilers and the correlation between sex hormone levels were estimated in our experiment. One day old chicks were sexed, and chicks of each sex were randomly distributed on three experimental treatments; the first treatment group (TAM20) chicks were supplied with estrogenic antagonist tamoxifen citrate 20 mg/kg body weight through oral administration for four times every other day from third until ninth d; Androgen treatment chicks were injected intramuscular with veterinary androgen AD GAN@ (Boldenone Undecylenate 50 mg) 1 cm/10 kg body weight at fifth and ninth day, and the third treatment was control. Androgen treatment reported the highest feed intake with the lowest for TAM20 treatment. Concerning carcass characteristics, early androgen injection increased breast percentage significantly compared to TAM20 treatment. Androgen supplementation increased significantly comb the percentage. However, TAM20 decreased it particularly compared to control. Moreover, the percentage of comb and shanks was substantially higher for males than females. Concerning the effects of both treatments on sex hormones, androgen showed favorable effects on testosterone and estrogen compared to Tamoxifen 20 treatment. On the other hand, the administration of TAM 20 improves phagocytic activity compared to androgen administration.

Key words: androgen; TAM20; estrogen, phagocytic index; performance; carcass characteristics

INTRODUCTION

Improving the immune response of poultry will be reflected positively on its productivity and performance. Disease, heavy vaccinations, rearing system, environmental conditions, management, and other factors act as immune stressors that affect birds' immune status, affecting growth efficiency and enteric diseases, causing significant economic shortfalls (Yang et al., 2011; Younis et al., 2020). The effect of a gonadal steroid on the immune system varies depending on various factors such as animal species, gender, and age. The dose and hormonal administration methods, the antigen, and the host's immunocompetence may differ from immunosuppression to immunization (Ahmed and Talal, 1990; Hussein et al., 2019). Females have more robust immune responses than males (Lin et al., 1996). But this does not prove that androgens like testosterone decrease the immune system. Because of increased estrogen levels, women may have stronger immunological responses (Olsen and Kovacs, 1996) or other mechanisms based on sex-specific changes in immunological responses. Due to genetics or other factors, immune responses may differ between men and women (Ahmed and Talal, 1990).

Tamoxifen's estrogen receptor agonist/antagonist properties are not the only ones it has (Komm and Mirkin, 2014; Younis et al., 2020); it also affects sphingolipid biosynthesis, among other things (Sharma et al., 2014). Such ‘off-target’ results have been shown to confer Tamoxifen's therapeutic action (Mandlekar and Kong, 2001); however, its impact on specific cell types, particularly circulating neutrophils, is still unclear (Corriden et al., 2015; Mirzaei et al., 2022). A significant immunosuppressive effect has been hypothesized based on early studies of Tamoxifen's effect on the neutrophil function that prevents transendothelial migration (de Oliveira et al., 2004; Moreland et al., 2006; Swelum et al., 2020, 2021a,b). Corriden et al. (2015) used in vitro and in vivo methods. DNA-based neutrophil extracellular traps were promoted by Tamoxifen and its effects on neutrophil chemotaxis and phagocytosis (NETs). Antimicrobial peptides, histones, and/or granule proteases coated NETs can kill bacteria and other pathogens by trapping and encasing them (Brinkmann and Zychlinsky, 2007; von Köckritz-Blickwede and Nizet, 2009). It also enhances pathogen death in vitro and MRSA clearance in vivo. Intracellular ceramide regulates neutrophil activity.

Tamoxifen, its active metabolite 4-hydroxytamoxifen, and its primary metabolite N-desmethyltamoxifen all increased NET production in freshly separated human neutrophils, according to fluorescence-based extracellular DNA detection (Corriden et al., 2015). The influence of steroidal hormones on birds' immune response is measured after ova injection (Andersson et al., 2004) or after late and long administration through either hormone implantation (Owen-Ashley et al., 2004). Our experiment studied the effect of synthetic androgen and estrogenic antagonist (Tamoxifen) administration for a short period at early ages on performance, carcass characteristics, edible and inedible organs percentages, phagocytic index, and level of sex hormones of males and females broilers chickens beside correlation coefficient between sex hormones levels and measured traits.

MATERIALS AND METHODS

Birds' Management

The Native Experimental Animal Care Committee accepted this experimental technique (DMU/VetMed-2019-/0145). This work was done at the Damanhur University poultry farm of the animal husbandry and wealth department. Two hundred twenty-five males and 225 females' one-day-old Arbor Acres chicks were obtained from a local hatchery after they were sexed. Each sex's Chicks were identified by wing bands and then randomly distributed on 3 experimental treatments (75 chicks per treatment). Each treatment included 5 replicates (15 chicks per replicate). During the first week of life, chicks of each treatment were housed collectively to can brooded well under a gas brooder and achieve 35°C under the brooder; after the first week, the chick of each replicate was housed separately on a wood shaving floor pen 1.5 m2 and supplied with 32°C brooding temperature decreased 1 oc every 2 d until 24°C.

In the first week, the light was provided for 24 h, and 5 FC was reduced to 18 h daily until the end of the experiment at 45 d. Chicks were vaccinated against Newcastle and Infectious Bronchitis at the seventh d of age through eye dropping, against Infectious Bursal Disease at 2 wk of age, and New Castle Disease again at 18 d and 30 d of age through spraying. Starter mash ration 23% CP provided for the first 3 wk of age replaced by grower crumbled ration 21% CP until the fifth week and finisher pelleted ration 19% CP until the end of the experiment. Ration stages were purchased from a local ration company. Feed and water were introduced ad libitum through manual feeders and waterers with frequent cleaning and sanitizing feeders and waterers.

Experimental Design

After sexing and wing banding of chicks, 225 of each sex were randomly distributed on three experimental treatments (75 chicks/ treatment). Chicks of the first treatment (TAM20) were supplied with tamoxifen citrate (obtained from Amriya for Pharmaceutical Industries, Alexandria, Egypt) was used as TAM citrate) as an estrogenic antagonist, 20 mg/kg body weight through oral administration of the drug after diluted with water, birds received four doses of tamoxifen citrate every other day from 3rd until 9th days according to Younis et al. (2020). Under the second treatment (Androgen), chicks were injected intramuscularly with veterinary androgen AD GAN@ (Boldenone Undecylenate 50 mg) 1 cm/10 kg body weight on the fifth and ninth day to allow withdrawal time for the drug over 20 d as recommended by the manufacturer. The third treatment was the control treatment, wherever chicks of each treatment were redistributed on five replicates (15 chicks per replicate).

Growth Traits

Acute Initial and final body weights were estimated using a sensitive scale, total weight gain assessed by subtracting the initial weight from the final one, and feed intake estimated weekly by subtracting ration residues at the end of the week from ration supplied through the week to calculate net feed intake then total feed intake estimated, additionally feed conversion ratio estimated by the division of weight gain on feed intake multiplying by 100.

Carcass Characteristics

Forty carcass traits were measured at 45 d of age. Five birds per replicate were fasted for 12 h before slaughtering but still supplied with water. Birds are weighed before slaughtering and after evisceration to estimate hot carcass weight and dressing percentage by dividing carcass weight by life weight. All internal organs, including the intestine, heart, spleen, liver, and gizzard, were weighed and calculated as a percentage of live weight after evacuated and abdominal fat. Also, comb and shanks were weighed and calculated as percentages of life weight. Carcass divided and thigh, breast (including bone and skin), neck with backbone and wings were weighed and calculated as a percentage of carcass weight.

Hormonal Assay

Blood samples were collected from the wing veins of three birds per replication at the end of the experiment. The serum was inaccessible by centrifugation at 3,000 rpm for 15 min and kept at (−20°C) until analysis. The serum testosterone and estrogen concentrations were assessed using the commercial Elisa kit (Wuhan Fine Biotech Co., Ltd, China) in an enzyme-linked immunosorbent test (ELISA) based on instructions from the manufacturer.

Phagocytic Index

Phagocytic activity was evaluated following (Jacobs, 1964) by the ability of white blood cells to engulf heat-killed organisms in a standard suspension at 37°C. The MOS chosen for such a purpose was Staph aureus.

Statistics

Data have been analyzed with a 2-way SAS variance analysis (Cary, 2002). Proc GLM (P < 0.05). The Duncan multiple range tests determined significant differences between means (Duncan, 1955) by adopting the following model:

Yijk=μ+Ti+Sj+TSij+eijk

Where: Yijk = an observation, µ = the overall mean, Ti = effect of treatment, Sj = effect of sex, TSij = the interaction between treatment and sex and eijk=random error.

RESULTS

Performance Traits

Table 1 illustrates that neither tamoxifen nor androgen supplementation substantially influenced the body weight, total weight gain, nor feed conversion ratio compared to the control. On the contrary, feed intake was significantly highest for androgen treatments, followed by control. The lowest values were reported for TAM20 treatments (P < 0.0001). Males and females reported similar weight, weight gain, feed intake, and feed conversion ratio. Concerning treatment sex interaction, although there were no noteworthy differences between treatments, androgen and TAM20 treatments induced higher productive performance values for females than males, with adverse results reported for control treatments (Table 1).

Table 1.

Effect of date palm pollen ethanolic extract (500 mg/kg bw/day) and/or doxorubicin (2.5 mg/kg bw/day) on body, heart, and relative heart weights myocyte cross-sectional area of control and treated rats.

Items Initial weight Final weight Weight gain Feed intake Feed conversion
Treatment effect
 Androgen 44.5±1.17 2146.7±58.77 2102.20±58.3 3948.20±35.81a 1.89±0.05
 Control 45.83±1.2 2107.42±67.83 2061.58±68.03 3793.42±52.46b 1.86±0.07
 Tam20 45.42±0.96 2117.42±80.34 2072.00±80.32 3521.50±21.9c 1.73±0.08
 P-Value NS NS NS <0.0001 NS
Sex effect
 Female 46.39±0.79 2136.5±46.47 2090.11±46.61 3713.50±54.60 1.80±0.06
 Male 44.06±0.94 2106.75±68.03 2062.69±67.91 3776.13±51.51 1.86±0.06
 P-Value NS NS NS NS NS
Interaction effect
 Treatment Sex
 Androgen Female 43.75±1.25 2179.25±111.72 2135.5±110.68 3960.75±56.95a 1.87±0.1
Male 45.00±1.83 2125.00±71.66 2080.00±71.06 3939.83±50.14a 1.9±0.06
 Control Female 49.17 ± 0.83 2056.83 ± 55.5 2007.67 ± 54.77 3804.67 ± 88.74b 1.91 ± 0.09
Male 42.50 ± 1.12 2158 ± 127.05 2115.5 ± 127.27 3782.17 ± 64.68b 1.82 ± 0.11
 Tam20 Female 45.63 ± 1.13 2174.88 ± 80.34 2129.25 ± 80.89 3550.5 ± 29.17b 1.68 ± 0.08
Male 45.00 ± 2.04 2002.5 ± 185.13 1957.5 ± 184.03 3521.5 ± 36.08b 1.85 ± 0.19
 P-Value NS NS NS NS 0.02 NS
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Data are expressed as mean ± SEM.

a,b

Means within a column followed by different superscripts are significantly different (P < 0.05).

Carcass Characteristics

There were no substantial differences between different treatments in carcass weight, dressing percentage, and carcass cuts percentage relative to carcass weight, except that breast percentage was meaningfully higher (P < 0.05) for androgen treatments than TAM20 treatments, and the 2 treatments did not differ significantly from control. Females achieved significantly higher dressing and breast percentage than males, with opposite results observed for the thigh percentage; the interaction effect had the same treatment and sex effect trend, as shown in Table 2.

Table 2.

Effect of Tamoxifen and androgen supplementation on carcass characteristics of Arbor Acres chickens.

Level Carcass wt Dressing % Thigh Breast Should Neck
Treatment effect
 Androgen 1546.67 ± 68.95 73.89 ± 1.09 39.78 ± 0.66 38.11 ± 0.79a 11.22 ± 0.32 10.78 ± 0.22
 Control 1657.14 ± 93.4 76.14 ± 0.83 40.00 ± 0.62 36.86 ± 0.59ab 12.14 ± 0.49 10.71 ± 0.18
 Tam20 1511.2 ± 73.34 74.9 ± 1.02 39.90 ± 0.43 36.4 ± 0.65b 11.00 ± 0.21 11.2 ± 0.29
 P-value NS NS NS 0.049 NS NS
Sex effect
 Female 1603.17 ± 43.19 76.5 ± 0.5a 39.00 ± 0.28b 38.58 ± 0.48a 12.25 ± 1.44 10.75 ± 0.18
 Male 1528.14 ± 74.18 73.5 ± 0.86b 40.64 ± 0.45a 35.86 ± 0.43b 11.14 ± 0.25 11.07 ± 0.22
 P-value NS 0.0133 0.0128 0.0002 NS NS
Interaction effect
 Treatment Sex
 Androgen Female 1626.00 ± 64.48 75.5 ± 0.65 38.75 ± 0.75 39.50 ± 1.32a 11.00 ± 0.41 10.75 ± 0.48b
Male 1483.2 ± 111.14 72.6 ± 1.75 40.60 ± 0.93 37.00 ± 0.71bc 11.4 ± 0.51 10.80 ± 0.2b
 Control Female 1650.00 ± 37.04 77.0 ± 1.52 39.00 ± 0.88 38.33 ± 0.33ab 11.33 ± 0.84 11.0 ± 0.37ab
Male 1662.50 ± 172.7 75.5 ± 1.44 40.75 ± 0.95 35.75 ± 0.48cd 10.75 ± 0.48 10.5 ± 0.29b
 Tam20 Female 1556.80 ± 91.83 77.0 ± 1.05 39.20 ± 0.37 38.00 ± 0.45ab 10.8 ± 0.2 10.6 ± 0.24b
Male 1465.60 ± 121.3 72.8 ± 1.16 40.60 ± 0.68 34.80 ± 0.66d 11.2 ± 0.37 11.8 ± 0.37a
 P-value NS NS NS 0.045 NS 0.0401
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Data expressed as Mean ± SEM.

a,b,c,d

Mean within the same column with different superscripts are meaningfully different (P < 0.05).

The effect of treatment, sex, and their interaction on body organs is listed in Table 3. The treatment effect was insignificant except that the comb percentage was significantly highest (P < 0.0001) for androgen treatment, followed by control and TAM20 treatment. Concerning the sex effect, comb and shank percentages were higher (P < 0.01) for males than females, with no considerable differences for other measured body organs. Regarding the treatment of sex interaction, males under androgen treatment reported significant comb percentages followed by control. The lowest rate was for TAM20 treatment; on the contrary, the comb percentage for different therapy females was not significantly different.

Table 3.

Tamoxifen and androgen supplementation impact on Edible and inedible Organs of Arbor Acres chickens.

Level Liver % Heart % Spleen % Gizzard% Gizzard fat% Abdominall fat% Comb% Shank%
Treatment effect
 Androgen 2.44 ± 0.18 0.42 ± 0.03 0.08 ± 0.02 1.46 ± 0.09 0.86 ± 0.09 1.14 ± 0.11 0.06 ± 0.01a 3.67 ± 0.21
 Control 2.29 ± 0.18 0.5 ± 0.03 0.08 ± 0.02 1.43 ± 0.07 0.96 ± 0.05 1.56 ± 0.18 0.04 ± 0.01b 3.71 ± 0.30
 Tam20 2.5 ± 0.17 0.49 ± 0.02 0.09 ± 0.05 1.57 ± 0.07 0.82 ± 0.06 1.34 ± 0.13 0.02 ± 0.01c 3.8 ± 0.20
 P-Value NS NS NS NS NS NS 0.0003 NS
Sex effect
 Female 2.33 ± 0.14 0.44 ± 0.03 0.06 ± 0.01 1.48 ± 0.05 0.88 ± 0.07 1.38 ± 0.15 0.02 ± 0.002b 3.17 ± 0.10b
 Male 2.5 ± 0.14 0.49 ± 0.02 0.11 ± 0.04 1.51 ± 0.07 0.86 ± 0.04 1.29 ± 0.09 0.06 ± 0.01a 4.21 ± 0.24a
 P-Value NS NS NS NS NS NS <0.0001 <0.0001
Interaction effect
 Treatment Sex
 Androgen Female 2.75 ± 0.25a 0.38 ± 0.05 0.08 ± 0.03 1.4 ± 0.07 0.83 ± 0.16 1.28 ± 0.2 0.02 ± 0.005cd 3.0 ± 0.09c
Male 2.2 ± 0.20ab 0.46 ± 0.02 0.08 ± 0.02 1.5 ± 0.16 0.88 ± 0.1 1.04 ± 0.1 0.09 ± 0.01a 4.2 ± 0.22a
 Control Female 2.0 ± 0.10b 0.5 ± 0.06 0.05 ± 0.02 1.47 ± 0.03 1.03 ± 0.07 1.7 ± 0.45 0.02 ± 0.003cd 3.0 ± 0.05c
Male 2.5 ± 0.29ab 0.5 ± 0.04 0.1 ± 0.02 1.4 ± 0.12 0.9 ± 0.06 1.45 ± 0.09 0.06 ± 0.01b 4.25 ± 0.30a
 Tam20 Female 2.2 ± 0.2ab 0.46 ± 0.02 0.04 ± 0.01 1.54 ± 0.11 0.82 ± 0.11 1.28 ± 0.19 0.01 ± 0.004d 3.4 ± 0.21bc
Male 2.8 ± 0.2a 0.52 ± 0.02 0.15 ± 0.1 1.6 ± 0.1 0.82 ± 0.04 1.4 ± 0.2 0.03 ± 0.01c 4.20 ± 0.40a
 P-Value 0.0272 NS NS NS NS NS 0.0045
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Data expressed as Mean ± SEM.

a,b,c,d

Mean within the same column with different superscripts are meaningfully different (P < 0.05).

Serum Testosterone

Serum testosterone in androgen-treated birds was significantly increased, followed by the control and TAM20 groups (Table 3). Testosterone levels in males were also substantially increased. Meanwhile, treatment and sex interaction substantially impacted the highest-level testosterone hormone found in androgen-treated males, control males, and TAM20 males. The lowest level was seen in females of the three groups. Testosterone is also inversely proportional to phagocytic index, estrogen, total feed intake, weight gain, bodyweight, carcass%, dressing%, liver%, intestine%, abdominal fat%, and breast%. It is also positively proportional to total feed conversion, heart%, spleen, gizzard and gizzard fat%, shoulder %, neck& comb, and shank %, as shown in Table 5.

Table 5.

Correlation between testosterone, estrogen, phagocytic index and Edible and inedible organs, performance and carcass characteristics of Arbor Acres chickens.

Phag Test Estro W6 TFI TWG TFC Life Carc D.P Liv.p IntP H.P Spl.P gizP GFP AbFP ThiP Br.P Sh.P Ne.P CoP ShaP
Phag 1 −0.432 0.0105 0.170 −0.351 0.167 −0.275 −0.016 0.005 0.146 −0.040 0.143 −0.028 −0.074 0.066 −0.235 0.125 −0.024 0.006 0.194 −0.296 −0.512 −0.036
0.10 0.97 0.51 0.16 0.51 0.28 0.94 0.97 0.51 0.85 0.53 0.9 0.74 0.77 0.29 0.57 0.91 0.97 0.38 0.18 0.01 0.87
Test −0.432 1 −0.73 −0.101 −0.479 −0.178 −0.080 -0.169 −0.177 −0.138 −0.297 −0.070 0.348 0.012 0.038 0.018 −0.015 0.062 −0.058 0.262 0.231 0.151 0.136
0.1078 0.0002 0.709 0.060 0.507 0.768 0.46 0.44 0.54 0.18 0.76 0.121 0.951 0.86 0.93 0.94 0.78 0.80 0.25 0.31 0.51 0.55
Estro 0.010 −0.737 1 −0.037 0.718 0.0008 0.33 0.11 0.09 −0.03 0.32 0.10 −0.41 0.070 −0.05 −0.02 0.07 −0.04 0.09 −0.28 −0.04 −0.05 −0.20
0.97 0.0002 0.89 0.002 0.99 0.22 0.64 0.70 0.89 0.15 0.65 0.07 0.76 0.81 0.90 0.74 0.86 0.68 0.22 0.84 0.80 0.38
W6 0.17 −0.10 −0.037 1 0.094 0.96 −0.86 0.93 0.92 0.64 −0.14 −0.52 −0.07 0.11 −0.36 −0.049 0.32 −0.41 0.31 −0.25 −0.14 0.048 −0.36
0.51 0.70 0.89 0.54 <0.0001 <0.0001 <0.0001 <0.0001 0.0006 0.49 0.01 0.71 0.57 0.06 0.81 0.10 0.040 0.122 0.22 0.49 0.81 0.07
TFI −0.35 −0.47 0.718 0.09 1 0.07 0.34 0.21 0.21 0.14 −0.16 −0.22 −0.21 −0.19 −0.32 0.03 −0.15 −0.21 0.27 −0.17 −0.46 0.492 −0.08
0.166 0.060 0.002 0.54 0.61 0.023 0.29 0.31 0.48 0.43 0.31 0.30 0.34 0.11 0.85 0.46 0.29 0.18 0.41 0.018 0.012 0.69
TWG 0.16 −0.17 0.0008 0.96 0.076 1 −0.90 0.95 0.92 0.60 −0.14 −0.49 −0.09 0.14 −0.40 −0.071 0.20 −0.45 0.31 −0.28 −0.17 0.13 −0.31
0.51 0.50 0.99 <0.0001 0.61 <0.0001 <0.0001 <0.0001 0.001 0.48 0.01 0.66 0.47 0.04 0.73 0.31 0.02 0.12 0.17 0.41 0.50 0.12
TFC −0.27 −0.08 0.33 −0.86 0.340 −0.90 1 −0.88 −0.86 −0.56 0.11 0.45 0.01 −0.22 0.32 0.09 −0.23 0.42 −0.27 0.20 0.02 0.030 0.31
0.2848 0.768 0.2222 <0.0001 0.0235 <0.0001 <0.0001 <0.0001 0.003 0.57 0.03 0.92 0.27 0.11 0.63 0.26 0.03 0.18 0.33 0.89 0.88 0.12
Life −0.016 −0.16 0.11 0.93 0.215 0.951 −0.88 1 0.97 0.54 0.02 −0.61 −0.21 0.186 −0.34 0.035 0.20 −0.36 0.35 −0.28 −0.08 0.06 −0.37
0.9407 0.4637 0.6407 <0.0001 0.2998 <0.0001 <0.0001 <0.0001 0.001 0.87 0.0003 0.239 0.30 0.05 0.84 0.26 0.04 0.04 0.11 0.65 0.70 0.03
Carcass 0.005 −0.17 0.090 0.924 0.210 0.928 −0.86 0.97 1 0.70 −0.05 −0.67 −0.17 0.11 −0.403 0.04 0.24 −0.44 0.39 −0.39 −0.12 0.01 −0.45
0.97 0.44 0.70 <0.0001 0.31 <0.0001 <0.0001 <0.0001 <0.0001 0.76 <0.0001 0.32 0.53 0.02 0.79 0.18 0.01 0.02 0.02 0.51 0.93 0.009
DRESSP 0.14 −0.13 −0.03 0.64 0.14 0.60 −0.56 0.54 0.70 1 −0.29 −0.65 −0.006 −0.17 −0.46 0.08 0.26 −0.58 0.42 −0.62 −0.21 −0.21 −0.57
0.5156 0.54 0.89 0.0006 0.480 0.001 0.003 0.001 <0.0001 0.09 <0.0001 0.97 0.3 0.007 0.65 0.13 0.0004 0.01 0.0001 0.22 0.22 0.0006
LiverP −0.04 −0.29 0.32 −0.14 −0.16 −0.14 0.11 0.02 −0.05 −0.29 1 0.13 −0.13 0.20 −0.09 0.12 0.04 0.21 −0.20 −0.06 0.25 −0.23 0.024
0.85 0.18 0.15 0.49 0.43 0.48 0.57 0.87 0.76 0.09 0.491 0.46 0.26 0.60 0.50 0.79 0.2 0.26 0.72 0.16 0.19 0.89
IntP 0.14 −0.07 0.10 −0.52 −0.22 −0.49 0.45 −0.61 −0.67 −0.65 0.13 1 0.009 −0.03 0.32 0.01 −0.05 0.34 −0.64 0.25 0.22 −0.09 0.44
0.53 0.76 0.65 0.01 0.31 0.01 0.03 0.0003 <.0001 <.0001 0.49 0.95 0.85 0.08 0.92 0.79 0.06 0.0001 0.16 0.22 0.6 0.01
H.P −0.02 0.34 −0.41 −0.07 −0.21 −0.09 0.01 −0.21 −0.17 −0.006 −0.13 0.009 1 0.23 0.13 −0.17 −0.006 −0.17 −0.10 0.09 0.07 0.17 0.33
0.9 0.12 0.07 0.71 0.30 0.66 0.92 0.23 0.32 0.97 0.46 0.95 0.20 0.45 0.33 0.97 0.34 0.57 0.61 0.66 0.34 0.05
SplP −0.07 0.01 0.07 0.11 −0.19 0.14 −0.22 0.18 0.11 −0.17 0.20 −0.03 0.23 1 0.25 −0.14 −0.12 −0.09 0.05 0.21 0.32 0.02 0.06
0.74 0.95 0.76 0.57 0.34 0.47 0.27 0.30 0.53 0.34 0.26 0.85 0.20 0.16 0.42 0.51 0.61 0.74 0.22 0.07 0.87 0.71
gizP 0.06 0.038 −0.05 −0.36 −0.32 −0.40 0.32 −0.34 −0.40 −0.46 −0.09 0.32 0.13 0.25 1 0.09 −0.05 0.30 −0.160 0.48 0.29 −0.24 0.153
0.77 0.86 0.81 0.06 0.11 0.04 0.11 0.05 0.02 0.007 0.60 0.08 0.45 0.16 0.58 0.75 0.09 0.38 0.004 0.09 0.18 0.40
GFP −0.23 0.018 −0.02 −0.04 0.037 −0.07 0.09 0.03 0.04 0.08 0.12 0.01 −0.17 −0.14 0.09 1 0.31 0.22 −0.20 −0.24 0.01 −0.16 −0.25
0.29 0.93 0.90 0.81 0.8 0.7 0.63 0.8 0.7 0.6 0.5 0.9 0.33 0.4 0.58 0.07 0.21 0.26 0.18 0.93 0.37 0.16
AbFP 0.12 −0.01 0.07 0.32 −0.15 0.20 −0.23 0.20 0.24 0.26 0.04 −0.05 −0.006 −0.12 −0.05 0.31 1 0.02 −0.20 −0.08 0.16 −0.30 −0.27
0.577 0.945 0.740 0.107 0.465 0.319 0.264 0.266 0.180 0.136 0.790 0.790 0.97 0.51 0.7 0.07 0.87 0.2 0.62 0.35 0.09 0.12
Th.P −0.02 0.06 −0.04 −0.41 −0.21 −0.45 0.42 −0.36 −0.4 −0.58 0.2 0.34 −0.17 −0.09 0.30 0.22 0.02 1 −0.61 0.22 0.23 0.05 0.49
0.914 0.78 0.86 0.04 0.29 0.02 0.03 0.04 0.011 0.0004 0.245 0.065 0.34 0.61 0.091 0.21 0.87 0.0002 0.21 0.20 0.75 0.003
BrP 0.006 −0.05 0.09 0.31 0.27 0.31 −0.2 0.35 0.39 0.42 −0.20 −0.64 −0.1 0.05 −0.160 −0.20 −0.2 −0.61 1 −0.031 −0.39 −0.10 −0.55
0.97 0.80 0.68 0.12 0.18 0.123 0.188 0.04 0.02 0.01 0.26 0.0001 0.57 0.74 0.38 0.26 0.25 0.0002 0.86 0.025 0.57 0.0009
ShoP 0.19 0.26 −0.28 −0.25 −0.17 −0.28 0.20 −0.287 −0.39 −0.62 −0.06 0.25 0.09 0.21 0.48 −0.24 −0.08 0.22 −0.03 1 0.17 0.05 0.32
0.38 0.25 0.22 0.22 0.41 0.1 0.33 0.11 0.02 0.0001 0.72 0.16 0.61 0.22 0.004 0.18 0.62 0.21 0.86 0.33 0.77 0.06
NeP −0.29 0.23 −0.04 −0.14 −0.46 −0.17 0.02 −0.08 −0.12 −0.21 0.25 0.22 0.07 0.32 0.29 0.01 0.16 0.23 −0.39 0.17 1 −0.20 0.03
0.18 0.31 0.84 0.49 0.01 0.41 0.89 0.65 0.51 0.22 0.16 0.22 0.66 0.07 0.09 0.93 0.35 0.20 0.02 0.33 0.27 0.85
CoP −0.51 0.15 −0.05 0.04 0.49 0.13 0.03 0.06 0.01 −0.21 −0.23 −0.09 0.17 0.02 −0.24 −0.16 −0.30 0.058 −0.1 0.05 −0.20 1 0.52
0.014 0.51 0.80 0.81 0.01 0.50 0.88 0.70 0.93 0.22 0.19 0.6 0.34 0.87 0.1 0.3 0.09 0.75 0.57 0.77 0.27 0.002
ShaP −0.03 0.13 −0.20 −0.36 −0.08 −0.3 0.31 −0.3 −0.45 −0.57 0.02 0.44 0.33 0.068 0.15 −0.21 −0.27 0.49 −0.55 0.32 0.03 0.526 1
0.87 0.55 0.38 0.07 0.69 0.12 0.12 0.03 0.009 0.0006 0.89 0.01 0.05 0.71 0.40 0.16 0.12 0.003 0.0009 0.06 0.85 0.002
Open in a new tab

Data are expressed as Mean ± SEM.

Abfp., abdominal fat; Brp., breast %; Cop., Comb %; Estro., estrogen; Gizp., gizzard %; H.p .,heart %; Intp., Intestine %; Life., life weight; Liver p., liver percentage; Nep., neck %; Shop., shoulder %; Shap.,shank%;Splp., Spleen %; Phag., phagocytic index; Test., Testosterone; Tfi., Total feed intake; Thp., thigh %; Twg., Total weight gain; W6., weight 6.

Serum Estrogen

Table 4 showed a considerable rise in serum estrogen levels in androgen treated group compared to both control and TAM 20 groups. In female birds, estrogen levels have significantly increased compared to males in all groups. Besides, the interaction between sex and treatment greatly influenced estrogen hormone at the most advanced level found in androgen-treated females than control females, followed by TAM 20 females than males of both androgen and TAM 20 groups and finally control males. Estrogen is inversely proportional to testosterone, weight, dressing, heart %, gizzard%, gizzard fat %, shoulder, shank %shop, comp %, and neck %, and positively proportional to dressing %, abdominal fat %, and total feed intake as shown in Table 5.

Table 4.

Tamoxifen and androgen supplementation impact on serum testosterone, estrogen level, and Phagocytic index in Arbor Acres chickens.

Level Testosterone Estrogen Phagocytic index
Treat
 Androgen 1.18 ± 0.42a 55.83 ± 9.44a 35.5 ± 3.58b
 Control 0.79 ± 0.33b 41.17 ± 7.4b 42.33 ± 2.55a
 TAM20 0.61 ± 0.23c 37.5 ± 2.75b 47.00 ± 4.93a
 P value <.0001 0.0032 0.0071
Sex
 Female 0.14 ± 0.03b 57.44 ± 5.7a 48.67 ± 2.56a
 Male 1.58 ± 0.15a 32.22 ± 2.56b 34.56 ± 2.17b
P value <.0001 <.0001 <.0001
Treat*sex
 Androgen Female 0.25 ± 0.07d 75.67 ± 5.78a 42.33 ± 1.76bc
Male 2.11 ± 0.08a 36 ± 4.36cd 28.67 ± 3.76d
 Control Female 0.07 ± 0.02d 56.67 ± 4.1b 46.67 ± 2.6b
Male 1.51 ± 0.1b 25.67 ± 4.1d 38.00 ± 2.65bc
 TAM20 Female 0.1 ± 0.01d 40 ± 4.62c 57.00 ± 3.46a
Male 1.13 ± 0.11c 35 ± 3.21cd 37.00 ± 3.06cd
P value 0.0004 0.0055 0.1995
Open in a new tab

Data expressed as Mean ± SEM.

a,b,c,d

There is a considerable difference between the mean values in the same column with different superscripts (P < 0.05).

Phagocytic Index

The rise of the phagocytic index was substantial in TAM 20 and control groups, followed by androgen-treated birds, Table 4. Moreover, the phagocytic index showed a marked increase in females associated with males of all groups. Besides, treatment and sex interaction significantly affected such index, with the highest level in TAM20 females, followed by control females. Both androgen females and control males groups were followed by TAM 20 males, and finally, androgen-treated males. The phagocytic index is inversely proportional to testosterone, total feed intake, total feed conversion, liver %, heart %, spleen %, gizzard fat%, thigh %, neck%, comb %, and shoulder %, as shown in Table 5.

DISCUSSION

The impact of early and short administration of sex hormones agonist and antagonist on broiler chickens' performance and the correlation between sex hormones level, performance, and immune response were estimated. External hormonal supplementation on performance traits was significantly affected; only feed intake increased under androgen treatments. It decreased under TAM20 treatment compared to control, although body weight and weight gain increased numerically for females and decreased for males treated with steroidal hormones. In hens, sex steroids have had little success stimulating growth or boosting efficiency (Liebert, 2006).

Fennell and Scanes (1992) reported that the effects of androgens on the growth of white leghorn chickens were either reduced or unaffected. An anabolic effect on male and female chicks' body weight was identified when DHT was given in large quantities; however, the impact on testes growth was less pronounced (Abd El-Hack et al., 2018, 2022). Others have found that providing androgens to cockatiels slowed their growth. Exaggerated male secondary sex traits are linked to this growth (Dube and Tremblay, 1974).

A high dose of testosterone propionate (2.5 mg/wk) improved growth in female chicks receiving the injections twice weekly (Ma, 1954). Carcass characteristics did not significantly change among treatments, except that breast percentage was considerably higher in androgen treatments and lower in TAM20 treatments relative to control.

Testosterone therapy has been demonstrated to enhance growth hormone levels in the blood, resulting in increased muscular growth (Swerdloff and Wang, 1993). Comb percentages were significantly higher for androgen treatment males, control males, and TAM20 males. Adversely, different comb percentages for females of different treatments were insignificant. However, exogenous hormonal supplementation did not affect other edible and inedible organ percentages. Fennel and Scanes (1992) Androgens have stimulated male reproductive system development by facilitating the androgen receptor in the body's endocrine system. This can be seen in the growth of the testes and the hair on men's heads. Furthermore, according to testosterone propionate (TP) increased comb growth in the three experimental groups, while estradiol 3-benzoate (EB) inhibited it.

Body weight, weight gain, feed intake and conversion ratio did not change substantially by sex influence, contrary to Olawumi and Fagbuaro (2011) and Thutwa et al. (2012). The growth rate in males was significantly faster than in women, and the slaughter weights were substantially higher (Choo et al., 2014). There may be a reason for this discrepancy in the supplied hormone consequence. Observation of treatment sex interaction effect reflected better body weight and weight gain for males than females in the control treatment, which conformed with the authors' results; however, hormonal treatments inverted these results. On the contrary, reported similar feed conversion ratios.

Females had significantly higher dressing and breast percentages about the effect of sex on carcass traits. Males had a substantially higher thigh percentage. These results were at variance with Olawumi and Fagbuaro (2011) regarding dressing and breast percentage results; they reported nonsignificant differences between the 2 sexes for these traits and conformity with their thigh percentage results. Moreover, Castellini et al. (2006) showed that gender had no substantial impact on carcass traits. Nonetheless, Musa et al. (2006) reported a significant sex effect on these traits. Edible organ percentages were similar for the 2 sexes. These results agreed with Olawumi and Fagbuaro (2011). Concerning in edible organs percentages, comb and shank rates were significantly higher for males than females, which conforms with (Abdelnour et al., 2020; Aladaileh et al., 2020).

Administration of TAM 20 to birds led to a significant decrease in both testosterone and estrogen levels. This finding is in harmony with our previous study (Younis et al., 2020), which elucidated that TAM at a dose of 10 mg/kg BW had favorable effects on the level of both estrogen and testosterone in broilers as compared to the group that established TAM at a dose of 20 mg/kg B.W. Early egg production was reported to have been boosted by TAM treatment at modest dosages in young WL hens (Jacobs, 1964). Low dosages of TAM administered to male WL chicks increased testicular and comb growth and plasma testosterone levels, coinciding with early semen production and sexual activity. Conversely, TAM exhibits both anti-estrogenic and estrogenic effects on WL male chicks, depending on the amount of TAM administered (Rozenboim et al., 1989), and does not act as a pure estrogen antagonist as has previously been assumed (Sutherland, 1981).

Our results revealed elevated serum testosterone and estrogen in androgen-treated groups. This finding is in harmony with Alén et al. (1985), which described an increase in the level of such 2 hormones following androgen administration in power athletes. They attributed the high estrogen level to the administered androgen as a precursor for estrogen synthesis. Our findings on the impact of sex on testosterone and estrogen hormones agree with those of a prior study (Dewil et al., 1998), with much greater estrogen levels in females and testosterone in males reporting that factor to have a considerable impact on hormone levels.

Our results revealed a significant improvement in the TAM 20 group's phagocytic index compared to the androgen-treated group. This finding agrees with a previous study (Corriden et al., 2015), which reported that Tamoxifen improves neutrophils' bactericidal activity, with high NETs production as an impossible mechanism. Such enhancement occurs mainly through the alteration of cellular ceramide concentrations. Bioactive sphingolipid Ceramide is a cell stress signal associated with neutrophil apoptosis earlier (Scheel-Toellner et al., 2004; Seumois et al., 2007; Corriden et al., 2015). It has been found, however, that both Tamoxifen and synthetic ceramide are potent stimulators of the new cell death pathway known as NETosis (Wartha and Henriques-Normark, 2008; El-Tarabily et al., 2021; Seidavi et al., 2021). Moreover, both the apoptotic and autophagic pathways can be stimulated by ceramide (Maiuri et al., 2007). It most recently was involved in the manufacturing of NET (Remijsen et al., 2011; Younis et al., 2022).

Myeloid progenitors can differentiate into neutrophils with the help of androgen hormones. Testicular feminization mutation in animals and genetically engineered androgen receptor-deficient mice demonstrate neutropenia due to the androgen insensitivity mutation (Chuang et al., 2009). Androgen-deficient prostate cancer patients and gonadectomized animals show neutropenia before androgen-replacement therapy/DHT medication is administered (Trigunaite et al., 2013; Bird et al., 2017). Androgens have been shown to affect the function of neutrophils. Testosterone, for example, inhibits both the antibacterial action and the generation of pro-inflammatory cytokines by human neutrophils, while it promotes the anti-inflammatory cytokines IL-10 and TNF-alpha production (Malkin et al., 2004; Marin et al., 2010). These results are in harmony with our findings, which reported reduced phagocytic activity in the androgen-treated group.

In contrast to males, our findings showed that females had much higher phagocytic activity. The X chromosome and sex hormones have been linked to disparities in immunity between men and women (Oertelt-Prigione, 2012). It is well known that a person's sex hormones can influence the activity and development of immune cells and the vulnerability of cells and tissues to harm caused by aberrant (autoimmune) processes (Gubbels Bupp and Jorgensen, 2018). These 3 hormones also influence the immune cells' reaction to estrogen, progesterone, and testosterone. Receptors for nuclear and non-nuclear hormones are involved in their actions (Oertelt-Prigione, 2012). Gelmann (2002) showed that the X chromosome encodes for androgen receptors, which attach to testosterone and 5-dihydrotestosterone and then transmit their nuclear action via lineage to ARE (androgen response elements) in the promoter region of vulnerable genes.

As a result of its direct and indirect actions, estrogen acts on estrogen receptors (ER). The E/ER complexes are linked to specific estrogen response elements (ERE) inside the promoter or enhancer regions of genes. At the same time, the indirect response interacts with unrelated transcription factors to alter their function (Ho and Liao, 2002). The 2 ER isoforms—ER and ER—have a few similar target genes and a few unique ones (Stossi et al., 2004) and numerous strategies to control the production of cytokines in target cells (Oertelt-Prigione, 2012). As a rule, estrogen boosts immunological responses, whereas progesterone and androgens depress them (Younis and Ghoneim, 2022). The existence or absence of an extra X chromosome is the first consideration when examining the impact of genetics on sex differences. The X chromosome, which contains roughly 1,000 genes, plays a significant role in the body's ability to fight off infection (Fish, 2008). The X chromosome has an interesting immune regulator called IL-9. A recent study found a link between the IL-9 gene polymorphism and a virus infection's sex-specific prevalence. Male children are far more often than females to contract respiratory sincitial virus (RSV), and the polymorphism that has been linked to an elevated risk of infection has only been found in male patients (Schuurhof et al., 2010; Fazli et al., 2015).

CONCLUSIONS

This is the first study to estimate the impact of synthetic androgenic and estrogenic antagonists on the immune systems and physical traits of broiler males and females. Tamoxifen and androgen had no noticeable effect on weight gain. But androgen treatment significantly improved male-to-female secondary sexual characteristics compared to Tamoxifen with improved phagocytic index with Tamoxifen 20 supplementation. The positive effect of androgen treatment on sexual hormone levels was recorded compared to Tamoxifen 20 supplementation.

Acknowledgments

The authors acknowledge their respective universities for their support.

Author contributions: Conceptualization, MEMY, HAG, MS, MMAG; data curation, FAJ, KAM, MES, NMA, MEAE-H; formal analysis, MEMY, MS, MMAG; funding acquisition, FAJ, KAM, MES, NMA. An investigation, MEMY, HAG methodology, MEMY, HAG, MS, MMAG; writing—original draft, MEAE-H. All authors have read and agreed to the published version of the manuscript.

Ethical statement: This study was declared by The experimental protocol regarding the care and handling of animals was approved by the Native Experimental Animal Care Committee and approved by the Ethics of the Institutional Committee of Animal Husbandry and Animal Wealth Development Department, Faculty of Veterinary Medicine, Damanhour University, Damanhour, Egypt (DMU/VetMed-2020-/0145). All methods were performed according to the relevant guidelines and regulations of Damanhour University in handling experimental animals.

Data availability statement: Data are available upon request.

Disclosures

The authors declare no conflicts of interest.

References

  1. Abd El-Hack M.E., Alagawany M., Elrys A.S., Desoky E.S.M., Tolba H.M., Elnahal A.S., Swelum A.A. Effect of forage Moringa oleifera L. (moringa) on animal health and nutrition and its beneficial applications in soil, plants and water purification. Agriculture. 2018;8:145. [Google Scholar]
  2. Abd El-Hack M.E., El-Saadony M.T., Salem H.M., El-Tahan A.M., Soliman M.M., Youssef G.B., Swelum A.A. Alternatives to antibiotics for organic poultry production: types, modes of action and impacts on bird’s health and production. Poult. Sci. 2022;101:1–20. doi: 10.1016/j.psj.2022.101696. [DOI] [PMC free article] [PubMed] [Google Scholar]
  3. Abdelnour S.A., Swelum A.A., Salama A., Al-Ghadi M.Q., Qattan S.Y., Abd El-Hack M.E., El-Saadony M.T. The beneficial impacts of dietary phycocyanin supplementation on growing rabbits under high ambient temperature. Italian J. Anim. Sci. 2020;19:1046–1056. [Google Scholar]
  4. Ahmed S.A., Talal N. Sex hormones and the immune system—part 2. Animal data. Baillieres Clin. Rheumatol. 1990;4:13–31. doi: 10.1016/s0950-3579(05)80241-9. [DOI] [PubMed] [Google Scholar]
  5. Aladaileh S.H., Khafaga A.F., Abd El-Hack M.E., Al-Gabri N.A., Abukhalil M.H., Alfwuaires M.A., Abdelnour S. Spirulina platensis ameliorates the sub chronic toxicities of lead in rabbits via anti-oxidative, anti-inflammatory, and immune stimulatory properties. Sci. Total Environ. 2020;701 doi: 10.1016/j.scitotenv.2019.134879. [DOI] [PubMed] [Google Scholar]
  6. Alén M., Reinilä M., Vihko R. Response of serum hormones to androgen administration in power athletes. Med. Sci. Sports Exerc. 1985;17:354. [PubMed] [Google Scholar]
  7. Andersson S., Uller T., Lõhmus M., Sundström F. Effects of egg yolk testosterone on growth and immunity in a precocial bird. J. Evol. Biol. 2004;17:501–505. doi: 10.1111/j.1420-9101.2004.00706.x. [DOI] [PubMed] [Google Scholar]
  8. Bird A.K., Chang M., Barnard J., Goldman B.I., Meednu N., Rangel-Moreno J., Anolik J.H. Neutrophils slow disease progression in murine lupus via modulation of autoreactive germinal centers. J. Immunol. 2017;199:458–466. doi: 10.4049/jimmunol.1700354. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Brinkmann V., Zychlinsky A. Beneficial suicide: why neutrophils die to make NETs. Nat. Rev. Microbiol. 2007;5:577–582. doi: 10.1038/nrmicro1710. [DOI] [PubMed] [Google Scholar]
  10. Cary N.C.J.U. SAS Institute Inc.; 2002. SAS for Windows Release. 8. [Google Scholar]
  11. Castellini C., Mugnai C., Pedrazzoli M., Dal Bosco A. Productive performance and carcass traits of Leghorn chickens and their crosses reared according to the organic farming system. Proc. Atti XII European Poultry Conference; Verona; 2006. [Google Scholar]
  12. Choo Y., Kwon H., Oh S., Um J., Kim B., Kang C., Lee S., An B. Comparison of growth performance, carcass characteristics and meat quality of Korean local chickens and silky fowl. Asian-Australasian J. Anim. Sci. 2014;27:398. doi: 10.5713/ajas.2013.13638. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Chuang K.-H., Altuwaijri S., Li G., Lai J.-J., Chu C.-Y., Lai K.-P., Lin H.-Y., Hsu J.-W., Keng P., Wu M.-C. Neutropenia with impaired host defense against microbial infection in mice lacking androgen receptor. J. Exp. Med. 2009;206:1181–1199. doi: 10.1084/jem.20082521. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Corriden R., Hollands A., Olson J., Derieux J., Lopez J., Chang J.T., Gonzalez D.J., Nizet V. Tamoxifen augments the innate immune function of neutrophils through modulation of intracellular ceramide. Nat. Commun. 2015;6:1–8. doi: 10.1038/ncomms9369. [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. de Oliveira A.P.L., Oliveira-Filho R.M., da Silva Z.L., Borelli P., de Lima W.T. Regulation of allergic lung inflammation in rats: interaction between estradiol and corticosterone. NeuroImmunoModulation. 2004;11:20–27. doi: 10.1159/000072965. [DOI] [PubMed] [Google Scholar]
  16. Dewil E., Buyse J., Veldhuis J.D., Mast J., De Coster R., Decuypere E. In ovo treatment with an aromatase inhibitor masculinizes postnatal hormone levels, abdominal fat pad content, and GH pulsatility in broiler chickens. Domest. Anim. Endocrinol. 1998;15:115–127. doi: 10.1016/s0739-7240(97)00084-2. [DOI] [PubMed] [Google Scholar]
  17. Dube J.Y., Tremblay R.R. Aindrogen binding proteins in Cock2s tissues: properties of ear lobe protein and determination of binding sites in head appendages and other tissues. Endocrinology. 1974;95:1105–1112. doi: 10.1210/endo-95-4-1105. [DOI] [PubMed] [Google Scholar]
  18. Duncan D.B. Multiple range and multiple F tests. Biometrics. 1955;11:1–42. [Google Scholar]
  19. El-Tarabily K.A., El-Saadony M.T., Alagawany M., Arif M., Batiha G.E., Khafaga A.F., Abd El-Hack M.E. Using essential oils to overcome bacterial biofilm formation and their antimicrobial resistance. Saudi J. Biol. Sci. 2021;28:5145–5156. doi: 10.1016/j.sjbs.2021.05.033. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Fazli N., Hassanabadi A., Mottaghitalab M., Hajati H. Manipulation of broiler chickens sex differentiation by in ovo injection of aromatase inhibitors, and garlic and tomato extracts. Poult. Sci. 2015;94:2778–2783. doi: 10.3382/ps/pev236. [DOI] [PubMed] [Google Scholar]
  21. Fennell M.J., Scanes C.G. Inhibition of growth in chickens by testosterone, 5α-dihydrotestosterone, and 19-nortestosterone. Poult. Sci. 1992;71:357–366. doi: 10.3382/ps.0710357. [DOI] [PubMed] [Google Scholar]
  22. Fish E.N. The X-files in immunity: sex-based differences predispose immune responses. Nat. Rev. Immunol. 2008;8:737–744. doi: 10.1038/nri2394. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Gelmann E.P. Molecular biology of the androgen receptor. J. Clin. Oncol. 2002;20:3001–3015. doi: 10.1200/JCO.2002.10.018. [DOI] [PubMed] [Google Scholar]
  24. Gubbels Bupp M., Jorgensen T. Androgen-induced immunosuppression. Front. Immunol. 2018;9:794. doi: 10.3389/fimmu.2018.00794. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Ho K.J., Liao J.K. Nonnuclear actions of estrogen. Arterioscler. Thromb. Vasc. Biol. 2002;22:1952–1961. doi: 10.1161/01.atv.0000041200.85946.4a. [DOI] [PubMed] [Google Scholar]
  26. Hussein E.O.S., Suliman G.M., Al-Owaimer A.N., Ahmed S.H., Abudabos A.M., Abd El-Hack M.E., Swelum A.A. Effects of stock, sex, and muscle type on carcass characteristics and meat quality attributes of parent broiler breeders and broiler chickens. Poult. Sci. 2019;98:6586–6592. doi: 10.3382/ps/pez464. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Jacobs A. Phagocytosis in normal and anaemic blood. J. Clin. Pathol. 1964;17:185–187. doi: 10.1136/jcp.17.2.185. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Komm B.S., Mirkin S. An overview of current and emerging SERMs. J. Steroid Biochem. Mol. Biol. 2014;143:207–222. doi: 10.1016/j.jsbmb.2014.03.003. [DOI] [PubMed] [Google Scholar]
  29. Liebert F. Estimation of nitrogen maintenance requirements and potential for nitrogen deposition in fast-growing chickens depending on age and sex. Poult. Sci. 2006;85:1421–1429. doi: 10.1093/ps/85.8.1421. [DOI] [PubMed] [Google Scholar]
  30. Lin T., Lustig R.H., Chang C. The role of androgens-androgen receptor in immune system activity. Physiol. Immun. 1996;1:263–276. [Google Scholar]
  31. Ma C.-S. Mechanism of difference in growth rate between cockerels and pullets. Poult. Sci. 1954;33:1028–1031. [Google Scholar]
  32. Maiuri M.C., Zalckvar E., Kimchi A., Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol. 2007;8:741–752. doi: 10.1038/nrm2239. [DOI] [PubMed] [Google Scholar]
  33. Malkin C.J., Pugh P.J., Jones R.D., Kapoor D., Channer K.S., Jones T.H. The effect of testosterone replacement on endogenous inflammatory cytokines and lipid profiles in hypogonadal men. J. Clin. Endocrinol. Metabol. 2004;89:3313–3318. doi: 10.1210/jc.2003-031069. [DOI] [PubMed] [Google Scholar]
  34. Mandlekar S., Kong A.-N. Mechanisms of tamoxifen-induced apoptosis. Apoptosis. 2001;6:469–477. doi: 10.1023/a:1012437607881. [DOI] [PubMed] [Google Scholar]
  35. Marin D.P., Bolin A.P., de Cassia Macedo dos Santos R., Curi R., Otton R. Testosterone suppresses oxidative stress in human neutrophils. Cell Biochem. Funct. 2010;28:394–402. doi: 10.1002/cbf.1669. [DOI] [PubMed] [Google Scholar]
  36. Mirzaei M., Bouyeh M., Zahedi A., Seidavi A., Khan R.U., Tufarelli V., Laudadio V., Abd El-Hack M.E., Taha A.E., Swelum A.A. Influence of dietary L-carnitine and lysine–methionine levels on reproductive performance and blood metabolic constituents of breeder ducks. Reprod. Domest. Anim. 2022;57:253–261. doi: 10.1111/rda.14047. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Moreland J.G., Davis A.P., Bailey G., Nauseef W.M., Lamb F.S. Anion channels, including ClC-3, are required for normal neutrophil oxidative function, phagocytosis, and transendothelial migration. J. Biol. Chem. 2006;281:12277–12288. doi: 10.1074/jbc.M511030200. [DOI] [PubMed] [Google Scholar]
  38. Musa H., Chen G., Cheng J., Li B., Mekki D. Study on carcass characteristics of chicken breeds raised. Int. J. Poult. Sci. 2006;5:530–533. [Google Scholar]
  39. Oertelt-Prigione S. The influence of sex and gender on the immune response. Autoimmun. Rev. 2012;11:A479–A485. doi: 10.1016/j.autrev.2011.11.022. [DOI] [PubMed] [Google Scholar]
  40. Olawumi S., Fagbuaro S. Productive performance of three commercial broiler genotypes reared in the derived savannah zone of Nigeria. Int. J. Agric. Res. 2011;6:798–804. [Google Scholar]
  41. Olsen N.J., Kovacs W.J. Gonadal steroids and immunity. Endocr. Rev. 1996;17:369–384. doi: 10.1210/edrv-17-4-369. [DOI] [PubMed] [Google Scholar]
  42. Owen-Ashley N.T., Hasselquist D., Wingfield J.C. Androgens and the immunocompetence handicap hypothesis: unraveling direct and indirect pathways of immunosuppression in song sparrows. Am. Nat. 2004;164:490–505. doi: 10.1086/423714. [DOI] [PubMed] [Google Scholar]
  43. Remijsen Q., Berghe T.V., Wirawan E., Asselbergh B., Parthoens E., De Rycke R., Noppen S., Delforge M., Willems J., Vandenabeele P. Neutrophil extracellular trap cell death requires both autophagy and superoxide generation. Cell Res. 2011;21:290–304. doi: 10.1038/cr.2010.150. [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Rozenboim I., Dgany O., Robinzon B., Arnon E., Snapir N. The effect of Tamoxifen on the reproductive traits in White Leghorn cockerels. Pharmacol. Biochem. Behav. 1989;32:377–381. doi: 10.1016/0091-3057(89)90166-4. [DOI] [PubMed] [Google Scholar]
  45. Scheel-Toellner D., Wang K., Assi L., Webb P., Craddock R., Salmon M. WC1X. Portland Press Ltd. Biochemical Society; London: 2004. p. 0GB. (Clustering of Death Receptors in Lipid Rafts Initiates Neutrophil Spontaneous Apoptosis). [DOI] [PubMed] [Google Scholar]
  46. Schuurhof A., Bont L., Siezen C.L., Hodemaekers H., van Houwelingen H.C., Kimman T.G., Hoebee B., Kimpen J.L., Janssen R. Interleukin-9 polymorphism in infants with respiratory syncytial virus infection: an opposite effect in boys and girls. Pediatr. Pulmonol. 2010;45:608–613. doi: 10.1002/ppul.21229. [DOI] [PubMed] [Google Scholar]
  47. Seidavi A., Tavakoli M., Slozhenkina M., Gorlov I., Hashem N.M., Asroosh F., Taha A., Abd El-Hack M.E., Swelum A.A. The use of some plant-derived products as effective alternatives to antibiotic growth promoters in organic poultry production: a review. Environ. Sci. Pollut. Res. 2021;28:47856–47868. doi: 10.1007/s11356-021-15460-7. [DOI] [PubMed] [Google Scholar]
  48. Seumois G., Fillet M., Gillet L., Faccinetto C., Desmet C., François C., Dewals B., Oury C., Vanderplasschen A., Lekeux P. De novo C16-and C24-ceramide generation contributes to spontaneous neutrophil apoptosis. J. Leukoc. Biol. 2007;81:1477–1486. doi: 10.1189/jlb.0806529. [DOI] [PubMed] [Google Scholar]
  49. Sharma S., Bari V.K., Rawal Y., Paul S., Ganesan K. Sphingolipid biosynthetic pathway genes FEN1 and SUR4 modulate amphotericin B resistance. Antimicrob. Agents Chemother. 2014;58:2409–2414. doi: 10.1128/AAC.02130-13. [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Stossi F., Barnett D.H., Frasor J., Komm B., Lyttle C.R., Katzenellenbogen B.S. Transcriptional profiling of estrogen-regulated gene expression via estrogen receptor (ER) α or ERβ in human osteosarcoma cells: distinct and common target genes for these receptors. Endocrinology. 2004;145:3473–3486. doi: 10.1210/en.2003-1682. [DOI] [PubMed] [Google Scholar]
  51. Sutherland R.L. Estrogen antagonists in chick oviduct: antagonist activity of eight synthetic triphenylethylene derivatives and their interactions with cytoplasmic and nuclear estrogen receptors. Endocrinology. 1981;109:2061–2068. doi: 10.1210/endo-109-6-2061. [DOI] [PubMed] [Google Scholar]
  52. Swelum A.A., Elbestawy A.R., El-Saadony M.T., Hussein E.O., Alhotan R., Suliman G.M., Abd El-Hack M.E. Ways to minimize bacterial infections, with special reference to Escherichia coli, to cope with the first-week mortality in chicks: an updated overview. Poult. Sci. 2021;100 doi: 10.1016/j.psj.2021.101039. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. Swelum A.A., Hashem N.M., Abdelnour S.A., Taha A.E., Ohran H., Khafaga A.F., Abd El-Hack M.E. Effects of phytogenic feed additives on the reproductive performance of animals. Saudi J. Biol. Sci. 2021;28:5816–5822. doi: 10.1016/j.sjbs.2021.06.045. [DOI] [PMC free article] [PubMed] [Google Scholar]
  54. Swelum A.A.A., Hashem N.M., Abo-Ahmed A.I., Abd El-Hack M.E., Abdo M. Heat Shock Proteins in Inflammatory Diseases. Springer, Cham; Midtown Manhattan, New York City: 2020. The role of heat shock proteins in reproductive functions; pp. 407–427. [Google Scholar]
  55. Swerdloff R.S., Wang C. Androgens and aging in men. Exp. Gerontol. 1993;28:435–446. doi: 10.1016/0531-5565(93)90069-p. [DOI] [PubMed] [Google Scholar]
  56. Thutwa K., Nsoso S., Kgwatalala P., Moreki J. Comparative live weight, growth performance, feed intake, carcass traits and meat quality in two strains of Tswana chickens raised under intensive system in south east district of Botswana. Int. J.Appl. Poult. Res. 2012;1:21–26. [Google Scholar]
  57. Trigunaite A., Khan A., Der E., Song A., Varikuti S., Jørgensen T.N. Gr-1highCD11b+ cells suppress B cell differentiation and lupus-like disease in lupus-prone male mice. Arthritis Rheum. 2013;65:2392–2402. doi: 10.1002/art.38048. [DOI] [PubMed] [Google Scholar]
  58. von Köckritz-Blickwede M., Nizet V. Innate immunity turned inside-out: antimicrobial defense by phagocyte extracellular traps. J. Mol. Med. 2009;87:775–783. doi: 10.1007/s00109-009-0481-0. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Wartha F., Henriques-Normark B. ETosis: a novel cell death pathway. Sci. Signal. 2008;1:pe25. doi: 10.1126/stke.121pe25. -pe25. [DOI] [PubMed] [Google Scholar]
  60. Yang X., Li W., Feng Y., Yao J. Effects of immune stress on growth performance, immunity, and cecal microflora in chickens. Poult. Sci. 2011;90:2740–2746. doi: 10.3382/ps.2011-01591. [DOI] [PubMed] [Google Scholar]
  61. Younis M., Ghoneim H. The relationship between sex hormones, immune response and productive performance of broiler chickens. Alexandria J. Vet. Sci. 2022;74(2):40–49. [Google Scholar]
  62. Younis M.E., Aboelnour A., Swelum A.A., Ghoneim H.A., El-Hack M.E.A., Khafaga A.F., Al-Ghadi M.Q., Al-Himadi A.R., Almutairi B.O., Ammari A.A. Impact of oral supplementation of different levels of tamoxifen on productive and reproductive efficiencies and carcass traits of Avian48 and arbor acres broilers. Animals. 2020;10:1367. doi: 10.3390/ani10081367. [DOI] [PMC free article] [PubMed] [Google Scholar]
  63. Younis M.E., Alaryani F.S., Jaber F.A., Aboelnour A., Shukry M., Taha A.E, Abd El-Hack M.E., Abo Ghanima M.M. Impacts of sex steroids and aromatase inhibitor on performances, carcass characteristics and gonadal histology of broiler chickens slaughtered at different ages. Reprod. Domestic Anim. 2022 doi: 10.1111/rda.14215. [DOI] [PubMed] [Google Scholar]

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