Adaptation to Heat Stress in Broilers Using Dried Tomato Pomace and Zinc: Effects on Growth Performance, Oxidative Stress, Intestinal Features and Humoral Immunity

Mehreen Dost Muhammad1, Naila Chand1, Shabana Naz2, Ibrahim A. Alhidary3, Assar Ali Shah4, Rifat Ullah Khan5* and Caterina Losacco6

1Department of Poultry Science, Faculty of Animal Husbandry and Veterinary Sciences, The University of Agriculture, Peshawar, Pakistan

2Department of Zoology, Government College University, Faisalabad, Pakistan

3Department of Animal Production, College of Agriculture and Food science, King Saud University, Riadh, Saudi Arabia

4Institute of Animal Science, Jiangsu Academy of Agriculture Sciences, Nanjing 210093, China

5College of Veterinary Sciences, Faculty of Animal Husbandry and Veterinary Sciences, The University of Agriculture, Peshawar, Pakistan

6Department of Precision and Regenerative Medicine and Jonian Area (DiMePRe-J), Section of Veterinary Science and Animal Production, University of Bari ‘Aldo Moro’, s.p. Casamassima km 3, 70010 Valenzano, Italy

ABSTRACT

Dried tomato pomace (DTP) is a low-cost and nutritionally beneficial byproduct of tomato processing that is obtained during the production of tomato paste. This research aimed to assess the impact of Zinc (Zn) and DTP supplementation on the growth, carcass quality, blood metabolites, intestinal histology and antibody levels in broiler chickens exposed to heat stress. A total of 625 Hubbard broilers were distributed among 25 floor pens, with 25 birds per pen. The birds subjected to heat stress (HS) were provided with a basal diet (control), Zn at a concentration of 50 mg/kg (Zn-50), and two levels of DTP at rates of 10g/kg (DTP-10) and 20g/kg (DTP-20) of feed over a span of 35 days. The results demonstrated significantly higher (P<0.01) total feed consumption, weight gain, and feed conversion ratio for both the DTP-10 and DTP-20 groups as compared to the control group. Additionally, the dressing percentage was also notably higher (P<0.01) in these supplemented groups. Notably, the supplementation of DTP-10 and DTP-20 led to a reduction (P<0.01) in the levels of MDA (malondialdehyde) in the broilers experiencing heat stress. In conclusion, the findings of this study suggest that supplementation with DTP-10 and DTP-20 significantly improved growth performance, lowered MDA, and strengthened humoral immunity in thermal stressed broilers.

Article Information

Received 08 March 2022

Revised 05 September 2023

Accepted 20 September 2023

Available online 07 December 2023

(early access)

Published 05 April 2025

Authors’ Contribution

NC, MDM, RUK: Investigation, data analysis, writing first draft preparation. NC, RUK: Supervision, conceptualization, funding acquisition, data analysis, writing reviewing and editing. SN, NUK: Co-supervision, co-funding. RUK, IA, AAA: Writing reviewing and editing. RUK, IA, AAA: Co-funding, co- conceptualization, writing reviewing and editing. All authors have read and agreed to the published version of the manuscript.

Key words

Antioxidant, Broiler, Dried tomato pomace, Heat stress, Zinc

DOI: https://dx.doi.org/10.17582/journal.pjz/20220308070343

* Corresponding author: rukhan@aup.edu.pk

0030-9923/2025/0002-0879 $ 9.00/00

Copyright 2025 by the authors. Licensee Zoological Society of Pakistan.

This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).

INTRODUCTION

Heat stress is regarded as a severe problem with significant physiological implications for animal performance (Khan et al., 2012; Bai et al., 2023). Lack of sweat glands birds are compelled to rely on open mouth respiration, which can result in terrible physiological disequilibrium (Khan et al., 2011, 2023; Chand et al., 2018; Ahmad et al., 2020; Hafeez et al., 2021). To minimize chicken heat stress, a multidisciplinary approach is used to adjust the environment, ventilation system, and nutritional management (Khan et al., 2021). Vitamins, minerals, and phytochemicals help in order to mitigate the adverse impacts of heat stress (Zia et al., 2017; Sultan et al., 2018; Shah et al., 2023).

Several studies have recognized medicinal herbs as agents that promote growth in broiler chickens (Khan et al., 2012; Ahmad et al., 2020). Medicinal herbs can be used safely in animal and poultry feeds because they are natural products (Khan et al., 2012). Botanicals and their components can assist broiler chicks in growing and remaining healthy without changing their blood profile or generating any visible pathological concerns. This suggests that botanicals are efficient growth promoters that can be substituted for antibiotics (Haq et al., 2020).

Zinc (Zn) is a mineral that is used to combat the effects of environmental stress (Shah et al., 2019). Because Zn is a cofactor for over 200 enzymes, it plays a variety of critical activities. Its presence in the antioxidant defense system is one of their main roles. Free radicals cause oxidative damage to the cell membrane during zinc deficiency (Naz et al., 2016), affecting antioxidant enzymes and substances. It is thought that the antioxidant role of Zn is linked with higher production of metallothionein that act as antioxidant agent (Chand et al., 2020).

The seeds make up 44% of dry tomato pomace (DTP), while the pulp and flesh make up 56%. Seed includes 35.1 % total dietary fibre (TDF), 22.2-33.9 % crude protein (CP), 20.5-29.5 % fat, and 3.9-9.6 % ash, making it an important component of tomato pomace (Silva et al., 2019; Szabo et al., 2019; Concha-Meyer et al., 2020). According to an estimate, one g includes 4.5 % fat, 11 % CP, 0.13 mg of carotene, 0.8 mg of lycopene, and 1.73 mg of vitamin C (Sahin et al., 2008). Lycopene, folate, tocopherols, vitamin C, flavonoids, and phenolics are all antioxidants found in tomato pomace (Sahin et al., 2008; Selim et al., 2013; Khan et al., 2022). Supplementation at a dosage rate of 1% has been found to improve antioxidant potential and lower malondialdehyde (MDA) concentration in broilers grown at high temperatures (Selim et al., 2013). Supplementation of DTP was found to boost growth, immunity, and antioxidant status in many experiments in broilers (Sahin et al., 2008; Abdel-Baset et al., 2009; Palozza et al., 2011; Yitbarek, 2013; Hosseini-Vashan et al., 2016). The impact of DTP on broilers under heat stress has only been studied in a few research reports. Consequently, the goal of this study was to compare DTP and Zn under heat stress to see how it affected growth, redox balance, intestinal histology and immunological response in broilers.

MATERIALS AND METHODS

Preparation of dried tomato pomace powder (DTPP)

Fresh cleaned tomatoes were chopped into small pieces and dried under the shed for two weeks at room temperature and then milled into fine powder.

Animals husbandry and experimental protocol

A total of 625 male Hubbard broiler chicks, each only one day old, was methodically divided into 25 separate floor pens, accommodating 25 birds within each pen. Wood shavings were employed as the bedding material for these pens. To ensure proper sustenance, every pen was equipped with plastic feeders and water dispensers. Throughout the course of the trial, the broiler chickens were granted unrestricted access to both feed and water. Routine vaccinations were administered to safeguard against various diseases, including the New Castle disease virus. The broiler chickens were subjected to continuous illumination lasting 23 h each day. Furthermore, the thermal stress regimen, delineated in Table I, was imposed on the broiler chickens. The fundamental composition of the feed is outlined in Table II.

 

Table I. Thermal stress conditions during the experimental period.

H	Relative humidity (%)	Temperature (°C)
08:00	82.32	34.72
12:00	94.16	35.21
16:00	70.85	38.57
20:00	69.58	35.63
24:00	75.27	33.71
04:00	77.32	31.54

 

Table II. Composition of starter and finisher diets and their chemical composition as fed basis.

Ingredients (%)	Starter phase (1-21 days)	Finisher phase (22-35 days)	Dried tomato pomace
Corn	56.2	55.00
Soybean meal (44%)	29.5	26.5
Canola meal	5.95	5.41
Sunflower meal (28%)	3.5	3.9
Vegetable oil	2.15	2.2
Molasses	1.5	1.00
Dicalcium phosphate	1.8	1.95
Limestone	1.10	1.10
NaCl	0.01	0.01
NaHCO3	0.02	0.01
DL-Methionine	0.15	0.12
Lysine-HCl	0.21	0.33
Vitamins minerals premix1	0.3	0.27
Chemical composition
ME (kcal/kg)	2995	3000
Crude protein (%)	22.5	22.30
Crude protein (%)			22.67
Crude fibre (%)			8.75
Crude fats (%)			8.34

 

Table III. Feed intake, weight gain and feed conversion ratio of broilers under thermal stress and supplemented with dried tomato pomace.

Treatments	Feed intake (kg)			Weight gain (kg)			Feed conversion ratio (kg/kg)
	Starter phase	Finisher phase	Overall	Starter phase	Finisher phase	Overall	Starter phase	Finisher phase	Overall
Control	1.29± 0.01c	1.75± 0.01c	2.84± 0.01c	0.65± 0.01d	1.07± 0.01c	1.72± 0.01d	1.83± 0.01a	1.98± 0.01a	1.65± 0.01a
Zn-50	1.26± 0.01b	1.82± 0.01b	2.95± 0.01b	0.69± 0.01c	1.11± 0.01b	1.82± 0.01c	1.82± 0.01a	1.63± 0.01b	1.62± 0.01b
DTP-10	1.35± 0.01a	1.96± 0.01a	3.15± 0.01a	0.72± 0.01b	1.19± 0.01a	1.97± 0.01b	1.80± 0.01b	1.64± 0.0b	1.59± 0.01b
DTP-20	1.36± 0.01a	1.99± 0.01a	3.09± 0.01a	0.85± 0.01a	1.20± 0.01a	2.02± 0.01a	1.60± 0.01c	1.65± 0.01b	1.52± 0.01c
P value	0.0001	0.0012	0.0001	0.0001	0.001	0.001	0.001	0.0001	0.0001

 

Mean values in the same column with dissimilar superscript are statistically significant (P<0.05). Zn-50, Zn at the rate of 50 mg/kg; DTP-10 and DTP-20 indicate the supplementation of dried tomato pomace at the rate of 10 and 20 g/kg, respectively.

 

Experimental protocols and samplings

Four diets consisting of a control, and two levels of dried tomato pomace (DTP) at the rate of 10 (DTP-10) and 20 (DTP-20) and zinc (Zn-50) at the dose of 50 mg/kg of feed were included and allocated in a completely randomized design for 35 days, except the first week. The supplements were well mixed in the experimental diets. Feed intake was assessed on daily basis while body weight gain and feed conversion ratio (FCR) were assessed on a weekly basis. Three birds per pen were taken and killed on day 35. Dressing percentage was determined for individual birds and pooled on pen basis. Weight of spleen, bursa, and thymus were taken with help of sensitive scale. Blood samples of 3 ml was aseptically taken from the slaughtered birds, centrifuged (3000 rpm for 10 minutes) resulting in the separation of serum, which was stored at -80°C until it analysis.

Serum MD and antibody titre against New Castle disease (NDV)

The thiobarbituric acid (TBA) reaction was used to determine MDA in serum samples as published by Ohkawa et al. (1979). The colour generated was spectrophotometrically quantified at 532nm (IRMECO Model U2020). A haemagglutination inhibition (HI) test was conducted to find the humoral response against the ND virus.

Intestinal histology

Two birds were chosen from each pen, subsequently slaughtered, and their ilium were handled under aseptic conditions for the purpose of conducting histological examinations. To accomplish this, sections measuring 1 cm² were meticulously excised from the ilium and subsequently placed in a solution of 10% buffered formalin. Following this, the tissue samples underwent dehydration using a freshly prepared alcoholic solution. Utilizing a microtome, the tissue blocks were carefully sliced and then subjected to H & E staining. Ultimately, the stained sections were thoroughly examined under a microscope at a magnification of 40x.

Statistical analysis

Data were analysed using statistical analysis software (Statistix 8.1) in a Completely Randomized Design. Means were compared using Tukey test at the level of 5% probability.

RESULTS

Table III presents the impacts of DTP and Zn additives on parameters such as feed intake, body weight gain, and feed conversion ratio (FCR) in broilers experiencing thermal stress. The broiler chicks in the DTP-10 and DTP-20 groups exhibited the most substantial (P<0.01) average feed intake values throughout the starter, finisher, and entire growth phases. Conversely, the control group displayed the lowest feed intake levels. Notably, the total feed consumption was significantly higher (P<0.01) in the DTP-10 and DTP-20 groups over the entire duration of the study, followed by the Zn-50 group. Conversely, overall feed intake was the lowest in the the control group.

In the initial phase, the DTP-20 group exhibited a higher weight gain (P<0.05), while the control group displayed a notably smaller weight gain (P<0.01). In the final phase, both the DTP-10 and DTP-20 groups demonstrated significantly larger weight gains (P<0.01) when compared to the control group, with the Zn-50 group following suit. When considering the overall weight gain, both the DTP-10 and DTP-20 groups exhibited higher values (P<0.01), followed by the Zn-50 group, in contrast to the control group.

During the initial phase, the DTP-20 group exhibited a significantly lower (P<0.01) and comparable feed conversion ratio (FCR), whereas both the control group and Zn-50 group displayed poorer FCR. Upon comparing all treatment groups to the control group in the concluding phase, there was an improvement in FCR (P<0.05). In general, higher mean FCR values were observed in the DTP-20 group, followed by the DTP-10 and Zn-50 groups. Conversely, the control group exhibited a lower FCR value.

Table IV depicts the impact of DTP and Zn supplementation on variables including dressing percentage, as well as the weights of the immune organs. Remarkably, the DTP-10 group exhibited significantly higher dressing percentages (P<0.01) compared to the DTP-20 group, followed by the Zn-50 group. Conversely, the control group presented the lowest dressing percentage values (P<0.01). It’s noteworthy to mention that no significant changes were observed in the weights of the spleen, bursa, and thymus across the treatment groups.

Table IV illustrates the serum concentrations of MDA, and HI titres against New Castle disease (ND) in broilers facing thermal stress. Notably, the inclusion of DTP-10 and DTP-20 supplements led to a significant reduction in MDA levels among heat-stressed broilers (P<0.01). Among the treatment groups, the control group showed the lowest mean MDA value. Regarding antibody titers, the DTP-10 group displayed the highest levels, followed by the DTP-20 and Zn-50 groups, respectively.

Table V show the effect of supplements on the intestinal histology of broilers under heat stress. No significant change was observed in intestinal dimensions of broilers in the control and treatment groups.

DISCUSSION

This study reveals that ambient temperature exerts a detrimental impact on broiler development, antioxidant status, and immunological response. However, the introduction of DTP supplementation has shown to mitigate these adverse effects. Specifically, the DTP-10 and DTP-20 groups exhibited notably higher total mean feed consumption in comparison to the control group. This corroborates with previous findings from studies such as Abdel-Baset et al. (2009) and Yitbarek (2013). Moreover, similar positive outcomes were observed in terms of weight gain, where the DTP-10 and DTP-20 groups displayed significant improvements in broilers subjected to heat stress when contrasted with the control group.

The disposal of DTP has emerged as an environmental concern in multiple countries. Elevated ambient temperatures have been found to detrimentally affect broiler development, antioxidant status, and immunological responses, as evidenced by this study. However, the supplementation of DTP has shown promise in alleviating these adverse effects.

 

Table IV. Dressing percentage and weight of spleen, bursa and thymus, MDA, and ND titre of broilers supplemented with Zn and dried tomato pomace (DTP) under thermal stress. The values are Mean±SEM.

Groups	Dressing percentage	Spleen weight (g)	Bursa weight (g)	Thymus weight (g)	MDA (nmole/ml)	ND Titer (Log10)
Control	59.77±0.64b	0.11±0.01	0.10±0.01	0.22±0.01	1.97±0.26a	4.33±0.33c
Zn-50	60.43±0.81b	0.12±0.01	0.11±0.01	0.22±0.01	1.37±0.2b	4.66b±0.33c
DTP-10	64.75±0.5a	0.13±0.01	0.12±0.01	0.22±0.01	1.20±0.31c	6.66±0.33a
DTP-20	64.39±0.580a	0.12±0.01	0.11±0.01	0.21±0.01	1.10±0.27c	5.66±0.33b
P value	0.00002	0.0030	0.0007	0.0000	0.0000	0.0044

 

Within the same column mean values having different superscripts are significantly different (P<0.05). Zn-50, Zn at the rate of 50 mg/kg; DTP-10 and DTP-20 indicate the supplementation of dried tomato pomace at the rate of 10 and 20 g/kg, respectively.

 

Table V. Villus dimensions of broilers supplemented with Zn and dried tomato pomace (DTP) under thermal stress. The values are Mean±SEM.

Groups	Villus height (µm)	Villus width (µm)	Crypt depth (µm)	Villus height to crypt depth ratio
Control	851.67±4.87	179.12±3.98	200.43±4.87	4.23±2.12a
Zn-50	823.36±2.34	1180.17±1.34	210.23±4.43	4.55±2.11e
DTP-10	856.67±0.88	182.37±2.43	204.45±4.26	4.65±2.11b
DTP-20	845.00±3.48	181.12±3.67	211.76±4.35	4.60±02.22d
P value	0.324	0.650	0.08	0.07

 

In the context of this study, both the DTP-10 and DTP-20 groups exhibited significantly higher total mean feed consumption compared to the control group. Similar findings have been documented previously, echoing the works of Abdel-Baset et al. (2009) and Yitbarek (2013). Moreover, DTP-10 and DTP-20 supplementation led to substantial increases in weight gain among broilers exposed to heat stress, in contrast to the control group. However, in the realm of feeding rabbits, tomato pomace led to a remarkable 20% improvement in feed conversion ratio, as observed by Abdel-Azeem et al. (2009). The outcomes of this current study lend support to such assertions.

The mean dressing percentage exhibited an increase in both the DTP-10 and DTP-20 groups, while it decreased in the control group. The principal factors influencing higher FCR in the respective groups can be attributed to weight gain and FCR. The observed augmented feed intake and efficiency could be attributed to the presence of lysine in tomato pomace, a crucial amino acid that stimulates the synthesis of body muscle protein and consequently enhances weight growth. One hypothesis posits that the elevated feed intake might be linked to the elevated fiber content in the diets, which could potentially cause an expansion of the digestive tissue due to prolonged meal retention time for digestion, an idea in line with the work of Colombino et al. (2020).

In this particular study, the HI (hemagglutination inhibition) titers against New Castle disease virus (NDV) were notably higher in the DTP-10 group compared to the control group. This phenomenon could potentially be attributed to the presence of lutein in tomatoes. Lutein, functioning as a carotenoid, is known to modulate immune responses by enhancing immunological activity and promoting the proliferation of lymphocytes (Ribaya-Mercado et al., 2004).

The impact of DTP on antibody titers during instances of heat stress has been explored in only a limited number of cases. For instance, Selim et al. (2013) reported that tomato puree augmented humoral immunity against NDV in broilers subjected to thermal stress. Similarly, Hosseini-Vashan et al. (2016) found that administering DTP to broilers led to an increase in the production of antibodies against NDV during heat stress.

The observed elevation in antibody titers among groups supplemented with tomato pomace may be attributed to the presence of lutein in tomatoes. Lutein, a carotenoid, exerts an influence on the immune system by enhancing immune functionality and promoting the proliferation of lymphocytes, thereby elevating antibody titers against NDV (Ribaya-Mercado et al., 2004). Additionally, the presence of genistein, another substance found in tomato pomace, has been noted to increase the relative weight of lymphoid organs, consequently intensifying their responsiveness to antibodies against viral antigens. Genistein has been found to enhance immunological capacity and elevate blood lymphocyte counts in broilers (Rasouli and Janania, 2015).

Our research aligns with their discoveries. Our study indicates significantly reduced MDA levels in both the DTP-10 and DTP-20 groups. Tomato-based products have been shown to enhance the body’s antioxidant capacity and influence the status of these essential constituents within the body, as noted by Sahin et al. (2008). Lycopene, a primary carotenoid present in tomatoes, has the capacity to scavenge harmful free radicals and curtail the generation of reactive oxygen species, as highlighted by Palozza et al. (2011). This investigation also resonates with Sahin et al. (2011), who found that supplementing quails exposed to thermal stress with tomato pomace led to a reduction in liver MDA concentration and an increase in liver lycopene levels, along with heightened concentrations of antioxidant enzymes.

Lycopene found in tomato pomace has demonstrated the capability to upregulate key components of the antioxidant response. It triggers the synthesis of antioxidant enzymes, which collectively play a protective role against cellular damage from free radicals (Sahin et al., 2014). Saed et al. (2018) reached similar conclusions, observing that the inclusion of one percent tomato puree in the diets of broiler chicks exposed to high-temperature conditions resulted in improved antioxidant capacity and lowered MDA values. These outcomes also correspond with the findings of Hosseini-Vashan et al. (2016), who documented that supplementing broiler with 5% DTP led to decreased levels of plasma MDA. Sahin et al. (2011) further reinforced these findings by indicating that tomato powder supplementation enhanced the activity of antioxidant enzymes in the livers of thermally stressed quails.

CONCLUSION

From the results of the present study, we concluded that DTP-10 and DTP-20 enhanced the growth performance and MDA status and humoral immunity in broilers exposed to heat stress.

Acknowledgments

Authors are thankful to their respective institutions for support to carry out this study.

Funding

We extend our appreciation to the Researchers Supporting Project (No. RSPD2025R833), King Saud University, Riyadh, Saudi Arabia.

Ethical statement and IRB approval

This study has been approved by the departmental committee on ethics and animal welfare the University of Agriculture, Peshawar (12/PS/2020).

Competing interest

There is no potential competing interest with this study.

Consent to participate and consent to publish

All the authors have equally participated in this study and agreed to publish this work in this journal.

Data availability

Data is available in the thesis.

Statement of conflict of interest

The authors have declared no conflict of interest.

REFERENCES

Abdel-Baset, N.S. and Azeem, A.M.A., 2009. Evaluation of dried tomato pomace as feedstuff in the diets of growing rabbits. Int. J. Agro Vet. Med. Sci., 3: 12-18.

Ahmad, M., Chand, N., Khan, R.U., Ahmad, N., Khattak, I. and Naz, S., 2020. Dietary supplementation of milk thistle (Silybum marianum): growth performance, oxidative stress and immune response in natural summer stressed broilers. Trop. Anim. Hlth. Prod., 52: 711-715. https://doi.org/10.1007/s11250-019-02060-4

Bai, X., Wang, K., Khan, R.U., Zhang, C. and Hu, H., 2023. Effect of glutamine on the growth performance, oxidative stress, and Nrf2/p38 MAPK expression in the livers of heat-stressed broilers. Animals, 13: 652. https://doi.org/10.3390/ani13040652

Chand, N., Ali, P., Alhidary, I.A., Abelrahman, M.M., Albadani, H., Khan, M.A., Seidavi, A., Laudadio, V., Tufarelli, V. and Khan, R.U., 2021. Protective effect of grape (Vitis vinifera) seed powder and zinc-glycine complex on growth traits and gut health of broilers following Eimeria tenella challenge. Antibiotics, 10: 186. https://doi.org/10.3390/antibiotics10020186

Chand, N., Faheem, H., Khan, R.U., Qureshi, M.S., Alhidary, I.A. and Abudabos, A.M., 2016. Anticoccidial effect of mannanoligosacharide against experimentally induced coccidiosis in broiler. Environ. Sci. Poll. Res., 23: 14414-14421. https://doi.org/10.1007/s11356-016-6600-x

Chand, N., Naz, S., Zia ur Rehman and Khan, R.U., 2018. Blood biochemical profile of four fast-growing broiler strains under high ambient temperature. Appl. Biol. Chemist., 61: 273-279. https://doi.org/10.1007/s13765-018-0358-4

Chand, N., Zahirullah, Khan, R.U., Shah, M., Naz, S. and Tinelli, A., 2020. Zinc source modulates zootechnical characteristics, intestinal features, humoral response and paraoxonase (PON1) activity in broilers. Trop. Anim. Hlth. Prod., 52: 511-515. https://doi.org/10.1007/s11250-019-02036-4

Colombino, E., Ferrocino, I., Biasato, I., Cocolin, L.S., Prieto-Botella, D., Zduńczyk, Z., Jankowski, J., Milala, J., Kosmala, M., Fotschki, B. and Capucchio, M.T., 2020. Dried fruit pomace inclusion in poultry diet: Growth performance, intestinal morphology and physiology. J. Anim. Sci. Biotechnol., 11: 1-17. https://doi.org/10.1186/s40104-020-00464-z

Concha-Meyer, A., Palomo, I., Plaza, A., Gadioli Tarone, A., Junior, M.R.M., Sáyago-Ayerdi, S.G. and Fuentes, E., 2020. Platelet anti-aggregant activity and bioactive compounds of ultrasound-assisted extracts from whole and seedless tomato pomace. Foods, 9: 1564. https://doi.org/10.3390/foods9111564

Hafeez, A., Akram, W., Sultan, A., Konca, Y., Ayasan, T., Naz, S., Shahzada, W. and Khan, R.U., 2021. Effect of dietary inclusion of taurine on performance, carcass characteristics and muscle micro-measurements in broilers under cyclic heat stress. Ital. J. Anim. Sci., 20: 872-877. https://doi.org/10.1080/1828051X.2021.1921627

Hafeez, A., Sohail, M., Ahmad, A., Shah, M., Din, S., Khan, I., Shuib, M., Nasrullah, Shahzada, W., Iqbal, M. and Khan, R.U., 2020. Selected herbal plants showing enhanced growth performance, ileal digestibility, bone strength and blood metabolites in broilers. J. appl. Anim. Res., 48: 448-453. https://doi.org/10.1080/09712119.2020.1818569

Haq, I., Hafeez, A. and Khan, R.U., 2020. Protective effect of Nigella sativa and Saccharomyces cerevisiae on zootechnical characteristics, fecal Escherichia coli and hematopoietic potential in broiler infected with experimental Colibacillosis. Livest. Sci., 239:104119. https://doi.org/10.1016/j.livsci.2020.104119

Hosseini-Vashan, S.J., Golian, A. and Yaghobfar, A., 2016. Growth, immune, antioxidant, and bone responses of heat stress-exposed broilers fed diets supplemented with tomato pomace. Int. J. Biometeorol., 60: 1183-1192. https://doi.org/10.1007/s00484-015-1112-9

Khan, R.U., Naz, S., Nikousefat, Z., Selvaggi, M., Laudadio, V. and Tufarelli, V., 2012. Effect of ascorbic acid in heat-stressed poultry. World’s Poult. Sci. J., 68: 477-490. https://doi.org/10.1017/S004393391200058X

Khan, R.U., Naz, S., Nikousefat, Z., Tufarelli, V., Javdani, M., Rana, N. and Laudadio, V., 2011. Effect of vitamin E in heat-stressed poultry. World’s Poult. Sci. J., 67: 469-478. https://doi.org/10.1017/S0043933911000511

Khan, R.U., Naz, S., Nikousefat, Z., Tufarelli, V., Javdani, M., Qureshi, M.S. and Laudadio, V., 2012. Potential applications of ginger (Zingiber officinale) in poultry diets. World’s Poult. Sci. J., 68: 245-252. https://doi.org/10.1017/S004393391200030X

Khan, R.U., Khan, A., Naz, S., Ullah, Q., Laudadio, V., Tufarelli, V. and Ragni, M. 2021. Potential applications of Moringa oleifera in poultry health and production as alternative to antibiotics: a review. Antibiotics, 10: 1540. https://doi.org/10.3390/antibiotics10121540

Khan et al. 2022: Khan, R.U., Fatima, A., Naz, S., Ragni, M., Tarricone, S. and Tufarelli, V. 2022. Perspective, opportunities and challenges in using fennel (Foeniculum vulgare) in poultry health and production as alternative to antibiotics: a review. Antibiotics, 11: 278. https://doi.org/10.3390/antibiotics11020278

Khan, R.U., Naz, S., Ullah, H., Ullah, Q., Laudadio, V., Bozzo, G. and Tufarelli, V., 2023. Physiological dynamics in broiler chickens during heat stress and possible mitigation strategies. Anim. Biotechnol., 34: 438-447. https://doi.org/10.1080/10495398.2021.1972005

Khan, R.U., Shabana, N. and Kuldeep, D., 2014. Chromium: pharmacological applications in heat-stressed poultry. Int. J. Pharmacol., 10: 213-217. https://doi.org/10.3923/ijp.2014.213.217

Mackness, M.I., Arrol, S. and Durrington, P.N., 1991. Paraoxonase prevents accumulation of lipoperoxides in low-density lipoprotein. FEBS Lett., 286: 152-154. https://doi.org/10.1016/0014-5793(91)80962-3

Mezbani, A., Kavan, B.P., Kiani, A. and Masouri, B., 2019. Effect of dietary lycopene supplementation on growth performance, blood parameters and antioxidant enzymes status in broiler chickens. Livest. Res. Rural, 31: Article #12.

Naz, S., M. Idris, M.A. Khalique, Zia-ur-Rahman, I.A. Alhidary, M.M. Abdelrahman, R.U. Khan, N. Chand, U. Farooq and S. Ahmad, 2016. The activity and use of zinc in poultry diet. World’s Poult. Sci. J., 72: 159-167.

Ohkawa H., Ohishi, N. and Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal. Biochem., 95: 351-358.

Palozza, P., Parrone, N., Simone, R. and Catalano, A., 2011. Role of lycopene in the control of ROS-mediated cell growth: Implications in cancer prevention. Curr. Med. Chem., 18: 1846-1860. https://doi.org/10.2174/092986711795496845

Rasouli E. and Jahanian R., 2015. Improved performance and immunological responses as the result of dietary genistein supplementation of broiler chicks. Animals, 9: 1473–1480.

Rehman, Z.U., Chand, N., Khan, R.U., Khan, S. and Qureshi, M.S., 2018. An assessment of the growth and profitability potential of meat-type broiler strains under high ambient temperature. Pakistan J. Zool., 50: 429-435. https://doi.org/10.17582/journal.pjz/2018.50.2.429.435

Rehman, Z.U., Chand, N., Khan, R.U., Naz, S. and Alhidary, I.A., 2018. Serum biochemical profile of two broiler strains supplemented with vitamin E, raw ginger (Zingiber officinale) and L-carnitine under high ambient temperatures. S. Afr. J. Anim., 48: 935-942. https://doi.org/10.4314/sajas.v48i5.13

Ribaya-Mercado, J.D. and Blumberg, J.B., 2004. Lutein and zeaxanthin and their potential roles in disease prevention. J. Am. Coll. Nutr., 23: 567S-587S. https://doi.org/10.1080/07315724.2004.10719427

Saed, Z.J., Abdulateef, S.M., Mohammed, T.T. and Al-Khalani, F.M.H., 2018. Effect of dried tomato pomace as alternative to vitamin C supplemented diets in hematological indices and oxidative stability of egg yolk of laying hens in high-ambient temperature. Biochem. Cell. Arch., 18: 1647-1652.

Safiullah, Chand, N., Khan, R.U., Naz, S., Ahmad, M. and Gul, S., 2019. Effect of ginger (Zingiber officinale Roscoe) and organic selenium on growth dynamics, blood melanodialdehyde and paraoxonase in broilers exposed to heat stress. J. appl. Anim. Res., 47: 212-216. https://doi.org/10.1080/09712119.2019.1608211

Sahin, K., Orhan, C., Akdemir, F.A.T.İ.H., Tuzcu, M., Ali, S. and Sahin, N., 2011. Tomato powder supplementation activates Nrf-2 via ERK/Akt signaling pathway and attenuates heat stress-related responses in quails. Anim. Feed Sci. Technol., 165: 230-237. https://doi.org/10.1016/j.anifeedsci.2011.03.003

Sahin, K., Yazlak, H., Orhan, C., Tuzcu, M., Akdemir, F. and Sahin, N., 2014. The effect of lycopene on antioxidant status in rainbow trout (Oncorhynchus mykiss) reared under high stocking density. Aquaculture, 418: 132-138. https://doi.org/10.1016/j.aquaculture.2013.10.009

Sahin, N., Orhan, C., Tuzcu, M., Sahin, K. and Kucuk, O., 2008. The effects of tomato powder supplementation on performance and lipid peroxidation in quail. Poult. Sci., 87: 276-283. https://doi.org/10.3382/ps.2007-00207

Selim, N.A., Youssef, S.F., Abdel-Salam, A.F. and Nada, S.A., 2013. Evaluations of some natural antioxidant sources in broiler diets: 1-effect on growth, physiological and immunological performance of broiler chicks. Int. J. Poult. Sci., 12: 561-571. https://doi.org/10.3923/ijps.2013.561.571

Shah, M., Chand, N., Khan, R.U., Saeed, M., Ragni, M., Tarricone, S., Laudadio, V., Losacco, C. and Tufarelli, V., 2022. Mitigating heat stress in broiler chickens using dietary onion (Allium cepa) and ginger (Zingiber officinale) supplementation. S. Afr. J. Anim., 52: 811-818. https://doi.org/10.4314/sajas.v52i6.07

Silva, P.A. Y., Borba, B.C., Pereira, V.A., Reis, M.G., Caliari, M., Brooks, M.S.L. and Ferreira, T.A., 2019. Characterization of tomato processing by-product for use as a potential functional food ingredient: Nutritional composition, antioxidant activity and bioactive compounds. Int.J. Fd. Sci. Nutr., 70: 150-160. https://doi.org/10.1080/09637486.2018.1489530

Sultan, A., Ahmad, S., Khan, S., Khan, R.U., Chand, N., Tahir, M. and Shakoor, A., 2018. Comparative effect of zinc oxide and silymarin on growth, nutrient utilization and hematological parameters of heat distressed broiler. Pakistan J. Zool., 50: 751-756. https://doi.org/10.17582/journal.pjz/2018.50.2.751.756

Szabo, K., Diaconeasa, Z., Cătoi, A.F. and Vodnar, D.C., 2019. Screening of ten tomato varieties processing waste for bioactive components and their related antioxidant and antimicrobial activities. Antioxidants, 8: 292. https://doi.org/10.3390/antiox8080292

Yitbarek, M.B., 2013. The effect of feeding different levels of dried tomato pomace on the performance of Rhode Island Red (RIR) grower chicks. Int. J. Livest. Prod., 4: 35-41. https://doi.org/10.5897/IJLP12.034

Zia, R.N. Chand, S. Khan and R.U. Khan. 2017. Evaluating the immune response and antioxidant potential in four broiler strains under chronic high ambient temperature. Pakistan J. Zool., 49: 2087-2091.