Science of the Total Environment 703 (2020) 134399

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Science of the Total Environment

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Review Herbs as thermoregulatory agents in poultry: An overview ⇑ Mohamed E. Abd El-Hack a, , Sameh A. Abdelnour b, Ayman E. Taha c, Asmaa F. Khafaga d, Muhammad Arif e, Tugay Ayasan f, Ayman A. Swelum g, Mohammad H. Abukhalil h,i, Saad Alkahtani j, Lotfi Aleya k,*, Mohamed M. Abdel-Daim j,l a Department of Poultry, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt b Department of Animal Production, Faculty of Agriculture, Zagazig University, Zagazig 44511, Egypt c Department of Animal Husbandry and Animal Wealth Development, Faculty of Veterinary Medicine, Alexandria University, Edfina 22758, Egypt d Department of Pathology, Faculty of Veterinary Medicine, Alexandria University, Edfina 22758, Egypt e Department of Animal Sciences, College of Agriculture, University of Sargodha, 40100, Pakistan f East Mediterranean Agricultural Research Institute, Adana, Turkey g Department of Theriogenology, Faculty of Veterinary Medicine, Zagazig University, Zagazig 44511, Egypt h Department of Biology, Faculty of Science, Al-Hussein Bin Talal University, Ma’an 71110, Jordan i Department of Medical Analysis, Princess Aisha Bint Al-Hussein Faculty of Nursing and Health Sciences, Al-Hussein Bin Talal University, Ma’an 71110, Jordan j Department of Zoology, Science College, King Saud University, Riyadh 11451, Saudi Arabia k Chrono-Environnement Laboratory, UMR CNRS 6249, Bourgogne Franche-Comté University Besançon Cedex, France l Pharmacology Department, Faculty of Veterinary Medicine, Suez Canal University, Ismailia 41522, Egypt highlights graphical abstract

High temperature leads to severe economic loss in poultry production. Some herbs are supplemented to reduce the deleterious influences of heat stress. Thermoregulatory herbs alleviate heat stress-associated deleterious effects.

article info abstract

Article history: The adverse effect of increased environmental temperature during summer season on avian industry has Received 18 July 2019 received great global concern. High temperature leads to severe economic loss in poultry production, Received in revised form 28 August 2019 because it is considered as valuable stress factor. Several practical methods were used to alleviate the Accepted 9 September 2019 adverse impact of increased temperature; among them were dietary modifications. So, several types of Available online 12 September 2019

Abbreviations: ROS, radical oxygen species; NADPH, nicotinamide adenine dinucleotide phosphate; MDA, malondialdehyde; AST, aspartate aminotransferase; ALT, alanine aminotransferase; ALP, alkaline phosphatase; SOD, superoxide dismutase; HSP70, heat stress protein 70; HSP90, heat stress protein 70; SIRT1, sirtuin; AvUCP, avian uncoupling protein; PGC-1 a, peroxisome proliferator-activated receptor gamma coactivator 1-alpha; BWG, body weight gain; FI, feed intake; FCR, feed conversion ration; GSH, glutathione; GPX, glutathione peroxidase; HDL-C, high density lipoprotein C; LDL-C, high density lipoprotein C; IL-2, interleukin-2; IL-4, interleukin-4; RH, relative humidity; Nrf2, nuclear factor (erythroid-derived 2)-like 2; T3, triiodothyronine; T4, thyroxine; GB, Ginkgo biloba; RES, resveratrol; LE, licorice extract; PUFA, poly unsaturated fatty acids. ⇑ Corresponding authors. E-mail address: lotfi[email protected] (L. Aleya). https://doi.org/10.1016/j.scitotenv.2019.134399 0048-9697/Ó 2019 Elsevier B.V. All rights reserved. 2 M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399

herbs are supplemented to reduce the deleterious influences of thermal stress altitudes in various ani- Editor: Damia Barcelo mals, and even to prevent their adverse impacts. Therefore, sustainable supports for dietary modification based on herbs supplementations are largely needed, particularly when consider the additional advan- Keywords: tages of herbs such as availability, actual efficiency, low cost, as well as their free from residual impact Herbs and antibiotic resistance. Numerous types of herbs were concluded to their efficient properties by poultry Heat stress breeders to overcome a variety of the harmful effects of high ambient temperature. The present article Thermoregulatory agents deliberates the different practical applications of several members of the traditional herbal wealth to Poultry improve the general health state of poultry particularly as thermoregulatory and immunomodulatory agents, and for countering the heat stress-associated immunosuppressive effects. Additionally, the antioxidant activity of herbal growth promoters and their influence on improvement of production per- formances were a special aim of this review. The reported information will be helpful for improvement of general production and health status of birds reared under the heat stress via enhancement of immune response and stress tolerance, and popularizes usage of herbs amongst poultry producers. Ó 2019 Elsevier B.V. All rights reserved.

Contents

1. Introduction ...... 2 2. Mode of action ...... 3 3. Thermoregulatory role of some herbs...... 3 3.1. Black seed:...... 3 3.2. Ginger ...... 6 3.3. Artemisia annua L. (A. annua)...... 7 3.4. Fennel (Foeniculum vulgare Mill.) ...... 10 3.5. Hot red pepper ...... 10 3.6. Thyme ...... 10 3.7. Rosemary ...... 11 3.8. Dill ...... 11 3.9. Chicory ...... 11 3.10. Radix bupleuri...... 11 3.11. Moringa (Moringa oleifera)...... 12 3.12. Scutellaria baicalensis L...... 12 3.13. Curcuma xanthorrhiza ...... 12 3.14. Coriander seed...... 13 3.15. Cinnamon (Cinnamomum zeylanicum L.)...... 13 3.16. Licorice (Glycyrrhiza glabra)...... 13 3.17. Ginkgo biloba ...... 14 3.18. Resveratrol...... 14 4. Conclusion ...... 15 Declaration of Competing Interest ...... 15 Acknowledgment ...... 15 References ...... 15

1. Introduction genic additives; which were received great concern due to their safety, availability, low cost and their potential antioxidant effec- Currently, the global increase in environmental temperature tiveness against heat stress (Wan et al., 2017, 2018; Farghly becomes obvious serious challenge influencing the poultry indus- et al., 2018b). Commonly, avoiding the negative effects of heat try in tropical and subtropical countries. In poultry, when the stress is based on providing shade and evaporative cooling in pens ambient environmental temperature exceeds the thermo-neutral via soakers and fans (Collier et al., 2006). However recently, several zone (16–25 °C), the thermal injury initiated (Mehaisen et al., management strategies are applied during the thermal stress such 2017; Abd El-Hack et al., 2018; El-Kholy et al., 2018). During sum- as elevation of the nutrient density and diet energy (Wang et al., mer season, increased ambient temperature is able to induce ther- 2010), and dietary supplementation of various feed additives mal stress in farm animals all over the world; such stress is usually (Zimbelman et al., 2013; Alagawany et al., 2017; El-Kholy et al., related to increased body temperature, reduced growth and pro- 2018) or medical additives (Liu et al., 2013). Thus, extensive con- duction, as well as metabolic and oxidative alterations (Belhadj cern is paid for the dietary addition of various herbal feed additives Slimen et al., 2014; Daader et al., 2016; Farghly et al., 2018a; to resist the adverse impacts of increased environmental tempera- Abdelnour et al., 2019). Dietary modulation is an accepted applica- ture and enhancing the production and performance in poultry tion that developed to ameliorates the adverse impacts of thermal (Wang et al., 2008), rabbits (Liu et al., 2011), and pigs (Dong injury in poultry; including dietary inclusion of vitamins, minerals, et al., 2012). The advantage of these additives could be represented amino acids, and the phytogenic feed additives (Sahin et al., 2009; through their pharmacological and nutritional values, and through Khan et al., 2012a; Del Vesco et al., 2015; Hosseini-Vashan et al., absence of their side or residual effects compared to other feed 2015b, 2015a), among these feed additive there are natural phyto- additives (Wang et al., 2011). Additionally, some of these herbal M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 3 additives were concluded to their improvement effect on produc- 3. Thermoregulatory role of some herbs tion and lactation. So, development of novel effective herbal addi- tives or plant metabolites to mitigate environmentaly-induced 3.1. Black seed: hyperthermia became urgently needed. Moreover, the medicinal herbal therapy is now practiced globally for small livestock farms; Nigella sativa (N. sativa), or black seed, is an annually growing they also used commonly by veterinarians to ameliorates various flowering plant, which has grown to 20–30 cm tall and planted diseases of animals (Dhama et al., 2015). Improvements were in Asia and the Middle East (Khare, 2004). The flowers of this plant noticed in animals suffering harmful sequence of heat stress by are very delicate, pale and white colored. Nigella sativa have been dietary manipulation of some herbs such as (Black seed, Ginger, used intensively by people in Middle East and are commonly used Artemisia annua, Fennel, Hot red pepper, Thyme, Rosemary, Dill, in the kitchen. Also, it was added in many recipes because of its Chicory, Radix bupleuri, Moringa). The purpose of this paper is to valuable remedy effect in several diseases. A number of studies provide an overview of the published data concerning the general were investigated Nigella sativa as feed additives in ruminant diets. applications of herbs or their active compounds against the harm- The seeds of Nigella sativa composed of protein (20–27%), fat (34.5– ful impacts of heat stress in poultry industry (Figs. 1–6 and 38.7%), carbohydrates (23.5–33.2%) crude fire (8.4%), and ash Table 1). (4.8%) (Babyan et al., 1978). The seeds also contain good amount of various vitamins and minerals like Zn, Cu, P, and F as well as car- 2. Mode of action otene, which converts by the liver to vitamin A (Ahmad et al., 2013). The Nigella sativa containing an active materials namely Concerning mode of action, it was suggested that dietary sup- nogelleone, thymoquinome, and thymohdroquinone that is able plementation of phytogenic plants can exert their efficient health to exert antitoxic and antimicrobial properties via increasing the supporting activity via promotion of the antioxidant system; they defense mechanisms against infectious diseases (Forouzanfar are able to directly scavenging the stress-related ROS production et al, 2014). through inhibition of enzymes or trace metals chelating (Thring In heat stressed pigeon, supplementation of black seed (2%) et al., 2011). Likewise, they have the ability to activate the antiox- found to possess a protective effect against hepatic lesions; where idant enzymes and inhibit the pro-oxidant enzymes including mild hepatocyte vacuolization and vascular congestion are noticed, lipoxygenase and NADPH oxidase. Schewe et al. (2008) reported without infiltration for inflammatory cells or damage for sinusoids. that phytogenic herbals could be acted via elevation of uric acid Additionally, black seed supplementation produced significant levels and amelioration of free radicals induced-oxidative injury. increase in weight gain and body weight compared to control or

Fig. 1. Multi-faceted strategies adopted by poultry to overcome heat stress. 4 M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399

Fig. 2. Diagram showing the contribution of different herbs to improve the general health state of poultry particularly as thermoregulatory and immunomodulatory agents, and for countering the heat stress-associated immunosuppressive effects.

heat stressed group (El-Shoukary et al., 2018). Pigeons supple- leinolenic acids; where these acids are required for growth. More- mented with dietary black seed under heat stress conditions over, presence of nigella, thymoquinone, and thymohydoquinone (34 °C) elucidated significant increase in feed intake (189.4% vs found to exert additional pharmacological and antimicrobial control) and feeding behavior, with a significant down regulation action. In broiler, addition of 10% Nigella sativa meal or 1.0% Nigella in feed conversion ratio and the aggressivity (Durrani et al., sativa seed or 0.5% Nigella sativa oil in heat stressed-broiler diets 2007; Gilani et al., 2004; El-Shoukary et al., 2018). These conse- had enhanced the productive traits, livability, carcass traits, appar- quences may attribute to the stimulative effect of dietary black ent digestibility and economic return. Meanwhile, (Shewita and seed on digestive enzymes activities, enhancement of diet palata- Taha, 2011) reported that the increased levels of N. Sativa above bility, and improvement of animals appetite (Shewita and Taha, 6 g/kg diet had significant negative impact on growth performance 2011; Arif et al., 2019). Likewise, black seed has a potential protec- parameters such as body weight, weight gain, relative growth rate tive effect against the adverse influence of pathogens in the diges- and FCR of broilers chicks. In Cobb broilers raised in hot tropical tive system by dint of their containing of high level of essential oils, conditions, Ali et al. (2014) reported that inclusion of Nigella sativa which leading to enhancement of carcass traits, feed consumption, at 0.5% added with 500 ppm vitamin C significantly decreased HDL and feed conversion ratio (Gilani et al., 2004). These findings were and increased H/L ratio and concluded that the higher levels of related to the significant elevation in the total antioxidant poten- black cumin feeding (0.75 and 1%) combined with additional vita- tial, and significant reduction in levels of cholesterol, catalase, min C 500 ppm had similar impact on growth performances as well and glucose. The previous findings suggested that black seed is as blood lipids compared to control birds. able to practice many therapeutic effects such as antihistaminic, El-Shoukary et al. (2014) concluded significant increase in feed antioxidant (Guler et al., 2007; Kanter et al., 2006) and hepatopro- intake, dressing percentage, and daily body gain, while there was tective properties (Al-Ghamdi, 2003; Kanter et al., 2005). Hassan significant decline in panting behavior, water to feed ratio, corti- et al. (2004) attributed such effects to the increased content of costerone and T3 levels as affected by dietary inclusion of 1% unsaturated fatty acids in black seed including linoleic, oleic, and Nigella Sativa seeds (black seed) to broiler diet under summer heat M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 5

Fig. 3. Benefits of the dietary supplementation of black seed in heat stressed animals and poultry.

Fig. 4. Benefits of the dietary supplementation of ginger in heat stressed animals and poultry. 6 M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399

Fig. 5. Benefits of the dietary supplementation of Artemisia annua L. in heat stressed animals and poultry.

stress conditions in Egypt. On the other hand, there was no signif- It is used widely to treat various disorders (Khan et al., 2012b). icance difference in drinking behavior, slaughter weight, feed con- Important constituents of ginger include gingerdione, gingerdiol version rate and T4 level (El-Shoukary et al., 2014). and shogaols. These compounds possess several pharmacological It has been reported that different supplementation of black activities such as antioxidant and antimicrobial activities cumin oil (0.5, 1%), seeds (1, 2%) or meal (10, 20%) to heat stressed (Rehman et al., 2011; Khan et al., 2012a). Recently, co- broilers diet improved growth performance and reduced the nega- administration of cold pressed ginger oil with antiepileptic Topira- tive impacts of heat stress (Mohammed and Al-Suwaiegh, 2016). mate found to attenuate the sexual dysfunction in patients suf- Noteworthy, enhancement effect was reflected on feed intake fered epilepsy, where authors recommended this combination (El (FI), feed conversion ratio (FCR), crude protein conversion, and Makawy et al., 2019). calorie conversion ratio of birds (Hermes et al., 2009a,b). Black Dietary inclusion of ginger to heat stressed-broilers diet (2%) led seeds-associated improvement effect in heat stressed broilers to significant (p<0.05) improvement in biochemical blood vari- could attribute to their efficient effect on body metabolism. ables and growth performance compared to control group Abou-Elkhair et al. (2018) indicated that dietary inclusion of cumin (Rehman et al., 2018). This improvement may own to the strong seeds in laying hens diet (0.5%) had no adverse impacts on egg antibacterial potential of phytogenic ginger compounds and to quality, laying performance, as well as biochemical constituents the beneficial impacts of these micronutrients on palatability, of serum. Moreover, the beneficial role of black cumin in reduction digestibility, metabolism, and general health status of birds of malondialdehyde (MDA) and cholesterol levels in serum and egg (Khan et al., 2012a; Rehman et al., 2018). Besides, the dried fer- was suggested; where their dietary inclusion able to reduce choles- mented ginger was concluded as a strong growth promoter in terol and improve the antioxidant potential of eggs and laying broilers (Incharoen et al., 2010) and egg-production-promoter in hens, which met the consumer’s demand. More recently, it was laying hens (Incharoen and Yamauchi, 2009). Moreover, broilers suggested that thymoquinone, which is the most abundant and supplemented with ginger at levels 2 and 4 g/kg diet showed the active compound in black cumin, may prevent neurotoxic- highest villus lengths where it was related to hypertrophy in both ity and As2O3-induced apoptosis and cytotoxicity (Firdaus et al., epithelial cells and intestinal villi and the greatest crypt depths 2019). compared to the non-supplemented control group (Shewita and Taha, 2018), while ginger had negative impacts on body weight, 3.2. Ginger FI and FCR at higher levels 6 g/kg diet that may attributed to the bitter taste of ginger at higher levels (Shewita and Taha, 2018). Ginger (Zingiber officinale Roscoe) is a common herbal plant that On these bases, the stimulatory effect of dried fermented ginger is extensively cultivated in Japan, where it processed into several might be useful in poultry production particularly in tropical area, products. However, huge amount of ginger by-products (approxi- where heat stress reduced the villus height in quail (Sandikci et al., mately 30–50 t) could be disposed from one company without 2004), broiler chicks (Mitchell and Carlisle, 1992) and destruct the using for other useful purposes (Incharoen and Yamauchi, 2009). jejunal villus tip (Liu et al., 2009) in procine. Khonyoung et al. M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 7

Fig. 6. Benefits of the dietary supplementation of hot red pepper in heat stressed animals and poultry. (For interpretation of the references to color in this figure legend, the reader is referred to the web version of this article.)

(2012) reported that, under thermal stress conditions, the dietary et al., 2009; Das, 2012). In broilers, dietary supplementation of A. inclusion of dried fermented ginger product (1%) to broiler diet annua as an efficient anti-parasitic drug against coccidiosis was could decline the abdominal fat content, and reduce the desqua- suggested (Brisibe et al., 2008; Dra˘gan et al., 2010). Cobb broilers mation of jejunal villus apex; meanwhile these desquamations (aged 14 days) subjected to constant 32 °C for 21 days by Saracila were significantly reduced with dietary dried fermented ginger et al. (2018), they reported that feeding of Artemisia annua powder increasing, and disappeared in the dried fermented ginger groups (1%) plus Artemisia annua oil (0.005%) to the broilers significantly at level 1%. In addition, it was reported that ginger root powder increased daily feed intake compared to control birds. Moreover, or ginger essential oil have a powerful antioxidant capacity than the same authors reported that significant decrease in the intesti- synthetic antioxidants such as vitamin E in broiler diets (Habibi nal and caecal count of Enterobacteriaceae, E. coli and Staphylococ- et al., 2014). Dietary supplementation of 7.5 g or 150 mg/kg feed cus colony, while increase Lactobacilli count in mixture of A. of ginger root or ginger essential oil to heat stressed broilers annua oil and powder group compared to control one. On the other (32 ± 2 °C for 8 h per d); respectively, significantly increased body hand, Engberg et al. (2012) reported that broilers (Ross 308) reared weight, body weight gain, superoxide dismutase and reduced within thermoneutral conditions from1 to 35 days of age and sup- malondialdehyde (MDA) levels in liver compared to the control plemented with 10 and 20 g Artemisia/kg diet, had a lower body group. Moreover, the inclusion of ginger powder or essential oil weight compared to control birds. Panaite et al. (2018) evaluate in heat stressed-broiler diets did not affect the carcass traits or the impact of ascorbic acid and Artemisia annua powder feeding blood variables (Habibi et al., 2014). on heat stressed broilers from 14 to 35 days under 32 °C with ascorbic acid and Artemisia annua on broiler performance, they 3.3. Artemisia annua L. (A. annua) reported that the heat stress affected adversely the intake and gain of the all groups. While treated groups had significantly lower Artemisia annua L. (A. annua) is herbal member of the Asteraceae Enterobacteriaceae count in the intestine than in control group, family (Compositea) which is growing annually in several countries but E. coli count and Lactobacilli concentration in the intestine were all over the world such as China, Italy, Argentina, Spain, USA, and significantly increased compared to control group France (Willcox et al., 2004; Das, 2012). The main active con- Dietary inclusion of 1 and 1.25 g/kg enzymatically treated Arte- stituents of A. annua included essential oils (such as camphene, misia annua L. in heat stressed broiler diet enhanced body weight b-camphene), phenolics, sesquiterpenoids, flavonoids, amino acids, gain, feed consumption and carcass traits, and reduced blood pH mineral, and vitamins (Willcox et al. 2004; Brisibe et al., 2009; Das, in comparison with the heat stressed non-supplemented group. 2012). A. annua was traditionally used in treatment of malaria and Moreover, feeding of heat stressed broilers with Artemisia annua fever (Ferreira et al., 2010; Tu, 2011). Likewise, it was used success- supplemented to diet leading to decrease serum levels of corticos- fully as antioxidant, antibacterial, antihypertensive, and anti- terone, MDA, aspartate aminotransferase (AST), and alanine inflammatory agent, beside its nutritional properties (Brisibe aminotransferase activities (ALT). While it increased the levels of Table 1 8 Summarization of the previous studies on the use of herbs to alleviate heat stress in animals.

Medicinal herbs Species Heat stress Dose Main findings References 1. Black seed (Nigella Pigeons (34 °C, Egyptian summer 2% Increase in feed intake (189.4% vs control) and feeding behavior. El-Shoukary et al. sativa) season) A significant decrease in aggressive behavior and feed conversion ratio. (2018) Significant increase in body weight and bod weight gain Significant increase in total antioxidant capacity Significant decrease in glucose, cholesterol, and catalase levels Broiler chicks Egyptian summer season) 1% Significant increase in feed intake, dressing percentage, and daily body gain. El-Shoukary et al. Significant decline in panting behavior, water to feed ratio, corticosterone and T3 (2014) levels. No significance difference in drinking behavior, slaughter weight, feed conversion rate and T4 level Broiler chicks Oil (0.5, 1%), seeds (1, Improved growth performance and reduced the negative impacts of heat stress Mohammed and Al- 2%) or meal (10, 20%) suwaiegh (2016)

laying hens 0.5% No adverse impacts on egg quality, laying performance and biochemical con- Abou-Elkhair et al. 134399 (2020) 703 Environment Total the of Science / al. et El-Hack Abd M.E. stituents of serum (2018) 2. Ginger (Zingiber Broiler chicks 31 °C Dried fermented Declined abdominal fat content, and reduce desquamated of jejunal villus apex Khonyoung et al. (2012) officinale) ginger (0.25, 0.5 and 1%) Broiler chicks (32 ± 2 °C for 8 h per d) 7.5 g or 150 mg/kg Significantly increased body weight, body weight gain, superoxide dismutase and Habibi et al. (2014) feed of ginger root or reduced MDA levels in liver compared to the control group. ginger essential oil Did not affect carcass traits and blood variables 3. Artemisia annua L. Arbor Acres (34 ± 1 °C for 8 h/day and 1 and 1.25 g/kg Enhanced body weight gain, feed consumption and carcass traits and reduced blood Wan et al. (2017) (A. annua) male broilers 22 ± 1 °C for 16 h/day) pH Decrease serum levels of corticosterone, MDA, aspartate aminotransferase (AST), and alanine aminotransferase activities (ALT). While it increased the levels of serum superoxideImproved dismutase meat traits, (SOD), antioxidant tri-iodothyronine, enzymes activities, and tri-iodothyronine/thyroxine and energy status of breast Wan et al. (2018) Arbor Acres 34 ± 1 Cfor 8 h per day 0.75,kg 1.00 and 1.25 g/ muscle, male broilers (09.00–17.00 h) followed Significant decrease of HSP70and HSP90 and significant elevation in the expression by 22 ± 1 C for 16 h per of SIRT1, avUCP, and PGC-1 a 4. Fennel (Foeniculum Broiler chicksday Egyptian hot summer 1or2% Improved significantly feed intake, leukocytes, and meat breast percentage Ragab et al. (2013) Vulgare Mill.) season Had significantly influence on the reduction body temperature and reduce mortality rates Laying hens (24, and 34 °C) (0, 10, or and 20 g/kg No effect of body weight, feed intake, feed conversion rate. Gharaghani et al. (2015 of diet) egg quality were significantly improved after supplementation of 10 or 20 g of fen- nel /kg diet Lowering the number of broken eggs, Reduced significantly of MDA and carboxyl in eggs Reduced significantly yolk triglyceride and cholesterol contents. 5. Hot red pepper White Leghorn 8 °C greater than those of 50 mg/kg Lowering the H/L ratio Prieto and Campo chicks the control group No significant differences for tonic immobility duration and the fluctuating asym- (2010) metry between groups 6. Thyme Broiler chicks Thyme essential oil Enhance growth performance, immune activates Olfati and Mojtahedin (100, 150 and Reduced heterophil count and H/L ratio and increased lymphocyte count increased (2018) 200 mg/kg diet) relative weight of spleen, thymus and Bursa of fabricius Broiler chicks Egyptian hot summer 1or2% Thermoregulatory responses and growth performance parameters did not influ- Ragab et al. (2013) season enced by supplementation of the thyme dried leaves 7. Rosemary Rabbit 33.1 °C and relative A mixture of moringa Significantly improvement of growth performance, nutrient digestibility and antiox- Helal et al. (2017) humidity 43% for 9 weeks and rosemary leaves idant status as compared with control groups. of 0.5% each (5 g/kg diet) Laying hens 31 °C for 5 weeks 200 ml/ton ; did not affect the feed conversion rate, egg weight, and daily egg production Torki et al. (2018) 20 ml/100 kg; reduce the cholesterol in laying hens under heat stress condition and no effect on triglycerides 8. Dill Laying hens 31 °C for 5 weeks 15 ml/100 kg Reduction in serum levels of triglyceride and cholesterol in chicks under the condi- Torki et al. (2018) tion of thermal stress vs control birds Table 1 (continued)

Medicinal herbs Species Heat stress Dose Main findings References 9. Chicory Laying hens 31 °C for 5 weeks 250 ml chicory /100 kg diet; Increased egg mass but daily egg production and egg weight didn’t exhibited Torki et al. (2018) differences 2.5L chicory / ton diet showed increased Haugh unit as compared to control hen, increased eggshell thickness, and decreased serum levels of cholesterol and triglyceride in comparison to control hens. 10. Radix bupleuri Holstein cows 10 wks in hot summer 0.25 or 0.5 g/kg reducing the thermoregulatory response such respiration rates and rectal tempera- Pan et al. (2014) (27.5 to 29.8 °C) tures, as well as increasing dry matter intake, milk production, milk fat yield and milk protein yield Dairy cows 0.5, and 1.0 g increased blood total protein, albumin, superoxide dismutase (SOD), and glu- Cheng et al. (2018) tathione peroxidase (GSH-Px) activity, the immunoglobulin (Ig) A and IgG content, Interleukin (IL)-2 , IL-4 and , IL-4 level 11. Moringa (Moringa Rabbit 33.1 °C and relative 1% Improved live BW, daily body gain, FCR, as well as improve immune responses and Helal et al., 2017 oleifera) humidity 43% for 9 weeks apparent digestibility of crude fiber and ether extract favorable effect on lipid peroxidation

12. Cutellaria Broiler chicks 35 °C for 2 d 0.2% reduce intestinal lesions induced by thermal injury with subsequent elevation in Varmuzova et al. (2015) 134399 (2020) 703 Environment Total the of Science / al. et El-Hack Abd M.E. baicalensis L. poultry production and performance Broiler chicks 27 °C from age of 30 to 1 g/kg diet no influence on water and feed intake broiler Zmrhal et al. (2018) 34 days significant reduction of thermoregulatory behavior 13. Curcuma Broiler chicks exposed to 34 °C and 50% 200 and 400 mg/kg significant increase in erythrocyte GSH-PX and SOD activity, plasma levels of Akbarian et al. (2014) xanthorrhiza RH for 5 h daily in the growth hormone (GH) and serum levels of total protein finishing period significant decrease was reported for phosphorus, chloride, cholesterol, and low- density lipoprotein (LDL) significant elevation in bronchitis antibody titers 14. Coriander seed Broiler chicks summer heat stress 2% dressing percentage and feeding behaviors (such as daily body gain and feed intake) El-Shoukary et al. conditions in Egypt were significantly increased (2014) significant decline in panting behavior, water to feed ratio, corticosterone and T3 levels no significance difference in drinking behavior, slaughter weight, feed conversion Quail 34 °C for 8 h/d followed Cinnamon oil ratesignificant and T4 increase level in the activity of the antioxidant enzyme including GSH con- Simsek et al. (2013) 15. Cinnamon by 22 °C for 16 h/d (cinnamaldehyde tents of the tissues (Cinnamomumzeylanicum L.) (88.2%), benzyl The level of 500 ppm cinnamon oil exhibited a robust influence on antioxidant prop- alcohol (8.0%) and erties of the internal organs (P < 0.01) by activating antioxidant mechanism eugenol (1.0%)) 16. Licorice Broiler chicks 1, 2 or 4 mg LE/kg significant positive impact (p < 0.05) in alleviating the adverse effect of heat stress Lashin et al. (2017) (Glycyrrhiza body weight in on broiler performance parameters including (body weight, mortality rate, carcass glabra) drinking water traits, hematological and serum biochemical parameters including (protein, glucose, cholesterol, uric acid, (AST), (ALP), calcium, phosphorus, potassium and sodium levels 17. Ginkgo biloba Broiler chicks summer season 0.06% improved growth performance FCR, immunity against ND, IP and IB disease viruses El Iraqi et al. (2013) Broiler chicks Fermented Ginkgo higher (P < 0.05) growth performance parameters, immunity with elevated n-3 Kim et al. (2017) biloba5–10% PUFA and decreased SFA of broiler meat 18. Resveratrol Broiler chicks decreased (P < 0.05) in serum D-lactic acid, crypt depth, E. coli populations and flu- Ramis et al. (2015) orescein isothiocyanate dextran, higher (P < 0.05) body weight, number of goblet cells villus height, villus height/ crypt depth, Lactobacillus and Bifidobacterium populations, mRNA levels of clau- din-1, mucin-2, E-cadherin and occludin Broiler chicks protectant against thermal injury- induced spleen dysplasia in broilers via the stim- Zhang et al. (2018) ulation of the Nrf2 signaling pathway, which resulted in reduction of apoptosis 9 10 M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 serum superoxide dismutase (SOD), tri-iodothyronine (T3), and tri- chemical constituents. On these bases, authors suggested that fen- iodothyronine/thyroxine (T3/T4) compared to heat stressed broil- nel seeds are able to promote laying hens and egg quality variants. ers (Wan et al., 2017). The impacts of enzymatically treated Artemi- sia annua L. also, was reported by Wan et al. (2018) in heat-stressed 3.5. Hot red pepper broilers, they found that dietary supplementation of enzymatically treated Artemisia annua L. (1–1.25 g/kg diet) led to improved meat Red pepper (Capsicum annuum L.), one of the major sources of traits, antioxidant enzymes activities, and energy status of breast carotenoids including vitamin E, C, and A, is well-established as muscle; these improvement effects are related to modulated antioxidant agent (Krinsky, 2001). Red pepper is very rich in vita- expression of pertinent mRNA (significant decrease of heat stress min C, which has improving impact on production against heat protein-70 (HSP70) and heat stress protein-90 (HSP90), and signif- stress condition (Al-Kassie et al., 2012). The bioactive constituents icant elevation in the expression of SIRT1 (sirtuin), Avian uncou- of red pepper such as capsisin, capsantine, and capsaicin were con- pling protein (av UCP), and Peroxisome proliferator-activated cluded to their chemotherapeutic and chemopreventive influences receptor gamma coactivator 1-alpha (PGC-1 a). Therefore, A. annua (Jancso et al., 1997). However, fruits of red pepper are usually used could be seated as a promising herbal supplement to alleviate heat in broiler and layer production to increase the appetite of chicken stress in the poultry production (Wan et al., 2018) and as a possible (Ozer et al., 2005), darkening the color of egg yolk and promote the antioxidant that enhanced the antioxidant activity of broilers laying parameters (Ozer et al., 2006). Al-Kassie et al. (2012) con- chicken through scavenging of free radicals and providing hydro- cluded that dietary supplementation of hot red pepper was able gen of flavonoids and phenolic compounds (Wan et al., 2017). to reduce the ratio of heterophil/lymphocytes (H/L), suggesting its stimulating action on poultry immune system. During the heat 3.4. Fennel (Foeniculum vulgare Mill.) stress conditions, chicks exhibited an increase of H/L ratio, demon- strating that it is a more dependable indicator of the influence of Fennel (Foeniculum vulgare mill.) is an aromatic edible member thermal injury in chicks. Prieto and Campo (2010) suggested that of Apiaceae family, which is cultivated extensively in Mediter- dietary supplementation of capsaicin (active compound in red pep- ranean region. It is used since ancient time for humans as spice per, 50 mg/kg) was effective in alleviation of heat stress induced by and as traditional medicinal agent. It is an interesting non- elevated ambient temperature, as indicated by a lower H/L ratio. synthetic natural compound that is known as a major source fla- Feeding of Hot red pepper in broiler at level 0.5 g/100 g diet had voring product (Yaylayan, 1991). Fruit of fennel is used in several positive impact on growth performances and also had hypolipi- formulations such as liqueurs, savory, confectionery, sauces demic effect (Puvacˇa et al., 2016). Recently, Abou-Elkhair et al. (Guilled and Manzanons, 1996). Several studies concluded the role (2018) indicated that dietary supplementation of hot red pepper of fennel essential oil as a potent hepatoprotective, antioxidant, (5 g/kg diet) for laying hens efficiently affects the growth parame- and antimicrobial agent (Ruberto et al., 2000; Ozbek et al., 2003); ters without reported adverse impact on laying and egg quality where Damianova et al. (2004) had cleared the chemical composi- parameters. Likewise, concentration of MDA and cholesterol of tion of fennel volatile oil. Ragab et al. (2013) noticed that dietary serum and egg were efficiently decreased by dietary inclusion of inclusion of 1 or 2% fennel seeds in the diets of Ross broilers red pepper; suggesting its antioxidant and hypo-cholestrolemic improved significantly FI, leukocytes, and meat breast (%) under activity, as required by consumers. elevated temperature. Further, it has been reported that fennel seeds had significantly influence on reduction of body temperature 3.6. Thyme and mortality rates of Ross broilers under heat stress conditions. However, dietary inclusion of fennel resulted in mild effect on per- Genus Thymus is a member of Lamiaceae family which contains formance parameters including FI, body weight (BW) and egg pro- about 400 species of aromatic perennial with many varieties and duction rate; but the parameters of eggs quality was improved subspecies (De Martino et al., 2009). The major six components significantly by supplementation of fennel. Consistently, being reported are linalool, carvacrol, geraniol, thymol, gamma- Gharaghani et al. (2015) studied the potential role of fennel fruits terpineol and trans-thujan-4-ol/terpinen-4-ol (Rota et al., 2008). (Foeniculum vulgare Mill.) with different concentrations (0, 10, and/ Olfati and Mojtahedin (2018) concluded that dietary inclusion of or 20 g/kg diet) as anti-stressor agent in heat stressed- laying hens. thyme essential oil (150 and 200 mg/kg) could provide an effective Although the performance parameters such as body weight and protection against negative influences of heat stress in chicks feed intake did not affected by dietary inclusion of fennel, the reared under thermal stress through enhancement of growth per- parameters of egg quality were significantly improved after sup- formance and immune activity, and through reduction of hetero- plementation of 10 or 20 g of fennel /kg diet. Moreover, it has been phil count, and H/L ratio, and increased lymphocyte count and indicated that the inclusion of fennel (10 or 20 g/kg diet) in the diet relative weight of spleen, thymus and bursa of Fabricius as com- of heat stressed laying hens lowering the number of broken eggs, pared to heat stressed group. Conversably, Ragab et al. (2013) sug- and reduced significantly the levels of MDA and carboxyl in eggs, gested that the thermoregulatory responses and growth as well as the yolk contents of triglyceride and cholesterol performance parameters did not influenced by supplementation (Gharaghani et al., 2015). Chicks fed 1, 2 and 3 g fennel/kg diet of the thyme dried leaves (1 or 2%) in heat stressed broiler diets. had significantly higher RBCs, Hb and PCV than control group. Behboudi et al. (2016) reported that addition of thyme at (0.5 While a significant decline was quoted for for H/L ratio in chicks and 1% of diet) to broilers (25–42 day old) kept at 34 °C±2 fed fennel 2 and 3 g/kg diet (Mohammed and Abbas, 2009). (9.00–17.00) had no effects on body weight gain (BWG), FI, FCR, Generally, it is accepted that medicinal plants such as fennel H/L ratio, glutathione peroxidase (GPX) activity as well as serum fruits may has a remarkable improvement effect on egg quality, cholesterol level. However, Fallah and Mirzaei (2016) reported that and amelioration of the adverse impacts of heat stress. Such different levels of thyme powder (1, 1.5 and 5 g/kg diet) had no improvement may attribute to the presence of antioxidant com- effect on broilers growth performance, and the administered pounds such as anethole in fennel, which has a role in alleviation thyme hot water extracted at 5 g/l during 1–21 days of age did of thermal stress negative impact (Oktay et al., 2003). Abou- not affect the growth performance of broilers (Sadeghi et al., Elkhair et al. (2018) indicated that fennel seeds can be supple- 2012). Recently, Attia et al. (2017), supplemented broiler chicks mented to the laying hen’s diets at concentration of 0.5% without with different levels of thyme oil (TO) under hot climate conditions adverse impact on egg quality, laying performance, and serum bio- (heat stress) and reported that the TO (1.0 g/kg feed) improved M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 11

(FCR) compared to other groups. TO (1.5–2.0 g/kg feed) increased mance parameters. Additionally, dietary supplementation of dill plasma total protein and globulin levels, but albumin/globulin resulted in reduction in serum levels of triglyceride and cholesterol ratio was decreased plasma. Moreover, the TO groups significantly in chicks under the condition of thermal stress vs control birds decreased the plasma AST, and TO (2.0 g/kg feed) group enhanced (Torki et al., 2018). However, the dietary supplementation dill antibody titre against infectious bursa disease (IBD) than the con- had no effects on broiler growth performance and carcass traits; trol group. These authors finally conclude that, TO at 1.0 g/kg diet it positively impacted the lipid profile of serum and improved may be used as a potential growth enhancer for broilers in hot gut health as well, thereby enhanced overall performance of broiler region during 1–28 days. chickens (Vispute et al., 2019).

3.7. Rosemary 3.9. Chicory

Rosemary (Rosmarinus officinalis) is an herbal member of Labi- Chicory (Cicorium intybus L.) is perennial plant, which is com- atae family with needle-like leaves. It has been cultivated exten- monly used for ruminants as palatable forage crop (Li and Kemp, sively in Mediterranean region. Flowers of rosemary may be 2005). The roots of chicory contain large concentrations of inulin pink, purple, white, or blue. Through natural antioxidants, rose- and fructo-oligosaccharides. Inulin is a water-soluble polymer of mary has been clearly accepted as one of the species with the fructose with b-(2-1) glycosidic bond; it is usually used in highest antioxidant activity (Peng et al., 2005). The chemical anal- improvement of the intestinal microflora integrity. Moreover, it ysis of rosemary showed that it has several types of antioxidants, can be used to improve mineral absorption within the gastroin- including flavonoids such as carnosol, carnosic and rosmarinic testinal tract, and alternate lipid metabolism resulted in hypolipi- acid, and volatile oils (Okamura et al., 1994; Angelini et al., daemic impacts (Azorin-Ortuno et al., 2009). Likewise, inulin is 2003). Rosemary is well-known as a strong anti-oxidative herbal considered as common prebiotic due to its selective stimulating plant (Estevez et al., 2007). The major bioactive constituents of effect on the growth of Lactobacillus and Bifidobacterium (Rehman rosemary are rosmarinic acid, caffeic acid, betulinic acid, ursolic et al., 2008). Chicory ethylic acetate extract supplementation at acid, and camphor; where carnosol and carnosic acid are the most levels more than 250 mg/kg feed improved growth performance potent antioxidants (Nakatani, 2000; Crowley, 2008). Interest- and decreasing blood lipids of heat stress broilers (Taraz et al., ingly, the antioxidant activity of carnosic acid is three times higher 2015). Furthermore, feeding of Chicory extract and vitamin C in than carnosol, and seven times higher than butylated hydrox- heat stressed broiler chickens improvement in liver, kidney func- yanisol and butylated hydroxytoluene (Richheimer et al., 1996). tions and activity as well improved fat metabolism (Khodadadi Another trial was conducted by Helal et al. (2017) concluded that et al., 2016). heat stressed rabbit fed with a mixture of moringa and rosemary In recent trial conducted by Torki et al. (2018), under high leaves of 0.5% each (5 g/kg diet) had significantly improvement ambient temperatures, however the highest egg mass was of growth performance, nutrient digestibility and antioxidant sta- observed in the laying hens supplemented with chicory tus as compared with control groups. Tang et al. (2018) studied (250 ml/100 kg) vs to control hens, FC, daily egg production and the effect of rosemary on heat stressed broilers and reported that egg weight didn’t exhibited differences. Additionally, the laying purified rosemary extract could induce high levels of CRYAB and chickens supplemented with chicory (2.5 L/ton diet) showed HSP70 in hearts of chicken during and before heat stress, thus increased Haugh unit as compared to control hen (73.88, 69.91; rosemary purified extract could be used to alleviate heat stress respectively), increased eggshell thickness, and decreased serum in broiler chickens. levels of cholesterol and triglyceride in comparison to control hens. The dietary supplementation of 250 and 500 ppm rosemary essential oils in quails alleviated the heat stress induced testicular 3.10. Radix bupleuri lipid peroxidation (Turk et al., 2016). In laying hens, Torki et al. (2018) showed that supplementation of 200 ml/ton diet of rose- Radix bupleuri is a common herbal plant that is cultivated in mary extract did not affect the FCR, egg weight, and daily egg pro- Japan and Korea for the purpose of treatment of influenza and duction of layers under normal or heat stress conditions. Recently, common cold- associated symptoms such as inflammation, pain, it has been reported that rosemary extract (20 ml/100 kg) reduce and fever (Van Wyk and Wink, 2004). It is well-established that the cholesterol in laying hens under heat stress condition, while Radix bupleuri had several medical action including antipyretic, it didn’t effect triglycerides levels (Torki et al., 2018). Petricˇevic´ diaphoretic, as well as immunostimulatory function (Ashour and et al. (2018) concluded that feeding of rosemary powder at level Wink, 2011), with resultant production of polysaccharides (Xu 0.4% to broiler chicks had positive impacts on the growth perfor- et al., 2007), saikosaponins (Tan et al., 2008), and essential oils mance parameters, cecal microbiological composition and fat (Ashour et al., 2009). Saikosaponin triterpenes is the major sec- deposition. But with increasing the level of rosemary no effects ondary metabolites of genus Bupleurum representing approxi- has been reported. mately 7% of the total dry weight of roots (Ashour and Wink, 2011). The contained essential oils and saponins are able to modify 3.8. Dill the rumen fermentation and promote the animal production (Benchaar et al., 2008; Patra and Saxena, 2009). Radix bupleuri Dill (Anethum graveolens L.) is member of Apiaceae family. It is extract (BE) confirmed for its antipyretic effect in heat stressed lac- containing Carron and limonene (Kabeczka, 2002). Dill is widely tating dairy cows via reducing the thermoregulatory response such used as a traditional medicinal plant to treat gastrointestinal disor- respiration rates and rectal temperatures, as well as by increasing ders (Hosseinzadeh et al., 2002); decreasing blood total choles- dry matter intake, milk production, milk fat yield and milk protein terol, low density lipoprotein (LDL-C), triglyceride (Yazdanparast yield when fed at 0.25 or 0.5 g/kg, thus Radix bupleuri extract could and Bahramikia, 2008), and glucose (Panda, 2008), and elevate high be mitigate the deleterious influences of highly ambient tempera- density lipoprotein (HDL-C) (Yazdanparast and Alavi, 2001). More- ture on milk production of Holstein cows (Pan et al., 2014). Besides over, it has strong antioxidant potential (Satyanarayana et al., the antioxidant benefits, Radix bupleuri extract are also reported to 2004). Dietary supplemented with dill extract (15 ml/100 kg diet) improve the immune response and antioxidants capabilities of for laying hens under heat stress improved egg index and egg yolk thermal-stressed dairy cattle. The results of this experiment where index (Torki et al., 2018), while it has no effect on other egg perfor- obtained with different concentration of BE (0.25, 0.5, and 1.0 g of 12 M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399

BE/kg dry matter) fed to dairy cows under elevated temperature and performance (Varmuzova et al., 2015). Also, Park et al. conditions (Cheng et al., 2018). Cows which received, 0.5, and (2016) concluded that Scutellaria baicalensis L. extract had efficient 1.0 g of BE showed increased levels of blood total protein, albumin, effect on performance of broilers chicken reared under high envi- SOD, and GSX, the immunoglobulin A and G (Ig A, IgG), Interleukins ronmental temperatures. Such effect might contribute in behav- (IL-2 and IL-4) (Cheng et al., 2018) compared with control group. ioral alteration particularly under stress condition. Zmrhal et al. (2018) has perceived that no influence on water and feed intake 3.11. Moringa (Moringa oleifera) in broiler chicken reared under heat stress by dietary inclusion of Scutellaria baicalensis L. extract (1 g/kg diet). Nevertheless, the ben- Moringa oleifera (The Miracle Tree) is the most widely cultivated eficial influence of Scutellaria baicalensis L. extract as anti-stressor species of the genus Moringa. Moringa oleifera is able to inhibit the agent was observed through significant reduction of thermoregula- oxidative and morphological alterations by promoting the poten- tory behavior (Zmrhal et al., 2018). Zmrhal et al. (2017) concluded, tial of the antioxidant enzymes effectively via decrease lipid perox- however, that 0.1% addition of Scutellaria baicalensis in broiler diets idation and free radicals generation (Sreelatha and Padma, 2009). does not reduce negative impacts of heat stress neither negatively Moringa oleifera leaves have multiple antioxidants with high levels, affect meat production and recommended to increase the dose of such as phenolic acids (gallic, chlorogenic, ellagic and ferulic acid), Scutellaria baicalensis in broiler diets. Króliczewska et al. (2017) glucosinolates and flavonoids (kaempferol, quercetin and rutin) used Scutellaria baicalensis root (SBR) at levels (0.5, 1.0, and 1.5%) (Mbikay, 2012). Furthermore, moringa dry leaves have been in broiler diets and reported that Heterophile/Lymphocyte ratio reported to be a valuable source of b-carotene (precursor of vit. increased in the treated groups with SBR compared to the control A) and vitamins (B-complex, C, D and K) (Dorga and Tandon, one with lymphocytic depletion in chickens blood. They also 1975). Moringa dry leaves have positive effects on hematological recorded that the bursa of Fabricius and spleen relative weights measurements of rabbits (Chinwe and Isitua, 2010). Recently, El- of SBR groups significantly decreased compared to the control Badawi et al. (2014) concluded that improvement in nutrients group. They concluded that the addition of SBR significantly inhib- digestibility, dietary N utilization, growth performance and carcass ited the formation of RS of nuclei compared to some cytotoxic sub- dressing percentage have been recorded for growing rabbits fed stances. The SBR excess intake may cause immunologic inhibition, diets supplemented with low levels of moringa dry leaves (0.15% negatively affects the immune organs development, inhibited the and 0.30%). formation of radial segmentation nuclei showing antimetastatic A trial conducted by Hassan et al. (2016), who used broiler properties and the phagocytosis of chicken heterophils chicks subjected to heat stress climate and received 3 levels of (Króliczewska et al., 2017). Moringa oleifera (0.1, 0.2 and 0.3%), and recorded improvement in body weight and FCR as the level of Moringa increased. But mor- 3.13. Curcuma xanthorrhiza inga had no effect on carcass parameters. As well, Heterophil/Lym- phocyte (H/L) ratio was decreased by increase in the Moringa level. Curcuma xanthorrhiza (known in Indonesia as Javanese turmeric

Plasma total protein, globulin and Thyroid hormones (T3 and T4) or temulawak) is cultivated and naturally grows in Indonesia and increased significantly (p < 0.05) with increase the level of Moringa South-East Asia. Curcuma xanthorrhiza is commonly used in tradi- oleifera. AST decreased significantly (p < 0.05) while ALT were not tional medicine; where its root contained naturally effective com- affected following addition of Moringa oleifera levels. These authors pounds that used successfully in treatment of skin inflammations finally concluded that addition of up to 0.3% Moringa oleifera leaves and acne. In addition, it has been concluded that bioactive products meal improved broiler performance, physiological parameters and that extracted from C. xanthorrhiza exhibited antioxidant and anti- enhanced the ability to resist heat stress conditions. tumorigenic properties (Rukayadi et al., 2006). Hidanah et al. In rabbit diet, moringa leaves might be acted as an efficient her- (2017) reported that consumption of diet containing 2.5% of both bal additive with anti-stressor potential. Favorable effect of mor- Garcinia mangostana and Curcuma xanthorrhiza significantly inga leaves (1%) on growth performance of rabbits reared under increased live weight of heat stressed broilers than those fed the summer hot condition had confirmed in different experimental control diet. While the cholesterol level and abdominal fat ratio studies. Helal et al. (2017) concluded the enhancement effect of of broilers fed diets containing 5% Curcuma xanthorrhiza were sig- moringa leaves on some growth indices such as live body weight, nificantly higher compared to those fed control diet. Body weight, daily body gain (DBG), FCR, as well as improve immune responses DWG, crypt depth, villus length, and the villus-length-to-crypt- and apparent digestibility of crude fiber and ether extract; dietary depth ratio in the jejunum were significantly increased in cyclic moringa leaves inclusion led to favorable effect on lipid peroxida- heat stressed broilers fed Curcuma xanthorrhiza essential oil (CXEO) tion because of its antioxidant content (Chinwe, and Isitua, 2010; at level 400 mg of CXEO kg1of feed (Hosseini et al., 2016). In addi- El-Badawi et al., 2014; Helal et al., 2017). tion, the dietary supplementation of CXEO reduced the Hetero- phile/Lymphocyte ratio, corticosterone and creatine kinase levels, 3.12. Scutellaria baicalensis L. and mRNA levels of heat shock protein 70 in the jejunum and breast muscle suggesting their reduction effects of HS in broiler Currently, using of phytogenic feed additives is drawing great chickensv (Hosseini et al., 2016). concern. The positive role played in elimination of thermal stress Akbarian et al. (2014) found that dietary inclusion of 200 and associated-adverse effect was reported with using of Scutellaria 400 mg/kg feed of Curcuma xanthorrhiza essential oil in heat baicalensis L. The main active constituents of Scutellaria baicalensis stressed broiler (exposed to 34 °C and 50% RH for 5 h daily in the L including flavones like wogonoside and baicalin, however wogo- finishing period) led to significant increase in erythrocyte GPX nin and aglycones baicalein are the main extracted component and SOD activity, plasma levels of growth hormone (GH) and from the Scutellaria baicalensis L. roots. These included flavones serum levels of total protein. However, significant decrease was found to have several actions such as antioxidant, antibacterial, reported for phosphorus, chloride, cholesterol, and LDL. Further- antiviral, anti-malignance, neuro- and hepatoprotective actions more, it has been reported that Curcuma xanthorrhiza essential oil (Zhao et al., 2016). Moreover, supplementation of combination of resulted in significant elevation in bronchitis antibody titers Scutellaria baicalensis L. and curcuma extract was used commonly (p < 0.01) than the other groups. Several studies suggested that in broiler to efficiently reduce the intestinal lesions induced by the up-regulation of the antioxidant enzymes through herbal thermal injury with subsequent elevation in poultry production antioxidants contents may introduce alternative mechanism for M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 13 animal cells exposed to long lasting thermal injury. Exposure to Results revealed that supplementation of cinnamon increased feed heat stress for long time had adverse effect on antioxidant system intake and body weight gain, and decreased the concentration of via activating the minerals and vitamins excretion like Cu, Zn, Se, blood uric acid and lactate dehydrogenase, and malondialdehyde vit C, and vit E; where these substances play well-established role compared to control birds (P < 0.05). in activation of antioxidant enzymes (Sahin and Kucuk, 2003; Kanani et al. (2017) used 250 one-day-old broiler chicks to Balnave, 2004; Daader et al., 2016). In turn, the antioxidant investigate the effects of dietary supplementation of cinnamon enzymes activity will decrease. Therefore, dietary supplementation powders (0.5%) on meat quality and lipid peroxidation of broilers of natural antioxidants can be helpful in improvement of vitamins under heat stress condition (32 °C). The results showed that diet- and minerals excretion under thermal stress condition (Abdelnour ary supplementation of cinnamon compensated the decreased pH et al., 2018; Sahin et al., 2006). and DM values due to heat stress to some extent but could not restore them to the level of control treatment (p < 0.01). In addi- 3.14. Coriander seed tion, the thiobarbituric acid reactive substances and free radicals scavenging activity were increased in thigh meat of broilers reared El-Shoukary et al. (2014) concluded that dressing percentage under heat stress (p < 0.05), while these parameters were reduced and feeding behaviors (such as daily body gain and feed intake) by the supplementation of cinnamon. Sadeghi and Moghaddam were significantly increased while there was a significant decline (2018) conducted an experiment to evaluate the effects of cinna- in panting behavior, water to feed ratio, corticosterone and T3 mon powder on mixed sex Cobb-500 broilers performance, serum levels as affected by dietary inclusion of 2% coriander seed to broi- antioxidant status, and serum thyroid hormones. Heat stresses ler diet under summer heat stress conditions in Egypt. On the other were created by increasing ambient temperature to 32–34 °C dur- hand, there was no significance difference in drinking behavior, ing days 31–42 of the experiment. Chicks fed diets supplemented slaughter weight, feed conversion rate and T4 level (El-Shoukary with cinnamon had higher daily gain and spleen weight compared et al., 2014). Moreover, Al-Jaff (2011) concluded that inclusion of to the control. In addition, cinnamon – supplemented chicks coriander seeds at 2% in heat stressed broiler has enhancement showed increased activities of total superoxide dismutase (SOD), effect on broiler performance and blood pictures as well as catalase (CAT), total antioxidant capacity (TAC), corticosteroid immune system. He reported that supplementation of 2% coriander (CE), reduced concentrations of malondialdehyde (MDA) compared seeds for heat stressed broilers increased (P < 0.01) final body to the control (P < 0.05). Although few reports concerning cinna- weight, better FCR (P < 0.05), improved blood parameters mon toxicity are present, no toxicological trials were established (P < 0.05), increased serum protein and albumen, and decreased to evaluate its toxicity in poultry or other animal species. More serum globulin, cholesterol and glucose compared with other research is required to address this challenge. groups. The same percentage of coriander seeds inclusion (2%) to heat stressed broilers reared under summer condition in Iraq 3.16. Licorice (Glycyrrhiza glabra) (32–36 °C) were also reported by Hamodi et al. (2010); inclusion had a positive effect on final BW, FI, and FCR. Also, Barad et al. Glycyrrhiza glabra (licorice), since over 4000 years it has been (2016) concluded that inclusion of 2% coriander seed to Cobb- used as a medicinal product (Shibata, 2000). Licorice extract (LE) 400 broilers had no harmful effect on blood biochemical parame- has been reported for its anti-microbial (Fukai et al., 2002), anti- ters; it also improved the overall growth performance with maxi- inflammatory (Yokota et al., 1998), anti-atherosclerotic (Fuhrman mizing the profit of the enterprises. Furthermore Taha et al. et al., 2002), anti-fungal (Sato et al., 2000), anti-oxidative (Vaya (2019) concluded that using coriander seed powder at level 0.4% et al., 1997; Alagawany et al., 2019), estrogen-like, antiviral, anti- in broiler diets improved the parameters of growth performance infective, and radical scavenging activities (Mukhopadhyay and and most of carcass traits as well reduced the harmful ileum bac- Panja, 2008). The major components of LE consists of flavonoids teria count. (e.g., isoflavonoids, formononetin and liquiritin) and triterpene saponins (e.g., glycyrrhetinic acid, glycyrrhizin and licorice acid), 3.15. Cinnamon (Cinnamomum zeylanicum L.) starch, sugars, amino acids, ascorbic acid, choline, tannins, phytos- terols, coumarins, and some bitter substances (Shalaby et al., Cinnamon (Cinnamomum zeylanicum L.) is a common herbal 2004). Supplementation of 1, 2 or 4 mg LE / kg BW in drinking plant that produced natively in Sri Lanka and India. It is widely water of heat stressed-broiler chicks had significant positive used as spices, medical herb, and for essential oil production impact (p < 0.05) against the adverse effect of heat stress such as (Vasanthi and Parameswari, 2010), beside its antioxidant activity broiler performance parameters including (BW, mortality rate, car- (Mancini-Filho et al., 1998). Cinnamon contains several active phe- cass traits, hematological and serum biochemical parameters nolic compounds like catechin, flvonoids, isoflavones, flavones, and including protein, glucose, cholesterol, uric acid, AST, ALP, calcium, other phenolics; these phenolic constituents act as antioxidants phosphorus, potassium and sodium levels (Lashin et al., 2017). that are able to scavenging the ROS effectively. Moreover, cinna- Totally, LE acts as corticosteroids hormones that increase the resis- mon contains numerous vitamins and minerals that have strong tance of the body to heat stress with subsequent blood purifier antioxidative properties (Jayaprakasha et al., 2007; Gul and properties at hot weather (Armanini et al., 2003). Furthermore, Safdar, 2009). Dietary supplementation of cinnamon oil: cin- productivity quality and feed efficiency may be influenced by licor- namaldehyde (88.2%), benzyl alcohol (8.0%) and eugenol (1.0%) to ice bioactive substances (Wallace et al., 2010). Moreover, birds quails exposed to heat stress (34 °C for 8 h/d followed by 22 °C supplemented with LE consumed more water that had cooling for 16 h/d) revealed positive influences on stress and significant effect for heat stressed birds (Al-Daraji, 2012). Moreover, Al- increase in the activity of the antioxidant enzyme including GSH Daraji (2013) investigated the ameliorative effect of licorice extract contents of the tissues. The level of 500 ppm cinnamon oil exhib- (450 mg / liter licorice in drinking water) on productive perfor- ited a robust influence on antioxidant properties of the internal mance of broilers exposed to heat stress (38–43 °C for 6 h/day). organs (P < 0.01) by activating antioxidant mechanism, when Results revealed that birds treated with licorice extract showed added to heat stressed quails diet (Simsek et al., 2013). significant improvement in mean body weight, feed conversion Kanan et al. (2016) studied the effect of cinnamon powders ratio, water consumption, cumulative body weight, weight gain, (0.5%) on both performance and blood parameters of broiler chick- and feed conversion ratio, compared with control group. Gly- ens (200 one-day-old male chicks) under heat stress (32 °C). cyrrhetic acid, the active metabolite in licorice, inhibits the enzyme 14 M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399

11-ß-hydroxysteroid dehydrogenase enzyme type 2 with a resul- digestibility via enhancing the digestive enzymes and balancing tant cortisol-induced mineralocorticoid effect and the tendency the microbial ecosystem of the gut. Furthermore, broilers supple- towards the elevation of sodium and reduction of potassium levels. mented with fermented GB had higher (P < 0.05) growth perfor- This aldosterone-like action is the fundamental basis for under- mance parameters, immunity with elevated poly unsaturated standing its health benefits and the wide spectrum of adverse fatty acids (n-3 PUFA) and decreased saturated fatty acids of broiler effects. Although licorice is a US Food and Drug Administration meat (Kim et al., 2017) suggesting that GB is an appropriate feed (FDA) approved food supplement that used in many products with- additive in broiler diets. On the other hand, little is known about out precise regulations to prevent toxicity, the two main categories the side effect of GB in poultry and other species (Mei et al., of complications were licorice-induced hypertension and hypoka- 2017). Generally, research on toxicological effects of ginkgo is lemic myopathy (Omar et al., 2012). US Food and Drug Administra- much less extensive compared to the research on pharmaceutical tion limitations for the use of licorice and its derivatives in foods effects. are ranged from 0.05% in baked gods to 16.0% in hard candy (World Health Organization, 2005). Further toxicological studies in poultry are needed to evaluate the efficient as well as the 3.18. Resveratrol adverse effect of licorice in poultry industries. Resveratrol (RES), is a natural bioactive polyphenol that had many biological effects, including anti-obesity (Zhang et al., 3.17. Ginkgo biloba 2015), anti-inflammatory, antioxidant (Khafaga et al., 2019b) and aging-delay effects (Ramis et al., 2015). Broilers exposed to heat Ginkgo biloba (GB) used for several decades in the traditional stress and supplemented with RES exhibited decreased (P < 0.05) Chinese medicine, it is used as worldwide herbal drug that acting in serum D-lactic acid, crypt depth, E. coli populations and fluores- via several mechanisms including antioxidant and anti-apoptotic cein isothiocyanate dextran, while they possessed higher (P < 0.05) (Khafaga and Bayad, 2016a), antidiabetic, antiasthmatic, neuropro- body weight, number of goblet cells, villus height, villus height/ tective, cardio protective (Naik and Panda, 2007), and antitoxic crypt depth, Lactobacillus and Bifidobacterium populations, mRNA effect (Khafaga and Bayad, 2016b). The dietary supplementation levels of claudin-1, mucin-2, E-cadherin and occluding, with con- of GB could improve broiler growth parameters and immunity, clusion that resveratrol had ameliorating role against the heat while it suppresses caecal E. coli pathogenicity (Kim et al., 2016). stress adverse effects of broilers intestinal barrier function El Iraqi et al. (2013) reported that broiler fed GB during summer (Zhang et al., 2017a). Moreover, Zhang et al. (2017b) concluded season (heat stress) improved growth performance, FCR, immunity that RES beneficially ameliorates the adverse effect of heat stress against Newcastle disease (ND), IP and infectious bronchitis (IB) in broilers via regulating the antioxidant status of the muscle. disease viruses. This may attribute to the active principles from Additionally, Liu et al. (2014) investigated the effects of dietary essential oils that found in GB with subsequent enhancing for the supplementation of RES (0, 200, 400, or 600 mg/kg of diet) on the

Fig. 7. Benefits of the dietary supplementation of resveratrol in heat stressed animals and poultry. M.E. Abd El-Hack et al. / Science of the Total Environment 703 (2020) 134399 15 performance, growth index of immune organs, serum parameters, Abdelnour, S.A., Abd El-Hack, M.E., Khafaga, A.F., Arif, M., Taha, A.E., Noreldin, A.E., and expression levels of heat shock protein (Hsp) in the bursa of 2018. Stress biomarkers and proteomics alteration to thermal stress in ruminants: A review. J. Therm. Biol. 79, 120–134. Fabricius, thymus, and spleen of 42-d-old female black-boned Abdelnour, S.A., Abd El-Hack, M.E., Khafaga, A.F., Arif, M., Taha, A.E., Noreldin, A.E., chickens under heat stress condition (37 ± 2 °C for 15 d). The 2019. Stress biomarkers and proteomics alteration to thermal stress in results showed that RES supplemented-chickens exhibited signifi- ruminants. A review. J. Therm. Biol. 79, 120–134. Abou-Elkhair, R., Selim, S., Hussein, E., 2018. Effect of supplementing layer hen diet cant increase in feed intake and BW gain; serum GSH, growth hor- with phytogenic feed additives on laying performance, egg quality, egg lipid mone, and insulin-like growth factor-1 levels; and antioxidant peroxidation and blood biochemical constituents. Anim. Nutr. 4, 394–400. enzymes (GSH-Px, SOD, and CAT activities) as compared to control Ahmad, A., Husain, A., Mujeeb, M., Khan, S.A., Najmi, A.K., Siddique, N.S., Damanhouri, Z.A., Anwar, F., 2013. A review on therapeutic potential of chickens. Contritely, concentrations of serum malondialdehyde Nigella sativa: a miracle herb. Asian Pac. J. Trop. Biomed. 3, 337–352. https:// were decreased in the RES supplemented chickens. Moreover, doi.org/10.1016/S2221-1691(13)60075-1. RES attenuated the heat stress-induced overexpression of Hsp27, Akbarian, A., Golian, A., Kermanshahi, H., De Smet, S., Michiels, J., 2014. Antioxidant enzyme activities, plasma hormone levels and serum metabolites of finishing Hsp70, and Hsp90 mRNA in the bursa of Fabricius and spleen broiler chickens reared under high ambient temperature and fed lemon and and increased the low expression of Hsp27 and Hsp90 mRNA in orange peel extracts and Curcuma xanthorrhiza essential oil. J. Anim. Physiol. thymus upon heat stress. Interestingly, they concluded that the Anim. Nutr. 99, 150–162. dose of 400 mg/kg showed the strongest antioxidant effect. Liu Al-Daraji, Hazim J., 2013. Effects of liquorice extract, probiotic, potassium chloride and sodium bicarbonate on productive performance of broiler chickens exposed et al. (2016) reported that RES could ameliorates the intestinal to heat stress. Int. J. Adv. Res. 1 (4), 172–180. injuries via increasing mRNA and protein expression of Hsp70, Alagawany, M., Elnesr, Shaaban S., Farag, Mayada R., Abd El-Hack, Mohamed E., Hsp90, and NF-kappa B, and suppressing the production of epider- Khafaga, Asmaa F., Taha, Ayman E., Tiwari, Ruchi, Yatoo, Mohd. Iqbal, Bhatt, Prakash, Marappan, Gopi, Dhama, Kuldeep, 2019. Use of Licorice (Glycyrrhiza mal growth factor (EGF) in the mucosa. glabra) herb as a feed additive in poultry: current knowledge and prospects. On the other hand, RES found to be efficient protectant against Animals 9 (8), 536. https://doi.org/10.3390/ani9080536. thermal injury- induced spleen dysplasia in broilers via the stimu- Alagawany, M., Farag, M., Abd El-Hack, M.E., Patra, A., 2017. Heat stress: effects on productive and reproductive performance of quail. World’s Poult. Sci. 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Effect of low inulin doses with different polymerisation degree on lipid Declaration of Competing Interest metabolism, mineral absorption, and intestinal microbiota in rats with fat- supplemented diet. Food Chem. 113, 1058–1065. The authors declare that they have no known competing finan- Babyan, V.K., Kottunga, D., Halaby, G.A., 1978. Proximate analysis, fatty acid and cial interests or personal relationships that could have appeared amino acid composition of Nigella sativa seeds. J. Food Sci. 43, 1314–1315. https://doi.org/10.1111/j.1365-2621.1978.tb15297.x. to influence the work reported in this paper. Balnave, D., 2004. Challenges of accurately defining the nutrient requirements of heat stressed poultry. Poult. Sci. 83, 5–14. Barad, N.A., Savsani, H.H., Patil, S.S., Garg, D.D., Das, O., Singh, V., Kalaria, V.A., Acknowledgment Chatrabhuji, B.B., 2016. 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