Heba M. Salem1
Mohamed T. El-Saadony2
Taia A. Abd El-Mageed3Soliman M. Soliman4Asmaa F. Khafaga5
Ahmed M. Saad6
Ayman A. Swelum7,8Sameh A. Korma9Clara Mariana Gonçalves Lima10Samy Selim11Ahmad O. Babalghith12
Mohamed E. Abd El-Hack13Fatima A. Omer14
Synan F. AbuQamar14*
Khaled A. El-Tarabily14,15,16*Carlos Adam Conte-Junior17- 1Department of Poultry Diseases, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
- 2Department of Agricultural Microbiology, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
- 3Soil and Water Department, Faculty of Agriculture, Fayoum University, Fayoum, Egypt
- 4Department of Medicine and Infectious Diseases, Faculty of Veterinary Medicine, Cairo University, Giza, Egypt
- 5Department of Pathology, Faculty of Veterinary Medicine, Alexandria University, Alexandria, Egypt
- 6Biochemistry Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
- 7Department of Animal Production, College of Food and Agriculture Sciences, King Saud University, Riyadh, Saudi Arabia
- 8Department of Theriogenology, Faculty of Veterinary Medicine, Zagazig University, Zagazig, Egypt
- 9Department of Food Science, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
- 10Department of Food Science, Federal University of Lavras, Lavras, Minas Gerais, Brazil
- 11Department of Clinical Laboratory Sciences, College of Applied Medical Sciences, Jouf University, Sakaka, Saudi Arabia
- 12Medical Genetics Department, College of Medicine, Umm Al-Qura University, Makkah, Saudi Arabia
- 13Poultry Department, Faculty of Agriculture, Zagazig University, Zagazig, Egypt
- 14Department of Biology, College of Science, United Arab Emirates University, Al-Ain, United Arab Emirates
- 15Khalifa Center for Genetic Engineering and Biotechnology, United Arab Emirates University, Al-Ain, United Arab Emirates
- 16Harry Butler Institute, Murdoch University, Murdoch, WA, Australia
- 17Center for Food Analysis (NAL), Technological Development Support Laboratory (LADETEC), Federal University of Rio de Janeiro (UFRJ), Cidade Universitária, Rio de Janeiro, Brazil
Poultry production contributes markedly to bridging the global food gap. Many nations have limited the use of antibiotics as growth promoters due to increasing bacterial antibiotic tolerance/resistance, as well as the presence of antibiotic residues in edible tissues of the birds. Consequently, the world is turning to use natural alternatives to improve birds' productivity and immunity. Withania somnifera, commonly known as ashwagandha or winter cherry, is abundant in many countries of the world and is considered a potent medicinal herb because of its distinct chemical, medicinal, biological, and physiological properties. This plant exhibits antioxidant, cardioprotective, immunomodulatory, anti-aging, neuroprotective, antidiabetic, antimicrobial, antistress, antitumor, hepatoprotective, and growth-promoting activities. In poultry, dietary inclusion of W. somnifera revealed promising results in improving feed intake, body weight gain, feed efficiency, and feed conversion ratio, as well as reducing mortality, increasing livability, increasing disease resistance, reducing stress impacts, and maintaining health of the birds. This review sheds light on the distribution, chemical structure, and biological effects of W. somnifera and its impacts on poultry productivity, livability, carcass characteristics, meat quality, blood parameters, immune response, and economic efficiency.
Introduction
Global food production predominantly depends on animal protein. In many nations, the poultry business has grown in importance as a resource of high-quality eggs and meat to help balance the human food (1). The nutritional economic demands of various countries for a poultry-based diet have forced the intensive production of poultry (2). Furthermore, backyard poultry production is gradually evolving into economically organized flocks and is considered a competitive and rapidly growing section of animal-farming business (3). However, the global poultry industry is facing numerous challenges of sufficiency, safer products without any chemical and antimicrobial residues, and environmentally sustainable production (4). These conditions have led to the discovery and abundant use of various natural and safe feed additives that can be included in the poultry ration to improve productivity through a variety of mechanisms, such as boosting growth rate, enhancing feed conversion efficiency, decreasing pathogen propagation, increasing livability, and decreasing mortality in the poultry industry (4).
The feed additive should be safe, economic, biodegradable, free from environmental hazards, and non-toxic, as well as overcoming drug resistance problems and improving productivity (5). Thus, an eco-friendly substitution of antibacterial growth promoters (AGPs) with a natural growth promoter in the avian ration has recently acquired considerable attention (6, 7) to improve productivity and fight infections (8). Many natural growth promoters (NGPs) such as herbal extracts (9–11), probiotics (12–15), prebiotics (16, 17), phytogenic compounds (18–22), bioactive peptides (23–25), essential oils (26–28), organic acids (29), plants and their active constituents (30–35), and green-synthesized nanoparticles (36–41) are recognized as potential and safe alternatives to AGPs (42). The use of medicinal plants as feed additives to boost development and health is becoming increasingly common around the world (43, 44) owing to the unique properties of these plants, including low cost, low toxicity risk, and minimum human health and environmental hazards (45).
Traditional medicinal herbs are common therapeutics and more potent in combating the negative impacts of thermal stress on broiler productivity (44). The predominant mechanism by which medicinal herbs act in avian rations is to improve the metabolism by combating stress and regulating hormones (46). Numerous field studies on medicinal herbs from all over the world have revealed promising outputs in improving weight gain (WG) and feed efficiency, reducing mortality, elevating livability, and maintaining health among different avian species (47–49).
One of these medicinal herbs is Withania somnifera L. Dunal, commonly known as “ashwagandha” or “winter cherry” (50). W. somnifera is a subtropical plant of 30–150 cm height that belongs to the family Solanaceae and grows naturally in wide areas of Africa, the East Mediterranean region, Pakistan, and India (46). This plant is known as “Indian Ginseng” as it is therapeutically equivalent to Ginseng (51) and was depicted as an herbal tonic for health maintenance (52). W. somnifera is described as an adaptogen, antioxidant, hepatic stimulant, anti-inflammatory, aphrodisiac, astringent, antifungal, and antibacterial factor (53, 54). In addition, extracts of W. somnifera were reported to be potent immune stimulants and anticarcinogenic (55, 56). Preparations of W. somnifera were also found to improve circulating antibody titer and lysosomal enzyme activity and enhance phagocytosis (57). Therefore, many studies have described W. somnifera extracts as immunomodulatory (58), antioxidant (59), antitumor (57), hepatoprotective (60), and antibacterial (61) agents.
Furthermore, W. somnifera significantly improves the blood profile in the shape of increased hemoglobin (Hb) level and increased erythrocyte and white blood cell counts (62, 63). Moreover, different parts of the herb have anti-serotonergic and anabolic characteristics and have potent impacts in the therapy of arthritis and stress, as well as geriatric problems (64). W. somnifera was also reported to improve circulating cortisol, lower fatigue, accelerate physical performance, and lower refractory depression in livestock exposed to various stressors (50). Similarly, W. somnifera is thought to strengthen the physiological and immunological functions of stressed birds (65).
General characteristics of W. somnifera, active ingredients, and their activity
W. somnifera morphological features and distribution
W. somnifera (L.) Dunal, commonly identified as “ashwagandha,” “asgandh,” or “winter cherry,” is a member of the family Solanaceae (66). It is a 30–150-cm-high, upstanding, stellate–tomentose, undershrub with long tuberous roots, opposite leaves, small greenish flowers, and orange berry-like fruits (67).
W. somnifera is known as a wild plant in the northwestern areas of India, expanding from the mountainous region of Punjab, Himachal Pradesh, and Jammu to an altitude of 1,500 m (68). Due to its economic and medicinal properties, it is being widely cultivated (more than 4,000 ha) in drier parts of India (69, 70).
Chemical composition of W. somnifera
The chemical composition of W. somnifera is illustrated in Figure 1. The method of extraction of active components from W. somnifera plants affects the chemical composition of W. somnifera extracts (71). The chemical composition of W. somnifera has been widely investigated, and more than 39 active agents have been extracted, isolated, and identified in different studies (72, 73). Recently, different phytochemical constituents, such as total phenol, more than 12 alkaloids, 40 withanolides, and many sitoindosides, have been described (67). The withanolides are a group of naturally occurring steroidal lactones that impart a distinctive earthy odor and flavor to ashwagandha (74). These steroids comprise a lactone with a nine-carbon side chain linked to the C-17 position (71).
Figure 1. Chemical composition of Withania somnifera.
Different classes of withanolides have different lactone moiety variations. Withaferin A was the first member of this group to be identified (75). The Rf values of withaferin, withanolides D, and withanolides A (0.86) are 0.32, 0.50, and 0.86, respectively (76). The total alkaloid content in the roots of W. somnifera was found to vary between 0.13 and 0.31%, and much higher yields (up to 4.3%) were also reported (77). In addition, the W. somnifera roots include a small amount of soluble protein (5.6%) (76).
Pharmacological features of W. somnifera
The pharmaceutical features of W. somnifera are summarized in Figure 2. W. somnifera is commonly identified as a “Rasayana” in Ayurveda and is abundant in different ayurvedic products to enhance strength and stamina (52). The herb was traditionally utilized to improve youthful vigor, endurance, and strength, maintain health, accelerate the production of vital fluids, muscle, blood, lymph, and semen, and increase the capability of people to overcome environmental stress (78). The similarities between these rejuvenating features and those of ginseng roots have led to ashwagandha roots being known as “Indian Ginseng.” W. somnifera is also established as a general energy-stimulating tonic known as Medhya Rasayana that is used to promote learning and to improve memory (79).
Figure 2. Pharmacological features of Withania somnifera.
Ashwagandha is one of the main components in 74 Ayurvedic, 9 Siddha, 3 Unani, and 126 herbal preparations (68). The roots of this plant have been regarded as a useful internal medicine in rheumatism and dyspepsia and found to be fully diuretic (80). In recognition of the importance and value of W. somnifera as a therapeutic agent, this plant has also been the topic of significant modern scientific interest and appeared in “WHO monographs on selected medicinal plants” (81). Recently, many pharmacological research studies recorded the cardioprotective, immunomodulatory, anti-aging, neuroprotective, and antioxidant characteristics of W. somnifera (78).
Biological activities of W. somnifera
Several studies have described a safe, natural, and powerful antioxidant compound in ashwagandha and other plants of the family Solanaceae (78, 82) as it elevates the levels of three naturally occurring antioxidant enzymes, namely, superoxide dismutase, catalase, and glutathione peroxidase (52). In addition, oral supplementation of W. somnifera extract inhibited the increase in fat peroxidation in both rabbits and mice (83). The antioxidant activity of W. somnifera in mice was found to be imparted by glycowithanolides, withanolides, and sitoindosides VII–X (84). Withania usage considerably enhanced hemoglobin, red blood cell count, and hair melanin and lowered serum cholesterol level in treated individuals (85), and Withania root powder prohibited cadmium-stimulated oxidative stress in chickens and lead-stimulated oxidative damage in mice (86). In addition, W. somnifera (500 mg/kg body weight) exhibited an anti-nephron–cytotoxic effect when examined in mice with (87).
W. somnifera is a potent immune stimulant (78) and markedly improved the humoral-mediated (12%) and cell-mediated immune response (19.27%) (76) via the improvement in the numbers of neutrophil, gamma-interferon (IFN-γ), interleukin-2 (IL-2), and granulocyte–macrophage colony-stimulating factor (GM-CSF) (88). Withaferin A and withanolide D present in the root extract of W. somnifera increased the antimicrobial activity of immune cells by boosting nitric oxide synthase action of the macrophages (89).
W. somnifera is also a natural source of anti-inflammatory steroids and exhibits potent anti-inflammatory effects (90). Extracts of W. somnifera have an anti-inflammatory activity in different rheumatological situations (91). The extracts markedly lowered both paw swelling and bony degenerative alterations in rats with arthritis induced by Freund's adjuvant (78). Withaferin A safely and effectively suppressed the arthritic syndrome in a study on arthritic animals. Individuals treated with hydrocortisone showed weight loss, while the animals medicated with withaferin A revealed weight gain (92).
Ashwagandha was reported as a natural antidepressant and anxiolytic agent (78, 93). The root extracts of ashwagandha induce a γ-aminobutyric acid (GABA)-like activity that is responsible for the anti-anxiety effects (94). In addition, W. somnifera exhibits a dose-dependent antistress activity in treated mice (90). Ashwagandha roots include steroids that act as exogenous adrenocortical steroids and decrease adrenocorticotropic hormone (ACTH) secretion and, consequently, endogenous steroid production. Therefore, W. somnifera is considered a growth promoter, particularly during development (49).
Extracts of W. somnifera also presented large dose-dependent responses in different parameters such as pulse rate, blood pressure, serum cortisol, creatinine, protein, hemoglobin, and considerably higher responses in mean fasting serum lipid and blood glucose (95). Methanolic extracts of ashwagandha reduced ulcer index, volume of gastric secretion, free acidity, and total acidity in models of gastric ulcer in rats (96). Sitoindosides IX and X, two glycowithanolides from W. somnifera, showed a potent antistress action, caused marked mobilization and stimulation of peritoneal macrophages and phagocytosis, and improved the activity of lysosomal enzymes (97).
Withanolides have both antibacterial and antifungal activities (68). The root extract of W. somnifera exhibited a significant in vitro antibacterial activity against Raoultella planticola, Bacillus subtilis, Enterobacter aerogens, Klebsiella pneumoniae, Agrobacterium tumefaciens, and Escherichia coli (98). The minimum inhibitory concentration (MIC) of W. somnifera was 0.039 mg mL−1 against K. pneumoniae, E. aerogens, and A. tumefaciens. W. somnifera root extracts also demonstrated an effective antifungal activity against Fusarium solani (54).
W. somnifera root powder is traditionally used for the treatment of pulmonary tuberculosis and bubonic plague in Garhwal Himalaya (99). In broiler chicks, supplementation of 20% W. somnifera root extract at 20 mL L−1 of water lowered the severity, mortality, and recovery time of E. coli challenge and improved the humoral and cellular immune responses, suggesting the root extract had a protective effect in minimizing the impact of E. coli infection in these birds (100). W. somnifera also alleviated infectious bursal disease virus (IBDV)-induced stress and histological and immunological alterations and reduced IBDV persistence in the host (101). These findings were confirmed by Kumari et al. (98) in a trial with Salmonella-challenged broiler chickens. The Salmonella-challenged chickens supplemented with 0.5% Withania showed less reduction in the body weight (1,800 ± 130.38 g) compared with unsupplemented Salmonella-challenged chickens (1,600 ± 70.71 g), while a significantly higher body weight of 1,980 ± 66.33 g was observed in uninfected Withania-supplemented broilers compared with the control uninfected group.
W. somnifera alkaloids display long-standing hypotensive, bradycardic, and respiratory-stimulant activities due to the autonomic ganglion blocking effect and depressant action on higher cerebral centers (102). Ashwagandha also restored the myocardial antioxidant status and retained membrane integrity by lowering malonyl dialdehyde levels in isoprenaline-induced heart muscle necrosis in mice (103).
The glycowithanolides withaferin A (VII–X), which are found in the roots of ashwagandha, control the growth of nerve cell dendrites, exhibit a GABA mimetic effect during healing of brain tissue, and reverse neurotic atrophy or synaptic loss leading to dementia (104). Ashwagandha root extract also elevates cortical muscarinic acetylcholine receptor capacity, which leads to a cognition-enhancing and memory-enhancing activity in humans and animals (105). Ashwagandha has been considered as a tonic and nootropic agent and accompanied an enhancement in scopolamine-induced memory deficits in mice (104). W. somnifera methanolic extracts induce neurite extension, and dendritic atrophy could be avoided by treatment with withanolides (104).
Withaferin A also presented antitumorigenic, anticancer, and antiproliferative effects against different tumor cell lines (106) due to a depression in the expression of nuclear factor-kappa B and suppression of intercellular tumor necrosis factor, as well as potentiation of radiation-induced apoptosis in tumorous cell lines (107, 108). An alcoholic extract of W. somnifera had an antitumor and radio-sensitizing activity in Chinese hamster cells and Swiss mice inoculated with Ehrlich ascites carcinoma cells (109, 110). W. somnifera extract also reduced leucopenia induced by clophosmide in experimental animals (111).
W. somnifera exhibits hypoglycemic, diuretic, and hypocholesterolemic effects (112). W. somnifera root extracts produce hypoglycemic and hypolipidemic impacts in alloxan-induced diabetic rats (113, 114). These antidiabetic effects may be due to enhanced hepatic metabolism, improvement in insulin synthesis from pancreatic β-cells, or insulin-sparing activity (115).
Impacts of W. somnifera on performance, blood parameters, and carcass quality of birds
The impacts of W. somnifera on birds' performance and productivity are summarized in Figure 3 and Table 1.
Figure 3. Impacts of Withania somnifera supplementation on birds' performance and productivity.
Table 1. Withania somnifera effects and application.
Impacts of W. somnifera on feed intake, body weight gain, and feed conversion ratio of birds
The inclusion of Withania in broiler feed improved feed consumption during the final 3 weeks (fourth to sixth week) of a trial (117). Sanjyal and Sapkota (130) recorded the average weekly feed consumption of 222, 432, 716, 764, and 798 g, respectively, from the second to the sixth week on a Withania-containing ration, with the highest digestibility (P < 0.05) observed in ashwagandha-supplemented chickens. FI was 7.9% higher in Withania-supplemented chickens compared with the control birds. Ansari et al. (135) also recorded significantly increased FI (4,580.64 g) in broilers maintained on 1% W. somnifera root powder-based ration compared with unsupplemented chickens (3,954.22 g).
However, Shisodiya et al. (118) recorded a reduction in FI in broilers on a 0.5% Withania-based diet compared with the control birds. The effect of Withania feeding on digestibility of the feed was also recorded by Pandey et al. (119) who observed a significantly higher body weight with concurrent significantly reduced FI (3,720.85 g bird−1) in broilers on a Withania-based diet as compared to the control birds (3,916 g bird−1). The average weekly FI of broiler chickens (kg/bird) from 1 to 6 weeks of age as a result of dietary inclusion of a Withania-based indigenous herbal drug revealed marked (P < 0.05) differences in the weekly feed consumption of broilers and was reported to be 0.230, 0.370, 0.530, 0.760, 0.770, and 0.960 kg, respectively, in the control birds and 0.210, 0.360, 0.510, 0.740, 0.750, and 0.930 kg, respectively, in the treated group (120). However, it was also observed that the level of Withania root powder supplementation at either 1 g or 2 g kg−1 of feed in the basal diet did not reveal a significant difference in overall FI in broiler chickens (138). The FI of Japanese quails was also improved on a 1% Withania root powder-containing basal diet (3,536.35 g) compared with the control group (3,154.18 g) (134). Vasanthakumar et al. (132) also recorded significantly increased FI in broilers maintained on 1% W. somnifera root powder-based ration compared with unsupplemented control chickens.
Ghosal et al. (97) discussed the general health tonic activity of W. somnifera. The results of various investigations on W. somnifera revealed that it has an anabolic impact and increases liver biosynthesis to raise the body weight in animals and humans (91). Moreover, numerous researchers have reported that medicinal herbs, particularly W. somnifera, could be employed as growth promoters in poultry diets to improve productivity. With supplementation of 0.5% W. somnifera root powder in broiler chicks, Shisodiya et al. (118) reported substantial improvements in growth parameters such as low birth weight (LBW) and weekly BWG. Vasanthakumar et al. (132) also referred to the beneficial effect of ashwagandha in broilers. Furthermore, Ansari et al. (135) examined the comparative efficacy of six medicinal herbs, such as W. somnifera, Nigella sativa, Ipomea digitata, Boerhavia diffusa, Azadirachta indica, and Corylus avellana, on the performance of 210-day-old broiler chickens and recorded the maximum WG in the group supplemented with W. somnifera (1,819 g), followed by Nigella sativa (1,805 g) and Azadirachta indica (1,800 g), when plants were supplemented at a rate of 4 g kg−1 of feed. Herbal drugs, including W. somnifera, Asparagus racemosus, and Mucuna pruriens, improved the body weight of VenCobb-400 broilers (120).
The synergistic effect of three different herbs, namely, ashwagandha, shatavari, and kapikachhu, on production performance of broilers was examined by Pandey et al. (119), and they concluded that ashwagandha, shatavari, and kapikachhu powder mixture in the ratio of 2:1:1 when added at a rate of 2% in the poultry ration of the VenCobb-400 broilers resulted in a higher body weight compared with that of the control chicks. The increased productivity of herbs-treated groups was attributed to the immunomodulatory, antioxidant, and antistress effects of W. somnifera (128, 139, 140). The feasibility of replacing antibiotic growth promoters with herbal growth promoters was discussed by Sanjyal and Sapkota (130) in a trial performed on 192 VenCobb-400 broilers with antibiotic (chlortetracycline), probiotic (Lactobacillus acidophilus), and three herbal (amla, tulsi, and ashwagandha) growth promoters. In this trial, the optimal live body weight (290 g) was observed in the Withania-treated group during the second week of the experiment and was significantly larger compared with the control and other treatments. The Withania-supplemented group also showed the maximum WG during the third (194 g) and fifth (412 g) weeks of the trial (130). The positive impact of W. somnifera on BWG of birds might be explained by the phytogenic contents of W. somnifera increasing the secretion of endogenous enzymes, improving hepatic function, and increasing hepatic protein biosynthesis, which are reflected in an increased BWG of the treated birds.
Rindhe et al. (117) compared the efficacy of W. somnifera-containing herbal formulation with synthetic ascorbic acid in a 42-day trial on VenCobb-400 broilers and found that the mean live body weight of the Withania-supplemented group was significantly (P < 0.01) higher (2,281.67 ± 4.05 g) compared with that of chickens supplemented with ascorbic acid (2,173.33 ± 4.31 g) and control birds (2,000.00 ± 8.35 g). Kumari et al. (98) recorded less reduction in the body weight (1,800 ± 130.38 g) in 0.5% Withania-supplemented Salmonella-challenged chickens compared with unsupplemented Salmonella-challenged chickens (1,600 ± 70.71 g) and a significantly higher body weight of 1,980 ± 66.33 g in uninfected Withania-supplemented broilers compared with uninfected control broilers. The body weight of broilers was significantly impacted by supplementation with 20 g W. somnifera extract L−1 water when compared with the control chicks (1,736.59 ± 0.44 g vs. 1,452.13 ± 0.89 g, respectively) (98).
Similar impacts on the body weight of broiler chicks following administration of 20 g W. somnifera extract were recorded by Sajjad (131) and Kakar (141). Furthermore, a 0.15% root extract of ashwagandha was significantly (p < 0.05) superior in improving the body weight of broilers as compared to the control and 0.5% ashwagandha root powder-fed chickens (2,297.11 ± 49.8 g vs. 1,947.83 ± 41.39 g vs. 2,214.78 ± 57.41 g, respectively) (132). These results corroborated the data of Singh et al. (85) who also recorded the elevated body weight in ashwagandha-fed chickens. A dose-dependent positive impact of W. somnifera on LBW and BWG in broilers was reported in several studies. A dose-related effect of Withania during the different weeks of a trial was reported in the study of Ahmed et al. (137). In this trial, the body weight of Ross broiler chickens in weeks 4 and 5 of the trial was affected more significantly (P ≤ 0.05) by the addition of W. somnifera to basal feed compared with the control chickens, and during the period from 3 to 4 weeks of age, chickens that received 0.75 g W. somnifera resulted in a significantly (P ≤ 0.05) higher BWG compared with control and other treated groups, whereas the final body weight and BWG at the final interval (4–5 weeks) were significantly (P ≤ 0.05) increased in 1.5 g Withania-supplemented chickens (137). The improvement in the body weight with age may be due to the impact of W. somnifera in stimulating the thyroid gland directly and/or through the pituitary gland to secrete more thyroid anabolic hormones (137).
Similarly, Joshi et al. (138) proved the anabolic effect of W. somnifera with two different doses (T2: 1 g kg−1 feed and T3: 2 g kg−1 feed) and noticed a marked (P < 0.05) impact on overall body weight of broilers and chicks maintained on 2 g Withania/kg of feed (T3), with a final body weight of 2,199.30 ± 40.20 g compared with 2,138.86 ± 34.5 g (T2) and 2,076.26 ± 22.27 g (T1: control). Average weekly BWGs were higher in W. somnifera-fed groups compared with the control at the first and third weeks and overall, for the trial. In addition, the total WG (g) was statistically highest (2,152.98 ± 40.27 g) in the group that received 2 g Withania/kg feed. On the contrary, Thange et al. (142) did not observe any impact of various doses of dietary supplementation of W. somnifera on the body weight in broilers. The dietary supplementation of ashwagandha not only improved the body weight in the thermo-comfort zone but also accelerated the body weight in temperature extremes. Furthermore, a polyherbal premix containing W. somnifera root powder added to the chicken feed significantly improved the body weight of broilers after a 6-week trial in the summer when the mean temperature–humidity index (84.74 ± 2.51) was greater than the thermo-comfort zone of broilers (133).
Japanese quails also exhibited an improvement in performance with the supplementation of ashwagandha. The addition of 1% ashwagandha root powder significantly (P < 0.05) enhanced the body weight of Japanese quail chicks (134). Similarly, Ahmed et al. (136) reported a significant (P ≤ 0.05) improvement in BWG of quails fed with a 100 mg kg−1 ethanolic extract of ashwagandha as compared to the control birds.
The FCR (amount of feed intake/unit LWG) ultimately determines the economics of the broiler industry. A significant reduction in FCR was recorded by Shisodiya et al. (118) in broiler chicks when the basal diet was supplemented with 0.5% Withania root powder. Comparison of the effect of Withania and five different herbs, such as Corylus avellana, Boerhavia diffusa, Ipomea digitata, Azadirachta indica, and Nigella sativa, in broilers also revealed a significantly better FCR during most weeks in the birds fed the Withania-included diet (135). Rindhe et al. (117) reported a lower FCR (2.05) in ashwagandha-fed birds compared with ascorbic acid-supplemented and control broilers. A comparative study conducted by Sanjyal and Sapkota (130) in broiler chickens resulted in an improved FCR in a group fed with Withania root powder compared with antibiotic and two other herbs, namely, amla and tulsi.
Srivastava et al. (120) recorded enhanced weekly FCR from the first to the sixth week of age in Withania-treated broilers. The overall FCR (1.74) during all the weeks was statistically very low in broilers reared on 2% herbal formulation containing 50% Withania powder compared with the control birds (2.07) (119). A numerically improved feed conversion efficiency was recorded by Vasanthakumar et al. (132) in broiler chickens reared on 0.15% ashwagandha root extract. However, the graded level of Withania supplementation at 1 g kg−1 of feed and 2 g kg−1 of feed did not result in a significant (P > 0.05) difference in FCR in broiler chickens (138). Non-significant differences in FCR were also reported by Thange et al. (142). The improvement in feed efficiency was also observed in Japanese quails (134) with the addition of W. somnifera. 0.5%, 1.0%, and 1.5% Withania root powder feed supplementation (143). The enhanced FCR (P ≤ 0.05) was also reported when quails were supplemented with the ashwagandha root ethanolic extract (100 mg and 200 mg kg−1 feed) or with 2 g kg−1 diet of root powder in contrast to controls (136). A significant increase in FI of 3,231.27 ± 0.44 g was recorded in broiler chicks supplemented with a 20 g extract of W. somnifera L−1 water when compared with the control group (2,864.91 ± 0.89 g) (144).
To summarize, the overall improvement in the performance of poultry supplemented with dietary W. somnifera could be due to the impact of W. somnifera on increasing the level of the anabolic hormones, enhancing endogenous enzyme production, increasing nutrient digestion and absorption, improving liver function, increasing antioxidant capacity, and elevating hepatic protein biosynthesis.
Impacts of W. somnifera on hematological and biochemical blood parameters
The hematinic activity of W. somnifera on broiler chickens was recorded by Kumari et al. (98), who found a significantly higher Hb level, the packed cell volume (PCV), and non-significant mean corpuscular volume (MCV) and mean corpuscular hemoglobin concentration (MCHC) values between control and Withania-treated birds. The hematinic activity of W. somnifera root powder is attributed to direct and indirect action on the hematological parameters. A direct positive impact of W. somnifera was noticed on hemopoiesis in broiler chicks via stimulation of stem cell proliferation and improved bone marrow cellularity (49, 144). Also, W. somnifera root powder protected red blood cells from oxidative stress in broiler chickens through its antioxidant effect and improvement in the erythrocytic enzyme activity (133). Daisy (145) in broilers and Bhardwaj et al. (134) in Japanese quails reported significant improvements in total erythrocytic numbers. Less intense anemia was recorded in Salmonella-infected broiler chickens raised on ashwagandha root powder, with the chicks rapidly recovering from Salmonella infection (98). In broilers treated with the extract of Withania root powder (10, 20, and 30 g L−1), there was no significant difference in Hb levels (116). In contrast, Bhardwaj et al. (134) discovered a considerable increase in Hb content in Japanese quails. The PCV value of broilers treated with Withania extract at 10 and 20 g L−1 was considerably greater compared with that of the equivalent control group chicks (116).
Bhardwaj et al. (134) found a significant and linear rise in PCV in Japanese quails after adding increasing amounts of ashwagandha root powder (0.5, 1.0, and 1.5%) compared with the untreated quails. Marked elevations in phagocytic cell counts (55, 146, 147), along with an increase in phagocytic potential, were reported in avian species supplemented with W. somnifera (128). Furthermore, Gautam et al. (62) recorded a marked elevation in numbers of white blood cells of broilers. A higher mean total leukocyte count in chicks supplemented with 20 g L−1 Withania root extract was recorded; however, differences in the levels of monocytes, neutrophils, eosinophils, and lymphocytes in Withania-supplemented chicks were not significant when compared with the values found in the control chicks (116). The level of lymphocytes in broilers treated with 1.5% ashwagandha was significantly elevated up to 53.59% with no change in heterophil and monocyte levels (134).
The considerable hypoglycemic effect (12%) of W. somnifera root powder observed in human subjects was infrequently confirmed in broilers (112). The blood glucose level in broilers at the end of the sixth week of a trial was unaffected by a herbal preparation including W. somnifera root powder supplemented at 2% in basal diet (120). A similar non-significant role of ashwagandha on serum glucose levels was recorded in guinea pigs (148). Furthermore, broilers treated with ashwagandha leaves also showed non-significant alterations in blood glucose levels (137). However, lower plasma glucose (182.18 mg dl−1) was reported in broiler chickens treated with Withania at 0.01% of diet compared with that of control birds (249.52 mg dl−1) (133). The hypoglycemic impact of ashwagandha in broilers was predominantly reported under stress (149).
The elevation in serum protein following administration of Withania is due to the direct anabolic effect of ashwagandha or occurs indirectly through an increase in thyroid hormone level (150). During experimental hyperglycemia, W. somnifera root extract was reported to effectively reverse increased proteolysis and lower protein levels and improve serum albumin and total protein levels, which never strayed from the normal range during the experiment (113). The serum protein regulatory activity of ashwagandha was confirmed by Verma and Gaur (76) in pesticides-intoxicated cockerels, with 20 mg Withania root extract/bird/day producing a marked elevation in serum protein levels in the cockerels. In Salmonella-infected broilers, 0.5% ashwagandha root powder had a strong resistive effect on serum protein and albumin levels, as well as a marked elevation in serum globulin level (98). However, ashwagandha leaves did not confer this protein-modulating role (137). Significant rises in serum total protein and globulin concentrations with numerical elevation in albumin level were observed in broilers raised on W. somnifera root powder (151), and W. somnifera root extract at 20 mg/day/bird for month significantly accelerated serum total protein to 24.42 g/100 mL compared with 15.7 g 100 mL−1 in control cockerels (150).
The anabolic impact of ashwagandha was more effective under stress in broilers. In addition, a significant recovery from enrofloxacin-induced hypoproteinemia was reported in broilers treated with ashwagandha (152). Reductions in the severity of depression in serum total protein and albumin were recorded in Salmonella gallinarum-challenged broilers on ashwagandha supplementation (98). Withania-supplemented broiler chickens revealed higher plasma protein and total globulin levels compared with the control birds (133). Locally prepared herbal drugs, including W. somnifera, Mucuna pruriens, and Asparagus racemosus, supplemented at 2% of broiler ration resulted in non-significant differences in serum total protein among control and treated birds (120).
The total plasma cholesterol at 0.01% ashwagandha of broiler ration was significantly decreased compared with that of untreated control birds (133). Moreover, 2% W. somnifera root powder supplementation in layers revealed a 30% reduction in egg cholesterol concentrations and 26% lowering in egg-yolk triglycerides (153). Research in humans and rats verified the hypocholesterolemia and hypolipidemic impact of ashwagandha root powder (112, 113). The addition of 0.5% ashwagandha root powder markedly lowered the concentration of two major negative hepatic health indicator enzymes, namely, serum alanine aminotransferase (ALT) and aspartate aminotransferase (AST), in broilers infected with Salmonella gallinarum, while lactate dehydrogenase (LDH) activity remained markedly higher until the end of the experiment (35 days) and a significantly low decline in alkaline phosphatase (ALP) was recorded (98).
The hepatoprotective and cardioprotective activity of ashwagandha is due to the presence of alkaloids, withanolides, and free-radical scavenging characteristics of ashwagandha (60). E. coli-challenged guinea pigs and treated with W. somnifera also revealed a similar decrease in ALT and AST concentrations (148). Supplementation of ashwagandha in pesticides-intoxicated cockerels markedly reduced the toxic impact of the pesticides in terms of lowering ALT and AST concentrations with a concurrent significant appreciation in the activity of ALP related to development (149). The ALT- and AST-reducing effect of roots of W. somnifera was not observed with leaves of ashwagandha in broiler chickens (132). In contrast, a trial on a herbal preparation containing W. somnifera did not significantly impact serum ALT and AST in broiler chickens fed at 2% per kg of ration (120). A calcium-sparing impact of ashwagandha was recorded by Varma et al. (149).
Finally, the positive impact of W. somnifera on hematological and biochemical blood parameters could be attributed to the hematinic activity of W. somnifera in stimulating stem cell proliferation, improving bone marrow cellularity, elevating antioxidant capacity that delays lipid oxidation, increasing erythrocytic enzyme activity, improving phagocytic activity, elevating white blood cells production, regulating serum proteins, and reducing total plasma cholesterol and its different alkaloids. In addition, the withanolide contents of W. somnifera act as free-radical scavengers that mitigate the oxidative stress impacts and show hepatoprotective and cardioprotective effects.
W. somnifera antioxidant potential and its impacts on carcass characteristics and meat quality
Following exposure to acute and chronic heat stress, significant negative impacts on livability, productivity, immunity, and illness susceptibility were observed in poultry (154). Heat stress might contribute to the inferiority of acquired immunity in high-meat-yielding broiler lines. Heat stress lowered both cell-mediated and humoral immunity in birds, explored through evaluation of phagocytic activities and serum antibody titers, respectively (155). Significant amelioration (P < 0.05) in recovery from Salmonella gallinarum experimental infection was observed at 28 days post-infection of broilers supplemented with ashwagandha root powder (156).
The usage of different antioxidants in Cobb male broilers revealed a linear increase in serum T3 and T4 under heat stress (157). Furthermore, the use of a herbal preparation at 0.01% in basal feed—containing W. somnifera as one of the main ingredients—under thermal stress (84.74 ± 2.51 temperature–humidity index) significantly accelerated serum total protein and serum globulin in broiler chickens compared with the control birds, while there was non-significant variation in albumin content between treated and control broilers (133).
Ashwagandha protects broilers in terms of lowering mortality due to infection-related stress and promotes early recovery from disease. A ten-fold lower mortality (1.42%), relative to the control (14.28%), was reported by Pandey et al. (119) in broilers supplemented with ashwagandha. Kumari et al. (98) observed a considerable decline (50%) in mortalities of broiler chickens when the birds were supplemented with 0.5% W. somnifera root powder. The antistress and adaptogenic effect of ashwagandha lowered the severity of the infection and facilitated the early recovery of broilers from experimental infection with Salmonella gallinarum. Also, the cumulative mortalities in broilers were reported to be 4.4, 2.2, and 2.2% in control, 0.1%, and 0.2% ashwagandha-fed broilers, respectively (138). Similar results were recorded in mice treated with W. somnifera during experimental salmonellosis, indicating that supplementation with W. somnifera might have a promising impact in various species (61, 120).
Sanjyal and Sapkota (130) reported a higher dressing percentage in Withania-raised broilers (78%) as compared to the control birds (76%). A similar finding was reported by Ahmed et al. (137) who showed a non-significant elevation in dressing percentage in birds supplemented with 1.5 g ashwagandha leaves (76.41%) when compared with the control birds (75.23%). The leg weight of control (23.46%) and ashwagandha-fed broilers (22.20%) was also not significantly different (130). Congruent with this, non-significant differences in breast (40.18 and 37.04%) and thighs cut percent (25.90 and 27.60%) were reported in treated and control broilers (137). Conversely, Rindhe et al. (117) recorded a positive impact of a polyherbal antistress and antioxidant preparation containing W. somnifera, Ocimum sanctum, Terminalia chebula, and Phyllanthus emblica in increasing the carcass yield, dressing percentage, and filet, tender, and giblet yields. In the supplemented group, carcass yield was improved by 29.64%, dressing percentage by 0.83%, filet yield by 23.2%, tender yield by 12.88%, and giblet yield by 10.8%.
Similar findings of higher dressing percentage, breast weight, and leg weight were reported in groups fed with 10 ml plant extract (62.3%) when compared with control (51.11%) (158). The weight of liver in 1% ashwagandha and 0.15% ashwagandha extract (2.50)-supplemented broiler groups showed non-significant increases in the examined measures compared with the control chickens (132). Also, Sanjyal and Sapkota (130) found statistically similar percentage relative weights of liver, heart, and gizzard in broilers raised with W. somnifera. Vasanthakumar et al. (132) recorded a non-significant alteration in intestinal length of carcasses of broilers supplemented with ashwagandha as compared to the control birds; the observed intestinal lengths were 183.75, 213.50, and 221.33 cm in birds fed with control, ashwagandha root powder at 1% of feed, and ashwagandha root extract at 0.15% of feed, respectively.
The impact of W. somnifera on broiler meat quality is represented in Figure 4. The addition of ashwagandha to the basal feed of broilers significantly affects the sensory qualities of broiler meat. Meat from the broilers fed herbal feed additive containing W. somnifera was reported to be superior to the control with respect to all attributes, including flavor (6.72 and 5.90 for supplemented and control groups, respectively), appearance (7.32 and 6.5), tenderness (7.13 and 6.14), juiciness (7.30 and 7.01), stickiness to mouth (7.24 and 6.11), and overall acceptability (7.5 and 6.03) (119).
Figure 4. Impacts of Withania somnifera supplementation on broiler meat quality.
Another sensory evaluation of broiler meat revealed significant increases in organoleptic traits of broiler meat, i.e., appearance (6.10 and 6.48 for control and treated groups, respectively), odor (5.8 and 6.81), color (6 and 6.81), flavor (5.66 and 6.5), juiciness (6.1 and 6.83), texture (6 and 6.8), and overall palatability (6 and 6.6), in groups treated with plant products AV/LAP/19 including ashwagandha, compared with the control group (117). Improved tenderness with palatability was attributed to increases in collagen and myofibrillar solubility of meat due to AV/LAP/19 supplementation (117). The oxidative stability of broiler meat expressed in terms of thiobarbiturate acid (TBA) level displayed significantly lower values in the AV/LAP/19-treated group at the end of the 15th, 30th, 45th, and 60th storage days (0.33, 0.35, 0.42, and 0.54 mg malonaldehyde/kg, respectively) in comparison with those of the control group (0.31, 0.39, 0.50, 0.60, and 0.66 mg malonaldehyde/kg, respectively) (117).
In addition, a reduced level of tyrosine in broiler meat, which is indicative of less proteolysis, was recorded upon supplementation of AV/LAP/19 plant product. Thus, the reduced TBA and tyrosine level of broiler meat reported in the AV/LAP/19-treated group was found to improve the shelf life of frozen raw meat (117). Inclusion of the W. somnifera at 100 or 200 mg/kg in the diet of the broilers negated the negative impacts of oxidized oil by reducing the MDA content in thigh meat and increasing the activity of antioxidant enzymes, thereby improving the performance, immune reaction, and meat oxidative stability of broilers exposed to oxidative stress (53, 159).
W. somnifera immune modulation features
Manoharan et al. (53) reported an elevated antibody titer following consumption of W. somnifera extract in various avian models. W. somnifera extract at 10, 20, and 30 g L−1 effectively improved the antibody titer against infectious bursal disease (IBD) (116). The immunoglobulin concentrations were higher in 1.5% ashwagandha-fed Japanese quail compared with the control birds (134). The immune status of broilers as expressed by antibody titer values (log2) was enhanced in 1% ashwagandha root powder-treated (7.3) and 0.15% ashwagandha extract-treated (7.0) groups as compared to the control birds (6.6) (132). In addition, 1% ashwagandha root powder-raised broilers exhibited better immunity compared with the control birds (139), and humoral immunity of broilers was improved with ashwagandha root powder supplementation (159). In broiler during summer stress, total immunoglobulin was elevated following 0.01% W. somnifera supplementation (3.83) as compared to the control (2.79) (133). Okonkwo et al. (160) concluded that a high antibody titer could be obtained in broiler groups raised on herbal preparations including ashwagandha.
Impact of W. somnifera on broiler economics
The impact of W. somnifera addition on economic efficiency of broilers is expressed in Figure 5.
Figure 5. Impacts of Withania somnifera supplementation on economic efficiency of broilers.
Pedhavi et al. (161) reported a better net return upon treatment with a 20% root extract of W. somnifera in broilers. The improved net return was also reported by Javed et al. (158) following combined treatment with W. somnifera and Berberis lycium compared with their individual outcomes, which could be attributed to efficient feed utilization by the broiler chickens at 10% extract of the tested herbs. Ansari et al. (135) performed economic evaluation and showed a maximum profit per bird in W. somnifera root powder-raised broiler chickens (Rs. 21.44) compared with broilers fed with Nigella sativa (Rs. 20.60), Azadirachta indica (Rs. 20.38), or control birds.
In another study, net return was highest in the ashwagandha-treated group (Rs. 48.48), followed by synthetic growth promoters (Rs. 47.92) and then control birds (Rs. 47.34) (118). Mane et al. (162) also noted a higher net profit per bird in broilers fed with ashwagandha. In contrast, Kale et al. (163) reported less net profit per bird fed with ashwagandha (Rs. 15.60) compared with the control (Rs. 16.55); however, gross return was significantly higher in 0.25% ashwagandha-treated broiler chickens (Rs. 110.10) compared with the control group (Rs. 107.58). A higher cost of production observed for probiotic-supplemented (Rs. 141.8) and ashwagandha-supplemented (Rs. 134.7) groups as compared to the control group (Rs. 128.3) was due to the extra cost incurred on the usage of ashwagandha root powder and probiotics (130).
Conclusion
Withania somnifera is rich in valuable active components such as alkaloids and withanolides that act as free-radical scavengers, increase antioxidant capacity, stimulate the secretion of endogenous digestive enzymes, increase nutrient digestibility, improve blood parameters, enhance immunity, mitigate the negative impacts of stress, and alleviate the impact of diseases. Therefore, incorporation of W. somnifera, especially at a level of 2.5 g kg−1 feed in poultry ration or 20 ml l−1 in the drinking water, improves the livability, productivity, carcass traits, meat quality, disease resistance, blood parameters, and immunological status of the treated bird. Further, investigations should be adopted to determine the mechanism of action of potential active components of W. somnifera extracts and suggest the ideal dose and application method of these ingredients to obtain maximum beneficial effects.
Author contributions
All authors contributed equally to this review and have read and agreed to the published version of the manuscript.
Acknowledgments
KE-T thanks the library at Murdoch University, Australia for the valuable online resources and comprehensive databases. The authors would like also to thank the Fundação de Am-paro à Pesquisa do Estado do Rio de Janeiro (FAPERJ) Brazil—Grant Number (E-26/200.891/2021), and the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq)—Grant Number (313119/2020-1) for the financial support.
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
Publisher's note
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Keywords: antioxidant, birds' productivity, herbal extract, poultry, Withania somnifera
Citation: Salem HM, El-Saadony MT, Abd El-Mageed TA, Soliman SM, Khafaga AF, Saad AM, Swelum AA, Korma SA, Gonçalves Lima CM, Selim S, Babalghith AO, Abd El-Hack ME, Omer FA, AbuQamar SF, El-Tarabily KA and Conte-Junior CA (2022) Promising prospective effects of Withania somnifera on broiler performance and carcass characteristics: A comprehensive review. Front. Vet. Sci. 9:918961. doi: 10.3389/fvets.2022.918961
Received: 14 April 2022; Accepted: 11 July 2022;
Published: 02 September 2022.
Edited by:
Domenico Bergero, University of Turin, ItalyReviewed by:
Muhammad Shazaib Ramay, Ankara University, TurkeyTiago Goulart Petrolli, University of West of Santa Catarina, Brazil
Copyright © 2022 Salem, El-Saadony, Abd El-Mageed, Soliman, Khafaga, Saad, Swelum, Korma, Gonçalves Lima, Selim, Babalghith, Abd El-Hack, Omer, AbuQamar, El-Tarabily and Conte-Junior. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: Synan F. AbuQamar, c2FidXFhbWFyJiN4MDAwNDA7dWFldS5hYy5hZQ==; Khaled A. El-Tarabily, a3RhcmFiaWx5JiN4MDAwNDA7dWFldS5hYy5hZQ==