Introduction
Antibiotic-based growth promoters have been commonly used as supplements in animal feeds for many years because they are well known to help growing animals to digest their food more efficiently and to grow strong and healthy individuals (Sojoudi et al., Reference SOJOUDI, DADASHBEIKI and BOUYEH2012). Some of the common antibiotics used in animal feeds are virginiamycin, salinomycin, neomysin, doxycyclin and avilamycin (Kumar et al., 2010). The use of antibiotic-based growth promoters has faced serious criticism and global concern due to their purported hazardous effects including microbial resistance, and their potentially harmful effects on human health (Rahmatnejad et al., Reference RAHMATNEJAD, ROSHANFEKR, ASHAYERIZADEH, MAMOOEE and ASHAYERIZADEH2009). These shortcomings lead to the search for alternative substances that eliminate these threats (Manesh, Reference MANESH2012). Nowadays there is increasing interest in the use of natural growth promoters such as probiotics, prebiotics or their combination and medicinal plants as feed additives in poultry diets to enhance the performance of poultry birds (Khan et al., Reference KHAN, DURRANI and CHAND2010; Reference KHAN, NAZ, TUFARELLI, SELVAGGI and LAUDADIO2011a).
Garlic (Allium sativum) has been known in folk medicine for thousands of years in the history of Greeks and Egyptians (Horton et al., Reference HORTON, FENNELL and PRASAD1991). Garlic is best known as a spice and herbal medicine for the treatment and prevention of an array of diseases (Adibmoradi et al., Reference ADIBMORADI, NAVIDSHAD, SEIFDAVATI and ROYAN2006). Garlic contains at least 33 sulphur containing compounds, several enzymes and 17 amino acids and minerals including selenium (Newall et al., Reference NEWALL, ANDERSON and PHILLIPSON1996). The major active ingredients in garlic are allicin, ajoene, diakyl polysulphides, s-allylcysteine, diallydisulphide, s-methyl-cysteine sulphoxide and s-allylcysteine sulphoxide, which may be responsible for the therapeutic properties of garlic observed (Chi et al., Reference CHI, KOH and STEWART1982; Canogullari et al., Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010). In the last decade, garlic has been widely reported to be incorporated into poultry diets to determine any effects on poultry performance. In this review, the literature regarding the use of this natural product is discussed.
Effects of garlic on broiler production
Numerous reports have been published, advocating the beneficial effects of garlic on feed efficiency and growth of broiler chickens. According to Mansoub (Reference MANSOUB2011), feed conversion ratio (FCR) and body weight (BW) of broilers were improved when they were fed garlic (1g/kg) in the basal diet. Aji et al. (Reference AJI, IGNATUIUS, ADO, NUHU and ABDULKARIM2011) reported that administration of 100 mg of garlic resulted in improved body weight gain at 7, 14 and 21 days of treatment in broiler chicks, although feed intake, FCR and carcass yield did not change. Kumar et al. (2010) found that a garlic supplemented diet (250 ppm) significantly increased the body weight gain of broiler chickens in a 42 day trial. In the same year, Pourali et al. (Reference POURALI, MIRGHELENJ and KERMANSHAHI2010) reported that garlic powder improved average daily feed intake, body weight gain, FCR, performance index as well as survivability. Mahmood et al. (Reference MAHMOOD, HASSAN, ALAM and AHMAD2009) concluded that a basal feed containing 0.5% garlic improved FCR and body weight gain in broilers but failed to produce positive effects on carcass yield in term of dressing percentage, relative weight of heart, gizzard, liver, spleen and pancreas. Javed et al. (Reference JAVED, DURRANI, HAFEEZ, KHAN and AHMAD2009) found that feed intake and FCR, body weight and carcass quality (dressing percentage, breast weight and leg weight) were improved in a 35 day experimental trial, when broilers were supplemented (at the rate of 10 ml/litre of drinking water) with an aqueous extract of medicinal plants containing garlic. Ramakrishna et al. (Reference RAMAKRISHNA, PLATEL and SRINIVASAN2003) suggested that garlic supplementation enhances the activity of pancreatic enzymes and provides an environment for better absorption of nutrients.
In 2008, Javandel et al. observed that feeding garlic at the level of 0.125 and 0.25% resulted in higher feed intake during the starter phase of broilers, although the same levels were not efficacious during the growing phase. Additionally, in this experiment, the authors did not find any difference in body weight and carcass characteristics in term of percentage of carcass, small intestines, proventriculus, gizzard, liver and abdominal fat. Ashayerizadeh et al. (Reference ASHAYERIZADEH, DASTER and SHARGH2009) demonstrated that garlic powder added into broiler feed had a significant effect on carcass yield, but feed intake and efficiency, body weight, thigh and breast weight did not change, although abdominal fat percentage decreased in garlic supplemented birds. Similarly, Mohebbifar and Torki (Reference MOHEBBIFAR and TORKI2011) reported that feeding garlic at 0 or 2 g/kg did not affect feed intake, FCR and weight gain in Ross broilers. Rahmatnejad et al. (Reference RAHMATNEJAD, ROSHANFEKR, ASHAYERIZADEH, MAMOOEE and ASHAYERIZADEH2009) concluded that garlic given at the rate of 1000 g/ton of feed did not affect feed intake, FCR and body weight gain. Horton et al. (Reference HORTON, FENNELL and PRASAD1991) and Konjufca et al. (Reference KONJUFCA, PESTI and BAKALLI1997) could not trace any effect of garlic supplementation on the performance of broiler chicks. Such a wide range of results may be attributed to the dose, duration and processing of the medicinal plants as well as the experimental conditions. Khan et al. (Reference KHAN, HASAN, SARDAR and ANJUM2008) suggested that differences in the results determined by different authors may be due to the use of different commercial products of garlic. The commercial garlic products may be divided into raw garlic (allicin rich) and processed garlic (non-allicin rich) which differ in the active substances they contain.
Effect on laying hen performance
Egg production and quality are heritable traits of major concern for breeders, industry and consumers. To improve these characteristics, correct nutritional, management and environmental practices are needed to enhance egg production and quality. Eggs are a delicate product which can lose quality rapidly during the period of collection to consumption. Thus improvement in egg quality is of paramount importance in the field of production and management (Mahmoud et al., Reference MAHMOUD, SAAD, GHARAIBEH, ZAKARIA and AMER2010). There is a dearth of literature available concerning the beneficial effects of garlic on egg quality. For example, Yalcin et al. (Reference YALCIN, ONBASILAR, REISLI and YALCIN2006) found that egg weight increased when laying hens were fed 5 and 10 g/kg garlic powder. Khan et al. (Reference KHAN, SARDAR and ANJUM2007) reported that egg production increased during the six weeks in which 0, 2, 6 or 8% garlic powder was fed to laying hens. Lim et al. (Reference LIM, YOU, AN and KANG2006) concluded that with increasing dietary garlic powder, the Haugh unit increased linearly after two weeks. Chowdhury et al. (Reference CHOWDHURY, CHOWDHURY and SMITH2002) also reported that yolk weight responded in a quadratic manner to increasing levels of sun-dried dietary garlic paste. Canogullari et al. (Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010) demonstrated that egg production increased significantly by adding 1% garlic powder in the feed of the laying hens, although egg weight, yolk index, shell weight, shell thickness, yolk weight did not change. In the same experiment, egg shell index and Haugh unit decreased significantly in the birds supplemented with 4% garlic powder. Yalcin et al. (Reference YALCIN, ONBASILAR, REISLI and YALCIN2006) reported that the supplementation of garlic powder had no significant effect on egg albumen index, egg shell index and egg Haugh unit values when laying hens were fed 5 and 10 g/kg garlic powder for 22 weeks. According to Mahmoud et al. (Reference MAHMOUD, SAAD, GHARAIBEH, ZAKARIA and AMER2010) egg albumin, yolk and shell weight as well as albumin height and Haugh unit were improved when laying hens were supplemented with 0.25, 0.50 and 1% garlic juice. Mottaghitalab and Taraz (Reference MOTTAGHITALAB and TARAZ2002) showed that the inclusion of 0, 5, 10 and 15 g/kg garlic powder significantly decreased yolk weight. Reddy et al. (Reference REDDY, LIGHTSEY and MAURICE1991) and Chowdhury et al. (Reference CHOWDHURY, CHOWDHURY and SMITH2002) concluded that supplementation of garlic did not affect egg production. Khan et al. (Reference KHAN, HASAN, SARDAR and ANJUM2008) concluded that feeding 8% dried garlic power may result in better egg production in Desi laying hens, with no effect on egg mass and egg weight. The differences in the results of different reports may be due to the different experimental protocols and garlic preparation in their experiments (Canogullari et al., Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010).
Immuno-modulating effects
The immune system of poultry can be broadly divided into two categories namely, the lymphoid and non-lymphoid systems. Bursa of fabricius and thymus are considered to be the primary lymphoid organs, whereas spleen is usually termed as secondary lymphoid organ. The non-lymphoid parts of the immune system include cells that provide a non-specific immunological defence to the host. Blood monocytes and tissue macrophages are unique due to their ubiquitous distribution throughout the body fluids, organs and cavities (Khan et al., Reference KHAN, NAZ, TUFARELLI, SELVAGGI and LAUDADIO2011b). Recently, Zialarimi et al. (2011) found that aqueous extract of garlic was more effective in inhibiting E. coli culture than mint (Menthe spp.) and onion (Allium cepa) in broiler chicks, suggesting the role of garlic in suppressing pathogenic bacteria.
Several reports are available advocating the strong immune potentiating effects of garlic. Szigeti et al. (Reference SZIGETI, PÁLFI, NAGY, INÉ, É., NAGY, SZMOLÉNY, BAGÓ and RADVÁNYI1998) reported that supplementing chickens with a modified product including garlic increased antibody production against Salmonella enteritidis, Pasteurella multocida and Leptospira Pomona bacteria. Ahsan-ul-Haq et al. (1999) reported that feeding broilers at the rate of 20 g/kg increased significantly antibody titre against Newcastle disease virus (NDV) and infectious bursal disease (IBD) in broiler chicks. Szigeti et al. (Reference SZIGETI, PÁLFI, NAGY, INÉ, É., NAGY, SZMOLÉNY, BAGÓ and RADVÁNYI1998) found that a product containing garlic, acidifiers and bacterial cell extracts enhances antibody production against NDV, whereas, Jafari et al. (Reference JAFARI, RAZI, GHORBANPOOR and MARASHIAN2008) reported that supplementing broilers with garlic (1 or 3%) does not have any beneficial effects on antibody production. Hanieh et al. (Reference HANIEH, NARABARA, PIAO, GERILE, ABE and KONDO2010) found that feeding garlic at the level of 10 g/kg diet enhanced titre against NDV and sheep red blood cells (RBCs) in White Leghorn chickens, although such effects were not recorded when the dose was as high as 30 g/kg. In the same line, Dorhoi et al. (Reference DORHOI, DOBREAN, ZAHAN and VIRAG2006) observed that macrophage engulfing RBCs percentage was higher when the laying hens were supplemented with 50 µg/ml of garlic and the engulfment was low when the dose was increased to 200 µg/ml. Recently, Nidaullah et al. (Reference NIDAULLAH, DURRANI, AHMAD, JAN and GUL2010) found that a plant mixture containing garlic at the level of 4 g produced better antibody response against NDV and IBD in broiler chicks. Rahimi et al. (Reference RAHIMI, ZADEH, KARIMI, OMIDBAIGI and ROKNI2011) found that 0.1% garlic in the diet of broilers improved antibody response against sheep RBCs and NDV, increased bursa of Fabricious weight and spleen weight and augmented hypersensitivity coetaneous basophilic response. Dorhoi et al. (Reference DORHOI, DOBREAN, ZAHAN and VIRAG2006) reported that garlic supplemented birds had heavier spleen and thymus weight and white blood cells (WBCs) count. The increase in the weight of the spleen and thymus are attributed to the enhanced lymphocyte proliferation and the increase in the WBCs production. Pourali et al. (Reference POURALI, MIRGHELENJ and KERMANSHAHI2010) showed that different concentrations of garlic powder improved antibody titre against NDV virus at 14th day of age. Hanieh et al. (Reference HANIEH, NARABARA, PIAO, GERILE, ABE and KONDO2010) suggested that the immuno-modulating effect of garlic is associated with its ability to enhanced phagocytosis of peritoneal macrophages, increased production of interleukins, interferon (INF- γ) and tumour necrosis factor (TNF- α) secretary metabolism of macrophages, antigen presenting cells and antioxidant function of this plant.
Mohebbifar and Torki (Reference MOHEBBIFAR and TORKI2011) demonstrated that adding 0 or 2g/kg garlic in the basal feed of Ross broilers did not affect the heterophil, lymphocyte, monocytes, eosinophil, basophil and heterophil to eosinophil ratio nor the serum antibody against NDV was positively changed. The discrepancies observed in the results are likely related to the preparation methods of garlic. In addition, the experimental design and dose of garlic used have a great deal in the differences of the results of immune functions (Hanieh et al., Reference HANIEH, NARABARA, PIAO, GERILE, ABE and KONDO2010).
Anti-cholesteremic effect
In the scientific literature, the hypolipidic and hypocholesterolimic effects of garlic are well documented. Ahsan-ul-Haq et al. (1999) reported that feeding garlic at the rate of 20 g/kg decreased blood cholesterol significantly in broiler chicks. Egg yolk cholesterol of laying hens decreased significantly in birds supplemented with 1 and 2% garlic powder (Canogullari et al., Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010). Chowdhury et al. (Reference CHOWDHURY, CHOWDHURY and SMITH2002) concluded that cholesterol concentration per gram of yolk decreased linearly with increasing levels of sun-dried dietary garlic paste. Khan et al. (Reference KHAN, SARDAR and ANJUM2007) showed that feeding dietary garlic at 2, 6 or 8% reduced egg yolk cholesterol, on average over six weeks, by 5.7, 14.3 and 23.6%, respectively. Khan et al. (Reference KHAN, HASAN, SARDAR and ANJUM2008) found that garlic powder given at the level of 8% may result in better serum and egg yolk cholesterol profile in laying hens. However, Mahmoud et al. (Reference MAHMOUD, SAAD, GHARAIBEH, ZAKARIA and AMER2010) observed that egg cholesterol did not change when laying hens were supplemented with garlic extracts in different concentrations (0, 0.25, 0.5 and 1%). If egg cholesterol can be reduced to minimum level, it would assist in the consumer perception regarding the healthiness of table eggs (Mahmoud et al., Reference MAHMOUD, SAAD, GHARAIBEH, ZAKARIA and AMER2010). Recently, in the study of Canogullari et al. (Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010) garlic powder at the rate of 1, 2 and 4% were found to reduced total lipid concentration and total trigylceride levels. Total triglyceride level was reduced by garlic powder supplementation at the levels of 1 and 2% garlic in laying hens (Azeke and Ekpo, Reference AZEKE and EKPO2008). Similarly, Yalcin et al. (Reference YALCIN, ONBASILAR, REISLI and YALCIN2006) reported a significant decrease in plasma triglycerides with the supplementation of garlic powder. Youn et al. (Reference YOUN, NAM, KIM, KANG, OHTANI and TANAKA1996) concluded that serum triglyceride was lowered by supplementing garlic powder to the diet.
Horton et al. (Reference HORTON, FENNELL and PRASAD1991) found that broilers fed garlic at 10,000 mg/kg reduced plasma cholesterol in 35 days treatment. Publications by Qureshi et al. (Reference QURESHI, DIN, ABUIRMEILEH, BURGER, AHMAD and ELSON1983b) documented that the serum cholesterol concentration in White Leghorn pullets was reduced from 20 to 25% using supplements of garlic paste, solvent extracted garlic paste and commercial garlic oil. Canogullari et al. (Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010) found that 1, 2 and 4% garlic powder increased high density lipoprotein (HDL) cholesterol in laying quails. However, Lim et al. (Reference LIM, YOU, AN and KANG2006) did not find any difference in HDL-cholesterol concentration by feeding garlic (1, 3 and 5%). Qureshi et al. (Reference QURESHI, DIN, ABUIRMEILEH, BURGER, AHMAD and ELSON1983b) reported a 28-41% reduction in low density lipoprotein (LDL) cholesterol in an experimental diet containing 3.8% garlic paste or a solvent extract of garlic paste, the residue or commercial garlic oil fed for four weeks. Recently, Mansoub (Reference MANSOUB2011) reported reductions in total cholesterol, LDL-cholesterol and triglycerides when broilers were supplemented with 1g/kg garlic. Prasad et al. (Reference PRASAD, ROSE, VIRMANI, GARG and PURI2009) observed that total cholesterol, triglycerides, LDL and very low density lipoprotein (VLDL) were significantly decreased, while HDL was significantly increased by garlic supplementation in chicken up to eight weeks of age in comparison to control group. Rahimi et al. (Reference RAHIMI, ZADEH, KARIMI, OMIDBAIGI and ROKNI2011) noted that supplementation of 0.1% garlic decreased cholesterol, triglyceride and LDL cholesterol but increased HDL level. Recently, Rehman et al. (Reference REHMAN, DURRANI, CHAND, KHAN and REHMAN2011) documented that a mixture of plants containing garlic as an active ingredient improved the cholesterol profile in terms of cholesterol, triglyceride, LDL cholesterol, VLDL cholesterol, total cholesterol to HDL ratio, LDL to HDL ratio, total cholesterol to VLDL ratio, VLDL to HDL ratio in broiler chicken serum. Konjufca et al. (Reference KONJUFCA, PESTI and BAKALLI1997) conducted an experiment on male Ross 208 which were fed a basal diet supplemented with 1.5, 3.0 or 4.5% commercial garlic powder from hatching to 21 days of age, and found that garlic powder resulted in reduced level of plasma cholesterol, liver cholesterol, breast and thigh muscle cholesterol.
The mechanism by which garlic reduces plasma cholesterol concentration is not fully understood. Some of the investigators are of the opinion that garlic depresses lipogenic and cholesterogenic activities of liver enzymes such as malic enzyme, fatty acid synthase, glucose-6-phosphate dehydrogenase and 3-hydroxy-3-methyl-glutaryl-CoA(HMG-CoA) reductase (Qureshi et al., Reference QURESHI, ABUIRMEILEH, DIN, ELSON and BURGER1983a; Reference QURESHI, DIN, ABUIRMEILEH, BURGER, AHMAD and ELSON1983b; Youn et al., Reference YOUN, NAM, KIM, KANG, OHTANI and TANAKA1996; Chowdhury et al., Reference CHOWDHURY, CHOWDHURY and SMITH2002; Canogullari et al., Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010; Mahmoud et al., Reference MAHMOUD, SAAD, GHARAIBEH, ZAKARIA and AMER2010). This hypothesis was demonstrated when several researchers measured cholesterol-clearing enzymes. For example, Qureshi et al. (Reference QURESHI, ABUIRMEILEH, DIN, ELSON and BURGER1983a) reported a dose-dependent inhibition of hepatic HMG-CoA reductase, cholesterol 7α-hydroxylase and fatty acid synthetase in chickens fed polar fractions of garlic powder equivalent to 1, 2, 4, 6 and 8% of fresh garlic paste. Konjufca et al. (Reference KONJUFCA, PESTI and BAKALLI1997) reported that feeding 3% commercial garlic powder reduced the activities of HMG-CoA reductase and cholesterol 7α-hydroxylase by 40%. Allicin has been proposed as the active compound in garlic responsible for health promotion and hypocholesterolaemic benefits (Lawson, Reference LAWSON1998). In terms of the mechanism of action, it is believed to reduce cholesterol synthesis, inhibit fatty acid synthesis and platelet aggregation and prevent thrombosis (Canogullari et al., Reference CANOGULLARI, BAYLAN, ERDOGAN, DUZGUNER and KUCUKGUL2010). Allicin is a volatile organic compound which has been shown to reduce serum lipids, phospholipids and total cholesterol and suppress cholesterol synthesis in chickens (Horton et al., Reference HORTON, FENNELL and PRASAD1991). According to Mahmoud et al. (Reference MAHMOUD, SAAD, GHARAIBEH, ZAKARIA and AMER2010) the difference in the results may be due to allicin degradation, as it is an unstable compound and poorly absorbed from the gut. Additionally, they suggested that the garlic preparation that involved heating or solvent processes may destroy active allicin.
Conclusions
The current archive of literature suggests that garlic may be a useful alternative to antibiotics in poultry production due to its wide range safety margin. However, little work has been done on its mechanism of action in poultry productivity. Therefore, further research is suggested to clarify its mode of action as well as the exact dose and duration for a more efficacious outcome.
