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Early Nutrition Programming (in ovo and Post-hatch Feeding) as a Strategy to Modulate Gut Health of Poultry

Published: August 24, 2020
By: Rajesh Jha 1, Amit Kumar Singh 1, Sudhir Yadav 1, Julio Francisco Diaz Berrocoso 2 and Birendra Mishra 1. / 1 Department of Human Nutrition, Food and Animal Sciences, University of Hawaii at Manoa, Honolulu, HI, United States; 2 Trouw Nutrition, Poultry Research Centre, Toledo, Spain.
Summary

Healthy gastrointestinal tract (GIT) is crucial for optimum performance, better feed efficiency, and overall health of poultry. In the past, antibiotic growth promoters (AGP) were commonly used to modulate the gut health of animals. However, considering the public health concern, the use of AGP in animal feeding is banned or regulated in several jurisdictions around the world. This necessitates the need for alternative nutritional strategies to produce healthy poultry. For that, several alternatives to AGP have been attempted with some success. However, effective modulation of the gut health parameters depends on the methods and timing of the compound being available to host animals. Routinely, the alternatives to AGP and other nutrients are provided in feed or water to poultry. However, the GIT of the newly hatched poultry is functionally immature, despite going through significant morphological, cellular, and molecular changes toward the end of incubation. Thus, early growth and development of GIT are of critical importance to enhance nutrients utilization and optimize the growth of poultry. Early nutrition programming using both in ovo and post-hatch feeding has been used as a means to modulate the early growth and development of GIT and found to be an effective strategy but with inconsistent results. This review summarizes the information on in ovo and post-hatch-feeding of different nutrients and feeds additives and their effects on gut development, histomorphology, microbiology, and immunology. Furthermore, this review will provide insight on the future of early nutrition programming as a strategy to enhance gut health, thereby improving overall health and production so that the poultry industry can benefit from this technique.

Keywords: broilers, gut health, histomorphology, immune system, in ovo feeding, post-hatch, nutritional strategy, poultry.

INTRODUCTION
Poultry production has increased at a faster rate than any other livestock animal globally. Among others, the nutritionally balanced-feeding program along with antibiotic growth promoters (AGP) in poultry diets played a significant role in achieving this success. However, the poultry industry is under pressure to redefine its nutrition program to grow safe and quality meat in the light of public health concern due to the use of AGP in poultry diets. Maintenance or improvement of gut health is essential for optimum growth, better feed efficiency, and overall health of poultry (1). Also, a healthy gut is critically important for the efficient conversion of feed into absorbable form for optimal nutrient utilization, thereby better growth performance of poultry.
Gut health covers the efficient nutrient utilization, macro-and micro-structural integrity of the gut, the stability of the microbiota, and the status of the immune system (2, 3). Moreover, gut health is a complex field combining nutrition, microbiology, immunology, and physiology of animals. When gut health is compromised, digestion, and nutrient absorption are affected (3), which in turn, may have a detrimental effect on feed efficiency and greater susceptibility to diseases leading to economic loss. In addition, recent regulatory changes on the use of antibiotics, different feed requirements, and more feed-efficient animals highlight the need for a better understanding of the gut function and overall gut health. Therefore, understanding and improving gut health by different nutritional strategies are becoming a reality in the monogastric animal industries, especially when antibiotics are not allowed in food-animals feeding program (3–5).
Chicks have been shown to benefit from early access to feed and water. A healthy 1-day-old chick is a crucial link between the hatchery and the broiler farm. The delayed intake of water and nutrients to chicks could lead to a diminishing of their overall growth performance with adverse effects on breast meat. The most extreme consequence of delayed feeding is increased mortality (6). Early feeding strategies have been suggested and developed to diminish or possibly reverse the negative effects of delayed feeding. These strategies range from in ovo feeding to specially designed post-hatch diets (7–9). The importance of early nutrition and its effect on growth performance and different components of gut health (histomorphology, microbiota, and immune system) have already been extensively studied in the last two decades (10–15). Some studies have gone in detail about specific nutrient supplementation and its effect on the host. For example, probiotics supplementation in early life prevent pathogenic infections, amino acids (L-arginine, L-lysine, L-histidine, threonine) are beneficial in growth performance, vitamin C and E boost immunity, carbohydrates increase glycogen stores, and creatine supplement promotes muscle growth (16). Also, the in ovo injection of sulfur-containing amino acids (methionine plus cysteine) in the embryonated eggs exposed to heat stress have positive effects on gene expression and antioxidant indices as well as reduce the lipid profile of newly hatched broiler chicks (17). This paper has reviewed the current state of knowledge on in ovo and post-hatch-feeding as a strategy to enhance the gut health of poultry. It emphasizes on the effects of different nutrients on intestinal histomorphology, microbiota, and immune system using in ovo or post-hatch feeding system. The paper further provides the potential application of the current knowledge for the advancement of the poultry industry. Also, it has highlighted current limitations and future potential and research needs for effective use of early feeding in birds.
 
IMPORTANCE OF EARLY FEEDING
The perinatal period spanning from late-term embryo to few days post-hatch is an important period for the development of the gastrointestinal tract (GIT) and the immune system of poultry. Unlike mammals that can influence the development of fetus even after parturition, avian species can leverage expression only through the composition of the egg. Due to this restriction, all necessary nutrients, growth factors, and the machinery needed for the development are required to be present in the fertilized egg. Also, because of a rapidly growing embryo and the fast-metabolic turnover of modern chicks, some of the essential nutrients can become depleted or insufficient during adverse environment and disease challenges. This constraint of nutrient reserves may limit the maximal development and growth of newly hatched chicks. The availability of essential nutrients can be improved, and the existing challenges can be overcome to some extent by providing early nutrition to the embryos and chicks. Early nutrition or feeding in poultry production is a concept of providing the required nutrients to the birds either during the period when the embryo is developing or immediately after hatch until they attain a fully matured digestive system (8).
A prominent early nutrition technique that could provide further opportunity to influence the development of a chick inside the egg and overcome the constraints of nutrient limitation during late incubation phase is in ovo feeding (IOF). This technique provides the opportunity to supply essential nutrients, neutraceuticals, and functional foods to uplift the status of growth and development of the embryo. Several routes including amniotic (8, 18), yolk sac (19, 20), and air sac (13, 21) have been used. Amniotic fluid in the amnion surrounds the developing embryo and is believed to provide mechanical protection, prevent desiccation, and adhesion of the embryo (22). The amniotic fluid also contains protein, minerals, hormones, water, and other nutrients needed for growth and development of the developing chicks which begin to imbibe it around d 13 of incubation until internal pipping (23). This natural phenomenon of consumption of amniotic fluid by the late-term embryo toward hatch provides opportunities to add various forms of essential nutrients that would ultimately reach the GIT of chicks. Nutritional substances injected into the amniotic cavity are ingested and get deposited in the lungs and intestine due to the rhythmic respiratory movements of the late-term embryo (18, 24). In ovo feeding can also be used to provide adequate nutrients to the late-term embryo to protect it from the negative effect of starvation during the extended window of hatching (25). Afsarian et al. (26) found that in ovo injection of thyroxine along with manipulation of the eggshell temperature decreased the mortality rate occurring due to cold-induced ascites and improved chick quality and post-hatch performance. Recently, Yang et al. (27) observed that IOF of creatine pyruvate increased glucose concentration in thigh muscles of neonatal broilers, which suggests that the energy metabolism can also be altered in embryo and chicks by in ovo injection of different bioactive compounds. Moreover, in ovo application of prebiotics can be advantageous as it has been reported to increase the numbers of beneficial bacteria and promote their early colonization in the intestine of neonatal chicks (28). Likewise, investigators are interested in inoculating eggs with probiotics and synbiotics as they can be used in small amount and provide improved immunity and a better post-hatch resistance against pathogens (29, 30).
Perinatal period is also very critical as the chicks must adjust to the nature of the changing nutrition mostly from yolk-based lipid diet to carbohydrate-based solid feed. It has been observed that chicks are more efficient in utilizing lipid following hatch and gradually gain the capacity to absorb more hexoses and amino acids (31, 32). The transition of a chick from nutrient utilization from embryonic reserves to feed forces for adjustment of the newly developed digestive system. Early post-hatch feeding is essential not only for normal growth and development but also for maintaining homeostasis. Early feeding of chicks can provide readily available energy to assist in restoring hepatic glycogen stores and maintain high body temperature during initial post-embryonic days (33). In contrast, higher inclusion of anti-nutrient like non-starch polysaccharides during the early growth period can deteriorate the feed efficiency and overall productivity of growing chickens (34). Due to the practical perspective of feeding program and due to limited information on the early nutritional requirement, poultry hatchlings (e.g., chicks, ducklings, and turkey poults) are fed starter diet after hatching till 2–4weeks (34–36). Several investigators have reported that chicken weight at 6–7 weeks had the linear relationship with their weight in the first week (37) and it was not due to the breeder age and day-old chicken weight (38). The pre-starter feed could be more expensive than starter feed, but such feeding last only for a shorter period of 3–4 days and has more favorable effect on the performance of birds (39). Broiler feeding in the first few days of life is one of the priorities that could affect growth, feed efficiency, uniformity, and finally the profit of farmers. Nutrient utilization in chicks at an early stage is dependent on digestion and absorption of nutrients in the GIT (40). Improved performance has been observed in broilers by feeding pre-starter containing carbohydrate and fat during the first hours of chicken life (39, 41). Some pre-starter diets are prepared with more focus on digestible nutrients than the total requirements, and it can precondition the chick to later digest complex substrates once they acquire matured enzyme production in the GIT (7, 42). Since highly digestible alternative substrates tend to be expensive, the use of different enzymes combination or the higher activity of enzymes than those applied in later phases of diet could improve the productive performance of birds. However, limited work has been conducted to date to estimate the nutrients requirement of first week chicks that could outperform in terms of market weight and disease resistance compared with those fed starter diet (43, 44).
The GIT, especially the small intestine of poultry has the highest post-hatch relative growth during the first week growing period (45, 46). Therefore, an early feed deprivation can lead to a decreased intestinal enterocyte length and villus surface area which negatively affects nutrient utilization and growth (47). Early feeding is expected to influence immune development either by providing nutrients for cell proliferation and differentiation or by providing substrates for antigenic and immunomodulator activity leading to the production of several immunoglobulins (48–50). It is understood that early access to nutrients is essential for a sound immunity and improved health of chicks and poults (51). By managing a proper nutritional strategy, a specific stimulus can be generated to guide this immune system toward a more appropriate and desired direction. The requirement of enhanced immunocompetence becomes exceptionally important in the view of reducing the dependence on antibiotic growth promoters (AGPs). One of the suitable alternatives to feeding AGPs can be a supplemental chicken cytokine (52). Also, early access to feed supplemented with mannanoligosaccharides and acidifier have been reported to improve the development of intestinal morphology and immune response of chickens to C. perfringens challenge compared to early feed restricted chicks (10). Recently, in a study on nursery pigs, Tiwari et al. (53) reported that the use of NSP degrading enzymes modulated the production of tight junction proteins that maintain the intestinal barrier function and hence can prevent the permeability of the gut to invading pathogens. However, Mateos et al. (54) reviewed literatures on the effect of early feed access or restriction and dietary changes in the prestarter diet and concluded that the difference in the productivity tends to disappear with increasing age of birds. Still, there is a scarcity of information on early nutritional modification and most of the studies until now have focused on early access of chicks to feed. Further research is warranted to determine if early prestarter diet would be worthy of optimizing metabolic homeostasis in poultry for prospective maximal growth and feed efficiency.
 
NUTRITION AND GUT HEALTH IN POULTRY
The term “gut health” is a very comprehensive topic that requires a holistic tactic involving nutrition, gut physiology, microbiology, and immunology. Nutrition and health are interdependent, and the interface between the two occurs largely in the gut. One of the most effective ways to influence poultry gut health is through nutrition programming. In fact, the early nutrition programing by the introduction of feed and water to the chick provides a good means to feed the gut. By doing this gut, development is most favorable. This will ensure the birds are better equipped to cope with the gut challenge. There are several nutritional strategies that can be adopted to influence gut health. In this section of the review, some prominent factors affecting intestinal health are briefly presented.
Diet Formulation
A balanced diet formulation to match nutrient content of feed with the nutrient requirements of the birds is considered as one of the most important aspects of the animal feeding program. In this respect, poultry diets should be formulated based on digestible values instead of “total” values in order to maximize protein digestibility. The ‘Balanced Protein’ (or ideal amino acid profile) concept for all the essential amino acids should be applied. The emphasis is not on minimum crude protein but rather on the proper balance or ratio of each amino acid to lysine. The use of synthetic amino acids will be beneficial and can help to prevent excess crude protein. An excess of indigestible protein in the hindgut can predispose to several intestinal challenges (e.g., wet litter).
Starch Properties
Among the nutrients in poultry diets, starch is the most important nutrients and main source of energy in the broiler’s diets (may contain up to 50% starch on a DM basis). Different cereal grains (wheat, corn, sorghum, rice) have different starch characteristics and physico-chemical properties. For example, wheat contains high levels of non-starch polysaccharides (NSP) such as β-glucans and arabinoxylans (55). The physico-chemical properties of NSP are responsible for their antinutritive activities in the broiler chicken, especially soluble viscous NSPs, which decreased the digestibility of protein, starch, and fat. In addition, high viscosity of the digesta has been shown to cause digestive and health problems, decreasing digeta passage rate, digestive enzymatic activities and nutrient digestibility, depressed feed efficiency, and growth rate of the birds (56) in diets based on barley, wheat, rye, or oats (high levels of NSP). On the other hand, insoluble and non-viscous NSPs may have a beneficial effect on gut health (57). Other NSP properties, such as resistance to the animal’s digestive enzymes also promote to create a viscous environment within the intestinal lumen, resulting in excretion of sticky droppings (58). In addition, the rate of starch digestion can favor the growth of Clostridium perfringens. Toxins produced by Cl. perfringens are responsible for necrotic enteritis (10). Therefore, the application of appropriate xylanase enzymes is necessary to enhance digestion of starch and gut health because they have the ability to break down NSP and reduce digesta viscosity, increase digesta passage rate, and improve bird performance (59–61)
Physical Texture and Form of Feed
The physical form of the raw materials used in broilers diets may affect the morphological and physiological characteristics of the entire intestinal tract (62, 63), although available published works in this area of research are inconsistent. Small grain particles give a larger surface area, and this may give rise to rapid feed passage in the gut. However, many studies (64– 66) have demonstrated that larger particles promote gizzard development and activity, and, consequently, feed is retained longer in the gizzard, and its particles are more uniform when pass to the small intestine, favoring their digestion. In addition, larger particle size of feed lead to longer feed retention time in the gut; this helps to release the starch entrapped in cereal grain cells and encourage more beneficial bacterial fermentation in the caeca. Therefore, the target for particle size should be 800–1000 microns. In this respect, feeding broiler chicken with whole wheat could reduce the numbers of Salmonella typhimurium and Cl. perfringens in the GIT of the birds (63, 67). In addition, the inclusion of whole wheat into the broiler diets increased growth rate and feed efficiency of the birds (68). In contrast, Svihus et al. (69) did not find significant effects of diets containing whole wheat on body weight gain and feed efficiency. However, the authors reported that the birds fed with whole-wheat diets were more efficient and the nutrients were better digested and absorbed than the birds fed with ground wheat diets. The authors suggested that the improvements in the digestion might result from the increased pancreas and liver secretions. Svihus et al. (70) compared the inclusion of ground or whole wheat on on passage rate through the anterior GIT, and reported that although the gizzard has high capacity for processing diets with whole wheat, the average passage rate for a diet through the gizzard does not seem to be affected by the form of the wheat. Based on these results, it can be concluded that when the GIT is healthy, the inclusion of whole wheat into the diet may help to improve gut development and utilization of feed nutrients and consequently broilers performance, but when the integrity of the GIT is impaired, the inclusion of whole wheat into the diet may decrease the performance of the birds. Also, the inclusion of whole wheat in diet will reduce the energy consumption for grinding and the final feed cost of the diets.
On the other hand, use of a hammer mill to grind grains is still acceptable for the production of broiler feeds, but it may be best used with a 6-mm sieve size and a rotation speed of 750 rpm (71). A roller mill will give a more even distribution of particle size and hence better overall uniformity. In addition, a roller mill tends to produce a sharp-edged particle with less dust while a hammer mill produces a more rounded particle, which results in considerably more dust and more durable pellets. The sharper edged particles produced by roller mills may provide physical stimulation of the gut lining and therefore lead to better gut health (72).
 
EFFECTS OF EARLY NUTRITION ON HISTOMORPHOLOGY
The GIT tissue acts as a physical and immunological barrier to the harmful chemicals and infectious agents that enter the host. It also provides a path to the nutrients for proper digestion and absorption (5). Yegani and Korver (5) also found that healthy gut morphology directly affects the metabolism of nutrients, disease resistance, and immune response by the host. Diet intake exposes the GIT to the external environment whose quality, quantity and timing largely affect the delicate balance between the host, diet and gut ecology. So, feed ingredient used in the diet should be favorable to host gut structure and commensal microbiota (1). In the adverse gut environment, birds are at high risk of developing necrotic enteritis, coccidiosis, and other toxin-producing pathogens. Gut histomorphology is one of the most commonly used parameters to diagnose the status of gut health.
The effects of early nutrition on histomorphology have been studied in the last decade (13, 15, 73). It is well-documented that the first days after hatch is a critical period for the development of the mucosa because of major change occurring in the source of nutrients as the yolk is replaced by an exogenous diet. The growth of the chickens is directly linked to the digestion and absorption of nutrients, which is a result of the morphological and functional development of the small intestine. Villus height, crypt depth, and villus height/crypt depth ratio, crypt proliferation, rate of enterocyte migration, mucosal enzyme activity and goblet cell development are good indicators for the functional capacity of the intestine (74). It is well-accepted that a deeper crypt is indicative of faster tissue turnover and, perhaps, higher demand for new tissue (53, 75). Furthermore, it has been reported that a high intestinal villus is associated with a well-differentiated intestinal mucosa with high digestive and absorptive capabilities (75). A meta-analysis study done for the effect of post-hatch feed and water deprivation (PHFWD) shows significant subnormality in the small intestine segment with reduced length and relative weight of duodenum, jejunum, and ileum, and shorter villus height and crypt depth during the first week of age (74). Therefore, in ovo and post-hatch feeding strategies should be taken into account as a strategy to modulate the gut health of poultry.
Early nutrition is a stimulus to the early development of GIT, early absorption of the yolk sac, improved performance and the health status of the birds later in life. In the case of PHFWD, chicks have significantly lower yolk sac weight at 3 days post-hatch than on the day of hatch (74, 76). reported that in ovo feeding on 17–18 day of incubation is functionally equivalent to 2-day-old bird intestine with the increased size of villi and increased capacity to digest and absorb disaccharides leading to greater body weight compared to control birds fed in conventionally. However, in the commercial setup newly hatched chicks do not get access to feed and water for at least 12–36 h due to the inevitable operation of the hatchery, sex determination, vaccination, and transportation to the production farms. There are many reports on the negative effects of post-hatch fasting period on the intestine function and growth performance in the long run (77, 78). Fasting could further increase the susceptibility to infection and compromise immunity leading to an increase in the production cost of chickens (33). In the post-hatch period, there is the rapid development of intestinal length, weight, and its enzymatical activities, where delay in feeding causes a reduction in development and expression of nutrient transporters affecting absorption of nutrients (5). Apajalahti et al. (79) relate dietary factors and their interaction with a microbial profile to find out the effects on the intestinal development, mucosal architecture, and the mucus composition of the GIT. Pre- or post-hatch intestine morphological development is also very critical to digest, assimilate and absorb nutrients from the gut. Researches by Biloni et al. (80) and Adeleye et al. (77) found that fasting (feed and water) birds for 24 h negatively affects the morphology of the gut with a decrease in duodenal and jejunal villus height compared to birds fed 4-h post-hatch.
Feeding a blend of perinatal supplement and probiotic supplement shows increased villus height, villus width, villus to crypt ratio, and villus surface area along with an increase in overall body weight supported by competitive exclusion of Salmonella (80). In ovo injection of prebiotic inulin has shown to increase the villus height on the first day and it is also known to increase mucin production to protect epithelial cells in the gut (81). Another research by Madej and Bednarczyk (82) found that in ovo inulin injection helps proliferate lymphoid tissue by T cells but no any effect on gut-associated lymphoid tissue. Berrocoso et al. (13) found some interesting results showing in ovo injection of 4.5 mg raffinose significantly affected the CD3 and ChB6 genes which are associated with the activity of T cell and B cell. The authors also found a linear increase in villus height and villus to crypt ratio of post-hatch birds with the increase in dose of raffinose. In ovo injection prebiotic galacto-oligosaccharides increased the overall body weight of broilers on 5th week due to its activity on sodium-dependent glucose co-transporters in the gut helps in monosaccharides absorption (83). The authors also found an increase in pancreatic secretion of trypsin and amylase on embryonic day 21 and day 7 post-hatch. In ovo injection of synbiotic preparation increases the number of goblet cells in the jejunum and ileum (84). These goblet cells produce mucus and protect the gut epithelium. The author also found an increase in width of the duodenal villi and crypt depth of 21-day old chickens fed Laminaria spp. as in ovo preparation. In conclusion, we can claim that early dietary intervention impact on all aspect of gut health such as gut microbial ecology, gut epithelium and immune system leading to benefit the overall growth performance of the chickens.
 
EFFECTS OF EARLY NUTRITION ON GUT MICROBIAL ECOLOGY
The confounding performance of modern chicken to gain body weight by 25% in a day by newly hatched chick and 5,000% by 5 weeks to 2 kg makes it more demanding to meet the nutrient requirement along with the enhancement of the microbial function to improve immunity, digestive and absorptive function to overall improvement of the bird growth (2). The established protective intestinal microbiota is very stable, but it can be influenced by different dietary, disease, and environmental factors. For example, feed additives (antibiotics, coccidiostats, buffers, or acidifiers that influence gut pH), disease and hygiene conditions (clean vs. dirty environment, pathogen load in the feed ingredients, humidity of the shed, litter type, and usage), and stress (change of feed, sudden disturbances, heat, or water stress) could also affect gut microflora. However, diet is perhaps the most critical factor influencing the gut microflora (1, 85). Young animals are more affected by dietary manipulations such as its composition, processing, digestibility, and feeding method may disturb the balance in the gut ecosystem, especially in young animals (79, 86–89). For example, corn and sorghum-based diet increased Enterococcus, barley-based diet increased Lactobacillus, oat increased Escherichia and Lactococcus, and rye-based diet increased the Streptococcus (90). Researches have shown that the gut immunity changes with the changes in the gut microbial activity. Newly hatched chickens are very prone to colonize their gut by pathogenic bacteria as they provide near-sterile and suitable environment and continues to establish a relatively stable ecology with the animal age. Here interaction between microbiota and the host plays a deciding role to determine the future ecology and stability of such microbiota in the gut. Pourabedin and Zhao (91) explained this shift of Clostridiaeae and Enterobacteriaceae as dominant ileum microbiota families on day 7 to Lactobacillaceae and Clostridiacea on day 35. Apajalahti et al. (92) showed that bacterial densities one-day post-hatch in the ileum and cecum of the broiler reaches 108 and 1010 cells per gram of digesta, respectively, and attends optimum levels of 109 and 10 11 per gram of ileal and cecal digesta, respectively, by 3 day post-hatch. This bacterial density remains stable for further 30 days or so in broiler chicken. Supplementing prebiotics in the diet at an early stage of life increases the abundance of Lactobacilli and Bifidobacterial and suppress coliform (93). Whereas, a study by Villaluenga et al. (94) found that in ovo administration of symbiotic on day 12 or 17 of incubation, increased the number of bifidobacteria in the post-hatch period. Another study by De Oliveira et al. (29) injecting in ovo probiotic preparation of Enterococcus faecium bacteria reduced the number of Salmonella enteritidis positive chicks post-hatch. This indicates that in ovo colonization of probiotics is potential enough to post hatch bacterial infection. In general, prebiotics stimulates the microbiome when administered in ovo at the early age of around 12 days and later probiotic at 17/18 days of incubation causes competitive exclusion. Thus, early beneficial microbiota colonization is very critical for the proper growth of chickens (80). Many hi-tech molecular techniques are used to study the gut microbiota; high-throughput sequencing is the most common one, along with targeted amplicon sequencing followed by shotgun sequencing, metaproteomics. These techniques have some limitations regarding characterizing the functional activity of gut microbiota, thus the holistic approach using multiomics might help to better understand these gut microbiota (85).
 
EFFECTS OF EARLY NUTRITION ON THE IMMUNE SYSTEM
Since there is a very short time for the chicks to grow to a marketable age, it becomes essential to adopt a sound management practice that would not only ensure a general well-being of birds but would also assist them to maintain a healthy gut microbiome, strong immunity and improved gut health. Several nutrients are important in the early development of the immune system. Vitamin A is necessary to maximize immuno-competence and for the optimum growth and feed efficiency of poultry (95, 96). Other nutrients which can affect early immune development are linoleic acid, iron, selenium, and some of the B vitamins (97). Much development of immune tissues in poultry occurs at late incubation and early post-hatch period. Thus, maternal nutritional status and deposition of nutrients as well as early nutrition play an important role in the modulation of the nutritional immune system. It has been known that vitamins A, D, and E have regulatory roles in the immune system (98). The complexity of the immune response requires various modes of communication of immune cells and immune-molecules. It has been found that the poultry is most susceptible to the invading pathogens during early hatch period as their immune system does not attain the full functionality by this age.
Nutritional modulation by providing micronutrients and required substrates through both in ovo and in feed during first-week post-hatch can support the proliferation of lymphoid organs and modify the population of the microbiome in GIT (97). This can ultimately result in improved immunity and enhanced integrity of the intestinal epithelium of growing birds.
The intestinal mucosa is exposed to a variety of non-self external materials including pathogenic microbes and its gut-associated lymphoid tissue (GALT) plays a significant role in the avian immune system (99). Hence, it is critical that delay in feeding is avoided as it can delay the onset of GALT function (11). In ovo injection of nutrients can play a vital role where delay in feeding is expected due to various limitation arising due to shipping and distribution of the day-old chicks.
In ovo manipulation of the embryo is not only a method of filling up the reserves with nutrients but it is also a tool that allows injecting other substances that can stimulate the immune system, modify the gut microbiome, and shift the level of production of metabolites. Dibner et al. (51) proposed the effect of early oral nutrition on the development of the immune system in hatchlings broiler chicks. According to the authors, early nutrition can provide the limiting substrates, affect endogenous levels of hormones or immunomodulators, and the presence of antigen in GIT can trigger the complete differentiation of immune cells like B-lymphocytes. Recently, the focus has been intensified on nutritional manipulation of growing embryo for improvement in immunity and health of birds during later growth periods. The improvement in the immune status of poultry by use of vitamins, amino acids, and prebiotics through in ovo feeding has been encouraging (13, 100, 101). Similar to the late in ovo feeding, Kadam et al. (102) injected amino acid threonine into the yolk sac of 14 d old embryo and found that it improved the humoral response of the broiler chicks. Bakyaraj et al. (103) reported that in ovo injection of amino acids, trace elements, and fatty acids and vitamins into the amniotic cavity of late-term embryo improved the cell-mediated immunity in chicks. A research conducted by Selvaraj and Cherian (104) using in ovo injection of fatty acids into amniotic cavity revealed that injection of linoleic acid (ω-6 fatty acid) increased cell-mediated immunity while the injection of ω-3 fatty acids of marine origin induced a humoral response. Likewise, glucose triggered humoral immunity while fructose and ribose modulated cellular immunity in broilers receiving in ovo injection in yolk sac/amnion on d 14 of incubation (105). It has also been found that in ovo feeding of amino acids can enhance the growth-related genes and modulate the expression of immune genes in broilers (106). Early improvement in the status of immunity in broilers is also dependent on the general health status and nutritional state of the bird. Some substrates like mannanoligosaccharides have the potential to exert a direct effect on the maturation of enterocytes, enhancement of digestive capacity and improvement of epithelial barrier function when fed in ovo (107). Also, early feeding of lectin extract into the amniotic cavity of chicken in a study by Dalloul et al. (108), produced resistance against orally challenged coccidiosis. This protection of chicken against coccidiosis infection is a clear indication of immunopotentiating effect of nutritional programming. The nitric oxide (NO) is produced by cells involved directly or indirectly in immune response and has a key role in immune regulation and neurotransmission. Besides its role as a signal molecule, NO can also act as a non-specific component of the immune system by destroying the invading pathogens, tumor cells, and parasites. In ovo feeding of arginine to late-term embryo has been documented to increase secretory immunoglobulin A (sIgA) in the intestinal mucosa and activate Arg-NO signaling pathway in broilers (109). The increase in the level of NO and sIgA indicates that in ovo feeding of arginine can enhance the immunological barrier function of intestinal mucosa and improve the overall immunity and intestinal health of birds.
The application of some additives as a nutritional approach to tackle deficiencies during the early feeding period also have some prospect in reinforcing the immunity of growing poults. Feeding of β-glucan can strengthen the innate immunity by up-regulating the oxidative burst, phagocytosis and bactericidal killing capacity of heterophils and decrease the incidence of organ invasion by Salmonella enteritica in neonatal chickens (110). Early feeding of the amino acid is essential as their oxidation rate increases during inflammation, and a regular diet may not accommodate the requirement of growing and challenged birds. It is known that glutamine provides energy and nitrogen source for the proliferation of immune and intestinal mucosal cells and is required along with cysteine for the synthesis of antioxidants like glutathione (111, 112). However, it is suggested that breeding poultry for higher immunocompetence would have some negative impact on some production performances that is not desirable in modern poultry production due to the short time of feed to meat or egg turnover (113). Hence, further works are required to be conducted to ascertain the effect of early nutritional programming vs. delayed intervention for tackling challenges originating due to metabolic and infectious diseases in poultry production.
 
FUTURE POTENTIAL AND LIMITATIONS OF EARLY NUTRITION PROGRAMING
The continuous development and improvement of in ovo technology have established a new scope for perinatal nutrition, allowing and creating new challenges and opportunities for nutritionists to optimize poultry production. The in ovo injection of important nutrients or substances into the amnion is a novel way to feed critical dietary components to embryos. Indeed, in ovo feeding may “jump-start” development, improving the nutritional status of the perinatal chick. The in ovo feeding technique has several advantages, including improvements of total digestive tract capacity; increased body weight, growth rate, and feed efficiency; reduction of post-hatch mortality and morbidity; improvements in the immune system and the response to enteric antigens; reduction in incidence of developmental skeletal disorders; and increase in muscle development and breast meat yield. The next step in the early nutrition could be to imprint genes of a bird at a very early age and turn it into a more efficient animal later. In addition, the administration of digestible nutrients into the amnion of embryos can bring an improvement in bird quality, increased glycogen reserves, fast development of the total digestive tract superior skeletal health, better muscle growth rate, higher body weight gain, improved feed conversion, and enhanced immune function (16). Using nutrigenomic data, almost 30 percent of genes expressed different activity over time by in ovo feeding.
The main limitations still are associated with embryo development and nutrient metabolism. Another question is a limitation in the probiotic preparation that fits the specific needs of the individual bird. Future early nutrition would be feeding complex symbiotic that would replace feed additives and supplements in the post-hatch feed and is more beneficial to the overall poultry industry.
 
CONCLUSION
With the increase in productivity and highly feed efficient birds, the nutritional demand of embryos and early aged chicks has changed over decades. Early nutrition programming is one of the latest and successful methods to feed embryos and recently hatched chicks to prepare chickens with the healthy gut, favorable microbiota, improved immunity, and overall improved growth performance. Currently used materials to feed as early nutrition includes probiotics, prebiotics, exogenous enzymes, amino acids, hormones, vaccines, and drugs. Early feeding to chicks with these nutrients and supplements has been found to improve total digestive tract development, increase growth rate and feed effiiency, reduce post-hatch mortality and morbidity, promote growth of beneficial gut microbiota, improve the immune system and the response to enteric antigens, reduce incidence of developmental skeletal disorders, and increase in muscle development and breast meat yield. Further works are required to fine-tune the in ovo feeding technique for application at commercial scale in farm condition, understand the embryonic development and nutrient metabolism process more precisely, and understand how early nutrition affects specific genes responsible for performance, intestinal health, and overall health-related traits in poultry.
 
AUTHOR CONTRIBUTIONS
AS, SY, and JB wrote this review manuscript. BM reviewed the manuscript and provided critical suggestions and comments. RJ decided a review topic, reviewed the literature and this review manuscript and provided critical review, suggestions, and comments.
 
This article was originally published in Frontiers in Veterinary Science. 6:82. doi: 10.3389/fvets.2019.00082. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (CC BY).

  1. Yadav S, Jha R. Strategies to modulate the intestinal microbiota and their e?ects on nutrient utilization, performance, and health of poultry. J Anim SciBiotechnol. (2019) 10:2. doi: 10.1186/s40104-018-0310-9
  2. Choct M. Managing gut health through nutrition. Br Poult Sci. (2009) 50:9–15. doi: 10.1080/00071660802538632
  3. Jha R, Berrocoso JD. Review: dietary fiber utilization and its e?ects on physiological functions and gut health of swine. Anim. (2015) 9:1441–52. doi: 10.1017/S1751731115000919
  4. Haygood AM, Jha R. Strategies to modulate the intestinal microbiota of Tilapia (Oreochromis sp.) in aquaculture: a review. Rev Aquacult. (2018) 10:320–333. doi: 10.1111/raq.12162
  5. Yegani M, Korver DR. Factors a?ecting intestinal health in poultry. Poult Sci. (2008) 87:2052–63. doi: 10.3382/ps.2008-00091
  6. Willemsen H, Debonne M, Swennen Q, Everaert N, Careghi C, Han H, et al. Delay in feed access and spread of hatch: importance of early nutrition. Worlds Poult Sci, J. Vol. 66:177–188. doi: 10.1017/S0043933910000243
  7. Leeson S. Predictions for commercial poultry nutrition. J Appl Poult Res. (2008) 17:315–22. doi: 10.3382/japr.2007-00101
  8. Uni Z, Ferket PR. Enhancement of Development of Oviparous Species by in ovoFeeding. U.S. Patent 6,592,878. Yissum Research Development Co. of Hebrew University and North Carolina State University Raleigh, N. C. (2003).
  9. Uni Z, Ferket RP. Methods for early nutrition and their potential. WorldsPoult Sci J. (2004) 60:101–11. doi: 10.1079/WPS20038
  10. Ao Z, Kocher A, Choct M. E?ects of dietary additives and early feeding on performance, gut development and immune status of broiler chickens challenged with Clostridium perfringens. Asian Austr J Anim Sci. (2012) 25:541–51. doi: 10.5713/ajas.2011.11378
  11. Bar Shira E, Sklan D, Friedman A. Impaired immune responses in broiler hatchling hindgut following delayed access to feed. Vet ImmunolImmunopathol. (2005) 105:33-45. doi: 10.1016/j.vetimm.2004.12.011
  12. Batal A, Parsons C. E?ect of fasting versus feeding oasis after hatching on nutrient utilization in chicks. Poult Sci. (2002) 81:853–9. doi: 10.1093/ps/81.6.853
  13. Berrocoso JD, Kida R, Singh AK, Kim YS, Jha R. E?ect of in ovo injection of ra?nose on growth performance and gut health parameters of broiler chicken. Poult Sci. (2017) 96:1573–80. doi: 10.3382/ps/pew430
  14. Hollemans MS, de Vries S, Lammers A, Clouard C. E?ects of early nutrition and transport of 1-day-old chickens on production performance and fear response. Poult Sci. (2018) 97:2534–42. doi: 10.3382/ps/pey106
  15. Noy Y, Sklan D. Yolk utilisation in the newly hatched poult. Br Poult Sci. (1998) 39:446–51. doi: 10.1080/00071669889042
  16. Peebles ED. In ovo applications in poultry: a review. Poult Sci. (2018) 97:1–17. doi: 10.3382/ps/pey081
  17. Elnesr SS, Elwan HAM, Xu QQ, Xie C, Dong XY, Zou XT. E?ects of in ovo injection of sulfur-containing amino acids on heat shock protein 70, corticosterone hormone, antioxidant indices, and lipid profile of newly hatched broiler chicks exposed to heat stress during incubation. Poult Sci. (2019). doi: 10.3382/ps/pey609. [Epub ahead of print].
  18. Jochemsen P, Jeurissen SH. The localization and uptake of in ovo injected soluble and particulate substances in the chicken. Poult Sci. (2002) 81:1811–7. doi: 10.1093/ps/81.12.1811
  19. Bhanja SK, Mandal AB. E?ect of in ovo injection of critical amino acids on pre and post-hatch growth, immunocompetence and development of digestive organs in broiler chickens. Asian-Australas J Anim Sci. (2005) 18:524–31. doi: 10.5713/ajas.2005.524
  20. Ohta Y, Yoshida T, Tsushima N, Kidd MT. The needle bore diameter for inovo amino acid injection has no e?ect on hatching performance in broiler breeder eggs. J Poult Sci. (2002) 39:194–7. doi: 10.2141/jpsa.39.194
  21. Maiorano G, Sobolewska A, Cianciullo D, Walasik K, Elminowska-Wenda G, Slawinska A, et al. Influence of in ovo prebiotic and synbiotic administration on meat quality of broiler chickens. Poult Sci. (2012) 91:2963–2969. doi: 10.3382/ps.2012-02208
  22. Romano? AL, Romano? AJ. Biochemistry of the Avian Embryo. New York, NY: Interscience Publishers (1967).
  23. Karcher DM, McMurtry JP, Applegate TJ. Developmental changes in amniotic and allantoic fluid insulin-like growth factor (IGF)-I and-II concentrations of avian embryos. Comp Biochem Physiol A Mol IntegrPhysiol. (2005) 142:404–9. doi: 10.1016/j.cbpa.2005.08.027
  24. Windle WF,   Barcroft  J.  Some factors  governing the   initiation  of  respiration in   the  chick.  Am   J   Physiol. (1938)  121:684–91. doi: 10.1152/ajplegacy.1938.121.3.684
  25. Uni Z, Ferket P, Tako E, Kedar O. In ovo feeding improves energy status of late-term chicken embryos. Poult Sci. (2005) 84:764–70. doi: 10.1093/ps/84.5.764
  26. Afsarian O, Shahir MH, Lourens A, Akhlaghi A, Lotfolahian H, Hoseini A, et al. Eggshell temperature manipulations during incubation and in ovo injection of thyroxine are associated with a decreased incidence of cold-induced ascites in broiler chickens. Poult Sci. (2018) 97:328–36. doi: 10.3382/ps/pex302
  27. Yang T, Zhao M, Li J, Zhang L, Jiang Y, Zhou G, Gao F. In ovo feeding of creatine pyruvate alters energy metabolism in muscle of embryos and post-hatch broilers. Asian-Australas. J. Anim. Sci. (2019). doi: 10.5713/ajas.18.0588. [Epub ahead of print].
  28. Tako E, Glahn RP, Knez M, Stangoulis JC. The e?ect of wheat prebiotics on the gut bacterial population and iron status of iron deficient broiler chickens. Nutr J. (2014) 13:58. doi: 10.1186/1475-2891-13-58
  29. De Oliveira JE, Van der Hoeven-Hangoor E, Van de Linde IB, Montijn RC, Van der Vossen JMBM. In ovo inoculation of chicken embryos with probiotic bacteria and its e?ect on posthatch Salmonella susceptibility. PoultSci. (2014) 93:818–829. doi: 10.3382/ps.2013-03409
  30. Slawinska A, Siwek MZ, Bednarczyk MF. E?ects of synbiotics injected in ovo on regulation of immune-related gene expression in adult chickens. Am J VetRes. (2014) 75:997–1003. doi: 10.2460/ajvr.75.11.997
  31. Noy Y, Sklan D. Energy utilization in newly hatched chicks. Poult Sci. (1999) 78:1750–6. doi: 10.1093/ps/78.12.1750
  32. Sklan D, Noy Y. Hydrolysis and absorption in the small intestines of post-hatch chicks. Poult Sci. (2000) 79:1306–10. doi: 10.1093/ps/79.9.1306
  33. Van den Brand H, Molenaar R, Van der Star I, Meijerhof R. Early feeding a?ects resistance against cold exposure in young broiler chickens. Poult Sci. (2010) 89:716–720. doi: 10.3382/ps.2009-00432
  34. Singh AK, Berrocoso JD, Dersjant-Li Y, Awati A, Jha R. E?ect of a combination of xylanase, amylase and protease on growth performance of broilers fed low and high fiber diets. Anim Feed Sci Tech. (2017) 232:16–20. doi: 10.1016/j.anifeedsci.2017.07.012
  35. National Research Council. Nutrient Requirements of Poultry. 9th ed. Natl Acad Press. Washington, DC (1994).
  36. Rostagno HS, Pupa JMR, Pack M. Diet formulation for broilers based on total versus digestible amino acids. J Appl Poult Res. (1995) 4:293–9. doi: 10.1093/japr/4.3.293
  37. Saki AA. E?ect of post-hatch feeding on broiler performance. Int J Poult SciSci. (2005) 4:4–6. doi: 10.3923/ijps.2005.4.6
  38. Pezeshkian S. Utilization of standard-pre-starter feed formulation flour corn, calcium propionate in primary nutrition of chicken. Poult. Jahan. (2002) 9:13–15
  39. Turner KA, Applegate TJ, Lilburn MS. E?ects of feeding high carbohydrate or fat diets: growth and metabolic status of the post hatch poultry following immediate or delayed access to feed. Poult Sci. (1999) 78:1537–80. doi: 10.1093/ps/78.11.1573
  40. Gri?ths L, Leeson S, Summers JD. Fat deposition in broilers: e?ect of dietary energy to protein balance and early life caloric restriction of productive performance and abdominal fat pad size. Poult Sci. (1977) 56:638–46. doi: 10.3382/ps.0560638
  41. Sell J, Angel CR, Piquer FJ, Mallarino EG, Albatshan HA. Developmental patterns of selected characteristic of the gastrointestinal tract of young turkeys. Poult Sci. (1991) 70:1200–5. doi: 10.3382/ps.0701200
  42. Maiorka A, Magro N, Bartels HAS, Kessler AM, Penz Jr AM. Di?erent sodium levels and electrolyte balances in pre-starter diets for broilers. Braz J Poult Sci. (2004) 6:154–6. doi: 10.1590/S1516-635X2004000 300002
  43. Garcia A, Batal AB. Changes in the digestible lysine and sulfur amino acid needs of broiler chicks during the first three weeks posthatching. Poult Sci. (2005) 84:1350–5. doi: 10.1093/ps/84.9.1350
  44. Noy Y, Sklan D. Nutrient use in chicks during the first week post-hatch. PoultSci. (2002) 81:391–9. doi: 10.1093/ps/81.3.391
  45. Dror  Y, Nir   I,  Nitsan Z.  The  relative growth of  internal  organs in light and heavy breeds. Br Poult Sci. (1977) 18:493–6 doi: 10.1080/00071667708416389
  46. Katanbaf MN, Dunnington EA, Siegel PB. Allomorphic relationships from hatching to 56 days in parental lines and F1 crosses of chickens selected 27 generations for high or low body weight. Growth Dev Aging. (1988) 52:11–21.
  47. Noy Y, Geyra A, Sklan D. The e?ect of early feeding on growth and small intestinal development in the post-hatch poult. Poult Sci. (2001) 80:912–9. doi: 10.1093/ps/80.7.912
  48. Ekino S, Nawa Y, Tanaka K, Matsuno K, Fujii H, Kotani M. Suppression of immune response by isolation of the bursa of Fabricius from environmental stimuli. Aust J Ex Biol Med Sci. (1980) 58:289–96. doi: 10.1038/icb.1980.28
  49. Jeurissen SH, Janse EM, Koch G, De Boer GF. Postnatal development of mucosa-associated lymphoid tissues in chickens. Cell Tissue Res. (1989) 258:119–24. doi: 10.1007/BF00223151
  50. Scha?ner T, Mueller J, Hess MW, Cottier H, Sordat B, Ropke C. The bursa of Fabricius: a central organ providing for contact between the lymphoid system and intestinal content. Cell Immunol. (1974) 13:304–12. doi: 10.1016/0008-8749(74)90247-0
  51. Dibner JJ, Knight CD, Kitchell ML, Atwell CA, Downs AC, Ivey FJ. Early feeding and development of the immune system in neonatal poultry. J ApplPoult Res. (1998) 7:425–36. doi: 10.1093/japr/7.4.425
  52. Lowenthal JW, Connick T, McWaters PG, York JJ. Development of T cell immune responsiveness in the chicken. Immunol Cell Bio. (1994) 72:115–22. doi: 10.1038/icb.1994.18
  53. Tiwari UP, Chen H, Kim SW, Jha R. Supplemental e?ect of xylanase and mannanase on nutrient 883 digestibility and gut health of nursery pigs studied using both in vivo and in vitro models. Anim Feed Sci Technol. (2018) 245:77–90. doi: 10.1016/j.anifeedsci.2018.07.002
  54. Mateos GG, Lázaro R, Gracia MI. The feasibility of using nutritional modifications to replace drugs in poultry feeds. J Appl Poult Res. (2002) 11:437–52. doi: 10.1093/japr/11.4.437
  55. Jha R, Overend DN, Simmins PH, Hickling D, Zijlstra RT. Chemical characteristics, feed processing quality, voluntary feed intake, growth performance, and energy digestibility among wheat classes fed in pelleted diets fed to weaned pigs. Anim Feed Sci Technol. (2011) 170:78–90 doi: 10.1016/j.anifeedsci.2011.08.006
  56. Bedford MR, Schulze H. Exogenous enzymes for pigs and poultry. Nutr Res Rev. (1998) 11:91–114. doi: 10.1079/NRR19980007
  57. Smits CHM, Annison G. Non-starch plant polysaccharides in broiler nutrition – towards a physiologically valid approach to their determination. Worlds Poult Sci, J. (1996) 52:203–221. doi: 10.1079/WPS1996 0016
  58. Choct M, Annison G. Anti-nutritive e?ect of wheat pentosans in broiler chickens: Roles of viscosity and gut microflora. Br Poult Sci. (1992) 33:821–34. doi: 10.1080/00071669208417524
  59. Leeson S, Caston L, Kiaei MM, Jones R. Commercial enzymes and their influence on broilers fed wheat or barley. J Appl Poult Res. (2009) 9:242–51. doi: 10.1093/japr/9.2.242
  60. Mathlouthi N, Juin H, Larbier M. E?ect of xylanase and betaglucanase  supplementation of wheat-or  wheat-  and  barley-based  diets  on the  performance of male  turkeys.  Br  Poult  Sci.  (2003)  44:291–298 doi: 10.1080/0007166031000096498
  61. Wu  YB,  Ravindran  V,  Thomas  DG,  Birtles  MJ,  Hendriks  WH. Influence  of  phytase and xylanase,  individually  or  in  combination, on performance, apparent metabolisable energy, digestive tract measurements and gut morphology in broilers fed wheat-based diets containing adequate level of phosphorus. Br Poult Sci. (2004) 45:76–84. doi: 10.1080/00071660410001668897
  62. Brunsgaard G. E?ects of cereal type and feed particle size on morphological characteristics, epithelial cell proliferation, and lectin binding patterns in the large intestine of pigs. J Anim Sci. (1998) 76:2787–98. doi: 10.2527/1998.76112787x
  63. Engberg RM, Hedemann MS, Steenfeldt S, Jensen BB. Influence of whole wheat and xylanase on broiler performance and microbial composition and activity in the digestive tract. Poult Sci. (2004) 83:925–38. doi: 10.1093/ps/83.6.925
  64. Amerah AM, Ravindran V, Lentle RG, Thomas DG. Feed particle size: implications on the digestion and performance of poultry. Worlds Poult Sci J. (2007) 63:439–55. doi: 10.1017/S004393390700 1560
  65. Penz AM, Bruno DG. Impacts of feed texture and particle sizeon broiler and layer feeding patterns. In: Proc XXIV World s Poult Congress. Salvador. Bahia: Area: Nutrition and Feed Technologies. (2012) pp. 1–8.
  66. Ravindran V, Singh Y, Amerah AM. Whole grain feeding: implications for intestinal function and microbiota. In: Ravindran V, editors Proc FifthInternational Broiler Nutritionists’ Conf. Queenstown (2014) pp. 83–98.
  67. Bjerrum L, Pedersen AB, Engberg RM. The influence of whole wheat feeding on Salmonella infection and gut flora composition in broilers. Avian Dis. (2005) 49:9–15. doi: 10.1637/7223-061504R
  68. Plavnik I, Macovsky B, Sklan D. E?ect of feeding whole wheat on performance of broiler chickens. Anim Feed Sci Technol. (2002) 96:229–36. doi: 10.1016/S0377-8401(01)00321-2
  69. Svihus B, Juvik E, Hetland H, Krogdahl A. Causes for improvement in nutritive value of broiler chicken diets with whole wheat instead of ground wheat. Br Poult Sci. (2004) 45:55–60. doi: 10.1080/00071660410001668860
  70. 70.   Svihus B, Hetland H, Choct M, Sundby F. Passage rate through the anterior digestive tract of broiler chickens fed on diets with ground and whole wheat. Br Poult Sci. (2002) 43:662–8. doi: 10.1080/0007166021000025037
  71. van der Klis JD. Improving feed conversion e?ciency by reducing nutrient wastage. In: Ravindran V, editors Proc Fifth International BroilerNutritionists’ Christchurch (2010) pp. 4–12.
  72. Bruerton K. Gut health in poultry– a nutritionist’s perspective. In: ProcMassey Technical Update Conf. (2014) 16:97–104.
  73. Fasina YO, Olowo YL. E?ect of commercial yeast-based product (Maxigen) on intestinal villi morphology and growth performance of broiler chickens. Int J Poult Sci. (2013) 12:09–14. doi: 10.3923/ijps.2013.9.14
  74. de Jong IC, van Riel J, Bracke MB, van den Brand H. A ’meta-analysis’ of e?ects of post-hatch food and water deprivation on development, performance and welfare of chickens. PLoS ONE. (2017) 12:e0189350. doi: 10.1371/journal.pone.0189350
  75. Jeurissen SH, Lewis F, van der Klis JD, Mroz Z, Rebel JM, and ter Huurne AA. Parameters and techniques to determine intestinal health of poultry as constituted by immunity, integrity, and functionality. Curr Issues IntestMicrobiol. (2002) 3:1–14.
  76. Tako E, Ferket PR, Uni Z. E?ects of in ovo feeding of carbohydrates and beta-hydroxy-beta-methylbutyrate on the development of chicken intestine. PoultSci. (2004) 83:2023–28. doi: 10.1093/ps/83.12.2023
  77. Adeleye OO, Otakoya IO, Fafiolu AO, Alabi JO, Egbeyale LT, Idowu OMO. Serum chemistry and gut morphology of two strains of broiler chickens to varying interval of post hatch feeding. Vet Anim Sci. (2018) 5:20–5. doi: 10.1016/j.vas.2017.12.001
  78. Henderson SN, Vicente JL, Pixley CM, Hargis BM, Tellez G. E?ect of an early nutritional supplement on broiler performance. Int J Poult Sci. (2008) 7:211–4. doi: 10.3923/ijps.2008.211.214
  79. Apajalahti J, Kuttunen A, Graham H. Characteristics of the gastrointestinal microbial communities, with special reference to the chicken. Worlds PoultSci J. (2004) 60:223–32. doi: 10.1079/WPS20040017
  80. Biloni A, Quintana CF, Menconi A, Kallapura G, Latorre J, Pixley C, et al. Evaluation of e?ects of EarlyBird associated with FloraMax-B11 on Salmonella Enteritidis, intestinal morphology, and performance of broiler chickens. Poult Sci. (2013) 92:2337–46. doi: 10.3382/ps.2013-03279
  81. Bogucka J, Dankowiakowska A, Elminowska-Wenda G, Sobolewska A, Szczerba A, Bednarczyk M. E?ects of prebiotics and synbiotics delivered inovo on broiler small intestine histomorphology during the first days after hatching. Folia Biol. (2016) 64:131–43. doi: 10.3409/fb64_3.131
  82. Madej JP, Bednarczyk M. E?ect of in ovo-delivered prebiotics and synbiotics on the morphology and specific immune cell composition in the gut-associated lymphoid tissue. Poult Sci. (2016) 95:19–29. doi: 10.3382/ps/pev291
  83. Pruszynska-Oszmalek E, Kolodziejski PA, Stadnicka K, Sassek M, Chalupka D, Kuston B, et al. In ovo injection of prebiotics and synbiotics a?ects the digestive potency of the pancreas in growing chickens. Poult Sci. (2015) 94:1909–16. doi: 10.3382/ps/pev162
  84. Sobolewska A, Bogucka J, Dankowiakowska A, Elminowska-Wenda G, Stadnicka K, Bednarczyk M. The impact of synbiotic administration through in ovo technology on the microstructure of a broiler chicken small intestine tissue on the 1st and 42nd day of rearing. J Anim Sci Biotechnol. (2017) 8:61. doi: 10.1186/s40104-017-0193-1
  85.  Borda-Molina D, Seifert J, Camarinha-Silva A. Current perspectives of the chicken gastrointestinal tract and its microbiome. Comput Struct Biotechnol J. (2018) 16:131–9. doi: 10.1016/j.csbj.2018.03.002
  86. Berrocoso JD, Yadav S, Jha R. Nitrogen-corrected apparent metabolizable energy value of macadamia nut cake for broiler chickens determined by di?erence and regression methods. Anim Feed Sci Technol. (2017) 234:65–71. doi: 10.1016/j.anifeedsci.2017.09.009
  87. Choct M, Hughes RJ, Wang J, Bedford MR, Morgan AJ, Annison G. Increased small intestinal fermentation is partly responsible for the anti-nutritive activity of non-starch polysaccharides in chickens. Br Poult Sci. (1996) 37:609–21. doi: 10.1080/00071669608417891
  88. Langhout DJ, Schutte JB, van Leeuwe P, Wiebenga J, Tamminga S. E?ect of dietary high- and low-methylated citrus pectin on the activity of the ileal microflora and morphology of the small intestinal wall of broiler chicks. BrPoul Sci. (1999) 40:340–7. doi: 10.1080/00071669987421
  89. Langhout DJ, Schutte JB, de Jong J, Sloetjes H, Verstegen MW, Tamminga S.E?ect of viscosity on digestion of nutrients in conventional and germ-free chicks. Br J Nutr. (2000) 83:533–540
  90. Apajalahti J. Structure and dietary modulation of intestinal microbial communities. In: Proc. 2nd Mid-Atlantic Nutr. Conf. Timonium, M. D. (2004).
  91. Pourabedin M, Zhao X. Prebiotics and gut microbiota in chickens. FemsMicrobiol Lett. (2015) 362:fnv122. doi: 10.1093/femsle/fnv122
  92. Apajalahti JH, Kettunen H, Kettunen A, Holben WE, Nurminen PH, Rautonen N, et al. Culture-independent microbial community analysis reveals that inulin in the diet primarily a?ects previously unknown bacteria in the mouse cecum. Appl Environ Microbiol. (2002) 68:4986–95. doi: 10.1128/AEM.68.10.4986-4995.2002
  93. Chee SH, Iji PA, Choct M, Mikkelsen LL, Kocher A. Characterisation and response of intestinal microflora and mucins to mannooligosaccharide and antibiotic supplementation in broiler chickens. Br Poult Sci. (2010) 51:368–80. doi: 10.1080/00071668.2010.503477
  94. Villaluenga CM, Wardenska M, Pilarski R, Bednarczyk M, Gulewicz K. Utilization of the chicken embryo model for assessment of biological activity of di?erent oligosaccharides. Folia Biol. (2004) 52:135–42. doi: 10.3409/1734916044527502
  95. Friedman A, Sklan D. E?ects of retinoids on immune responses in birds. Worlds Poult Sci J. (1997) 53:186–95. doi: 10.1079/WPS19970016
  96. Sklan D, Melamed D, Friedman A. The e?ect of varying levels of dietary vitamin A on immune response of the chick. Poult Sci. (1994) 73:843–7. doi: 10.3382/ps.0730843
  97. 97.  Klasing KC. Nutritional modulation of resistance to infectious diseases. PoultSci. (1998) 77:1119–25. doi: 10.1093/ps/77.8.1119
  98. Cook ME. Nutrition and the immune response of the domestic fowl. Crit RevPoult Biol. (1991) 3:167–89.
  99. Gallego M, Cacho ED, Bascuas JA. Antigenbinding cells in the Cecal tonsils and Peyer’s patches of the chicken after bovine serum albumin administration. Poult Sci. (1995) 74:472–9. doi: 10.3382/ps.0740472
  100. Gore AB, Qureshi MA. Enhancement of humoral and cellular immunity by vitamin E after embryonic exposure. Poult Sci. (1997) 76:984–91. doi: 10.1093/ps/76.7.984
  101. Kidd MT. Nutritional modulation of immune function in broilers. Poult Sci. (2004) 83:650–657. doi: 10.1093/ps/83.4.650
  102. Kadam MM, Bhanja SK, Mandal AB, Thakur R, Vasan P, Bhattacharyya A, et al. E?ect of in ovo threonine supplementation on early growth, immunological responses and digestive enzyme activities in broiler chickens. Br Poult Sci. (2008) 49:736–41. doi: 10.1080/000716608024 69333
  103. Bakyaraj S, Bhanja SK, Majumdar S, Dash B. Modulation of post-hatch growth and immunity through in ovo supplemented nutrients in broiler chickens. J Sci Food Agric. (2012) 92:313–20. doi: 10.1002/jsfa.4577
  104. Selvaraj  RK,  Cherian  G.  Dietary  n-3  fatty  acids  reduce  the  delayed hypersensitivity reaction and  antibody  production more  than   n-6 fatty acids in broiler birds. Eur J Lipid Sci Tech. (2004) 106:3–10.doi: 10.1002/ejlt.200300848
  105. Bhanja SK, Goel A, Pandey N, Mehra M, Majumdar S, Mandal AB. In ovo carbohydrate supplementation modulates growth and immunity-related genes in broiler chickens. J Anim Physiol Anim Nutr. (2015) 99:163–73. doi: 10.1111/jpn.12193
  106. Bhanja SK, Sudhagar M, Goel A, Pandey N, Mehra M, Agarwal SK, et al. Di?erential expression of growth and immunity related genes influenced by in ovo supplementation of amino acids in broiler chickens. Czech J Anim Sci. (2014) 59:399–408. doi: 10.17221/7651-CJAS
  107. Cheled-Shoval SL, Amit-Romach E, Barbakov M, Uni Z. The e?ect of in ovo administration of mannan oligosaccharide on small intestine development during the pre-and posthatch periods in chickens. Poult Sci. (2011) 90:2301–10. doi: 10.3382/ps.2011-01488
  108. Dalloul RA, Lillehoj HS, Lee JS, Lee SH, Chung KS. Immunopotentiating e?ect of a Fomitella fraxinea-derived lectin on chicken immunity and resistance to coccidiosis. Poult Sci. (2006) 85:446–51. doi: 10.1093/ps/85.3.446
  109. Gao T, Zhao MM, Zhang L, Li JL, Yu LL, Lv PA, et al. E?ects of in ovo feeding of l-arginine on the development of lymphoid organs and small intestinal immune barrier function in post-hatch broilers. Anim Feed Sci Tech. (2017) 225:8–19. doi: 10.1016/j.anifeedsci.2017.01.004
  110. Lowry VK, Farnell MB, Ferro PJ, Swaggerty CL, Bahl A, Kogut MH. Purified β-glucan as an abiotic feed additive up-regulates the innate immune response in immature chickens against Salmonella enterica serovar Enteritidis. Int J Food Microbiol. (2005) 98:309–18. doi: 10.1016/j.ijfoodmicro.2004. 06.008
  111. Newsholme P. Why is L-glutamine metabolism important to cells of the immune system in health, postinjury, surgery or infection? J Nutr. (2001) 131:2515S−2522S. doi: 10.1093/jn/131.9.2515S
  112. Obled C. Amino acid requirements in inflammatory states. Can J Anim Sci. (2003) 83:365–73. doi: 10.4141/A03-021
  113. Kadam MM, Barekatain MR, Bhanja SK, Iji PA. Prospects of in ovo feeding and nutrient supplementation for poultry: the science and commercial applications- a review. J Sci Food Agric. (2013) 93:3654–61. doi: 10.1002/jsfa.6301
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Authors:
Rajesh Jha
University of Hawai
Julio Diaz Berrocoso
FARM Faes
Birendra Mishra
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Sushil Chandra
18 de octubre de 2020

A good article
I am here for practical approach
1 Brooder house and brooder lights/heating system must be kept ON 12 hrs before arrival of chicks
2 Add probiotic, B complex and Vit A in water 12 hrs before arrival of chicks so that first water to chicks is lukewarm
3 Grounded maize to be given for first 24 hrs before introducing pre starter
4 Brooder temo must be maintained at 95 degree F during first week
5 Proper ventilation is a must with strict biosecurity
Level of Lysine, methionine, avl P must be kept as standard
Regards

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Hosna hajati
14 de diciembre de 2020
In ovo feeding is a very good idea specially for the weak embryos. I have worked on broilers and quails embryos many times and the results were promising.
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Narcisse rukundo
30 de noviembre de 2020
Good nutrition of chicken it is Importants in bodies to improving a good health in animals
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Oprea Petru
17 de noviembre de 2020
a very good article. Feeding in ovo has a very interesting perspective
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Dr Fawad khalil
3 de noviembre de 2020

Hello Dr. Sushil Chandra;
I appreciate your knowledge sharing and I totally agree with you regarding the role of probiotics during early ages in poultry. Can you guide us about the role of Lysine and Methionine in poultry individually?
Dr. Fawad Khalil
DVM, Mphil

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