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From colostrum to weaning: nutritional regulation of gut function in the dairy calf

Published: October 7, 2021
By: Amanda J. Fischer-Tlustos and Dr. Michael A. Steele 1 / 1 Associate Professor in Animal Physiology, Department of Animal Biosciences, University of Guelph, Guelph, ON.
Summary

Raising healthy and productive calves is fundamental in ensuring the long-term success of the Canadian dairy industry. Unfortunately, pre-weaning calves suffer from the highest rates of morbidity (34%) and mortality (5%) amongst all animals on the dairy farm. Digestive disorders occurring before 2 weeks of age are the largest contributor to calf sickness and death; however, a multitude of previous research has demonstrated that proper nutritional management can have a positive impact on gut function and development, as well as productivity and health. During the first day of life, ensuring passive transfer in newborn calves is essential. Yet, colostrum contains an abundance of bioactive compounds aside from IgG, such as oligosaccharides, fatty acids and growth hormones, that may have beneficial effects on early life gut development. Maximizing preweaning whole milk or milk replacer (MR) intake is essential in promoting animal health and elfare, but there is growing interest in feeding elevated levels of MR as the macronutrient composition, namely lactose and fat, differs greatly from whole milk. Moreover, weaning calves from enhanced milk feeding programs can often result in health and production challenges and the source and level of starch in calf starter may further exacerbate this issue. Further research regarding optimal nutritional strategies during the newborn, pre-weaning and weaning stages is needed to allow industry representatives and dairy producers to make confident decisions to promote calf health, welfare and productivity.

Introduction
The nutritional management of young dairy calves can have both short- and long-term effects, from influencing morbidity and mortality rates (Urie et al., 2018a) to reproductive efficiency and first-lactation milk yield (Faber et al., 2005; Soberon et al., 2012; Gelsinger et al., 2015). Although major improvements in calf nutritional strategies have been made over the past decade, dairy calves continue to suffer from the highest rates of mortality (5 - 6.4%) and morbidity (34%) amongst all animals on the dairy farm (Winder et al., 2018; Urie et al., 2018a). Digestive diseases and disorders (i.e. diarrhea) remain the most commonly reported cause of morbidity and mortality, accounting for over half of illnesses and one-third of deaths (Urie et al., 2018a). As such, digestive disorders represent a major cause of economic loss to dairy producers and cause concern from an animal welfare standpoint. Digestive disorders can often be mitigated through proper early life nutrition and health management regimens and developing strategies to improve calf gut health is fundamental in ensuring a profitable and sustainable dairy industry. Therefore, this review will focus on the effects of common nutritional strategies on gut development and function during three of the most challenging periods of the calf’s life. Specifically, this paper will describe colostrum and transition milk feeding during the first days of life, plane of nutrition and diet composition during the first weeks of life, and differential weaning strategies and their effects on gut development.
Colostrum Feeding
Ensuring Passive Transfer
The calf is essentially born immune-deficient and relies on the feeding of 3-4 L of high quality (> 50 g of IgG/L) colostrum with a total bacterial count < 100,000 cfu/ml in the first hours of life (Weaver et al., 2000; McGuirk and Collins, 2004) to ensure its health and survival. Although this is well known, failure of passive transfer (FPT; serum IgG ≤ 10 mg/mL) still occurs in 12-19% of heifer calves (Beam et al., 2009; Shivley et al., 2009). High rates of FPT are associated with increased calf morbidity and mortality (Urie et al., 2018a) and decreased average daily gain (ADG; Robison et al., 1988). Moreover, feeding inadequate amounts of colostrum results in decreased survival and milk yield through the first (DeNise et al., 1989) and second lactation (Faber et al., 2005). Therefore, there is a significant need to improve colostrum management practices to not only promote calf health and welfare but also to ensure future productivity.
As previously mentioned, one of the most critical factors in ensuring the passive transfer of IgG is the timely feeding of colostrum after birth. Immediately after birth, the gut is considered “open” as the intestinal cells can non-selectively absorb large molecules, such as IgG, into circulation. Fischer et al. (2018a) demonstrated that calves fed colostrum at 6 and 12 h after birth displayed a 28% and 32% reduction in maximum serum IgG concentrations and the apparent efficiency of absorption of IgG, respectively, compared to calves fed immediately after birth. Importantly, calves fed at 6 and 12 h of life did not differ in any IgG parameters measured, suggesting that there may be a critical time point between 1 to 6 h of life in which the closure of the small intestine progresses to a finite degree. Unfortunately, the exact mechanism by which gut closure occurs has yet to be elucidated and future research is needed to determine the factors that control gut closure in the absence of colostrum feeding.
In addition to the quickness of colostrum feeding, Hare et al. (unpublished data) found that feeding multiple meals of colostrum can positively influence serum IgG concentrations. Specifically, calves fed colostrum for 3 d of life had greater maximum serum IgG concentrations compared to calves fed whole milk after the initial colostrum meal. Furthermore, calves fed multiple meals of colostrum had more persistent serum IgG concentrations (i.e. concentrations remained at a greater proportion of maximum IgG concentration reached) compared to calves only fed one meal, which may assist in preventing early life morbidity by reducing the high rates of digestive disorders. In addition, previous work found that the method by which colostrum is fed can influence serum IgG concentrations, with calves fed from a nipple bottle or an esophageal tube feeder having FPT rates of 14% and 9%, respectively (Shivley et al., 2018). However, a study directly investigating the influence of feeding 3 L of colostrum via nipple bottle or tube feeder on passive transfer (Desjardins-Morrissette et al., 2018) found no differences in serum IgG concentrations. The authors suggested that feeding large volumes of colostrum (≥ 3 L) via an esophageal tube feeder likely results in a negligible proportion of colostrum overflow into the rumen, which would not influence serum IgG concentrations to a large extent.
Establishing a Healthy Gut
Due to the importance of IgG in ensuring the health and survival of the newborn calf, colostrum has largely been known for promoting the acquisition of passive immunity over the past decades.
However, recent work has found that colostrum plays a key role in establishing a healthy gut bacterial community, which fundamentally promotes host health (Round and Mazmanian, 2009) and proper immune system development (Russell et al., 2013). In 2015, Malmuthuge et al. found that feeding colostrum resulted in a higher abundance of total bacteria and proportion of Bifidobacterium in the small intestine at 12 h of life, suggesting that colostrum is necessary for accelerating the microbial colonization of the gastrointestinal tract (GIT). Similarly, calves fed colostrum at 12 h of life tended to have a decreased proportion of Bifidobacterium and Lactobacillus associated with the colon mucosa compared to calves fed immediately after birth (Fischer et al., 2018a). It has been suggested that colostrum oligosaccharides (OS), which are up to 72 times greater in colostrum than in whole milk (Fischer-Tlustos et al., 2020), may mediate the early establishment of gut microbiota by acting as prebiotic compounds for beneficial bacterial species (Yu et al., 2013; Fischer et al., 2018b). Importantly, not feeding colostrum has been associated with an increased prevalence of small intestinal Escherichia coli (Malmuthuge et al., 2015) and delaying colostrum feeding until 12 h of life increases the abundance of opportunistic pathogens, namely Enterococcus and Streptococcus (Ma et al., 2019). Although these studies offer insight into the development of the calf gut microbiota and the potential influence that colostrum may have on promoting a healthy gut environment, how the colonization of these specific bacterial groups may affect future health and productivity needs to be explored further. 
Colostrum not only contains compounds that promote gut bacterial colonization, but also contains high levels of nutrients, namely fat, that have been implicated in stimulating the secretion of glucagon-like peptide (GLP)-1 and GLP-2 (Burrin et al., 2003). Specifically, it was found that feeding colostrum by nipple bottle or tube-feeder both equally promoted the secretion of GLP-1 and GLP-2 (Desjardins-Morrissette et al., 2018), while delaying colostrum feeding until 12 h of life reduced plasma GLP-1 and GLP-2 concentrations compared to calves fed immediately after birth (Inabu et al., 2018). GLP-1 and GLP-2 are known for playing a key role in glucose homeostasis (Fukumori et al., 2012) and stimulating gastrointestinal growth (Taylor-Edwards et al., 2011), respectively, and thus it is clear that the early feeding of colostrum is important for ensuring optimal gut development and metabolism. In addition to promoting the secretion of gut hormones, fat also plays a key role in thermoregulation and certain omega fatty acids (FA) that are elevated in colostrum compared to whole milk (Hare et al., 2019) can have prolonged benefits in terms of antioxidant status and immune response (Opgenorth et al., 2019). In addition, colostrum contains elevated levels of insulin and insulin-like growth factor-1 (IGF-1; Blum and Hammon, 2000), both of which can promote intestinal cell proliferation, as well as antimicrobial compounds, such as lactoferrin and lactoperoxidase, which help to maintain a healthy gut environment (Pakkanen and Aalto, 1997). Therefore, although the multitude of bioactive colostral compounds have been largely overlooked during the past few decades, it is clear that colostrum has a much larger role in calf development than simply providing IgG.
Table 1. Levels of bioactive molecules in colostrum (milking 1) compared to whole milk1 and their proposed functions.
Levels of bioactive molecules in colostrum (milking 1) compared to whole milk1 and their proposed functions.
Transition Milk
The aforementioned bioactive molecules are not only elevated in colostrum but are also present at high concentrations in transition milk (TM, milkings 2-6) compared to whole milk. For instance, TM contains elevated levels of primary acidic OS (Fischer-Tlustos et al., 2020), IGF-1, insulin (Blum and Hammon, 2000), nucleotides (Gill et al., 2011) and proportions of omega-3 FA (Hare et al., 2019) compared to whole milk. Recent research has also determined that feeding a 1:1 colostrum:whole milk mixture (MIX) to simulate TM feeding increased small intestinal surface area and cell proliferation in certain intestinal segments at 3 d of life (Pyo et al., 2020) and increased GLP-1 production (Inabu et al., 2019), which can have beneficial effects on energy use. Furthermore, feeding MIX improved IgG persistency (91% of maximum concentration, Cmax) compared to calves fed whole milk (75% of Cmax) after the initial colostrum feeding (Hare et al., unpublished data). Although IgG in MIX, or TM, will not be transported circulation after 24 h of life (Weaver et al., 2000), antibodies remaining in the lumen may assist in providing local immunity against enteric pathogens (Berge et al., 2009). Despite this knowledge, a large proportion of dairy producers continue to discard TM and transition calves directly to milk replacer (MR) or whole milk after the first colostrum feeding, which may result in missed opportunities to improve newborn calf gut health and metabolism. The current lack of information regarding TM feeding emphasizes the need for future research describing the importance of these specific compounds on metabolic regulation and development in the newborn calf, which may lead the development of TM or colostrum:whole milk feeding strategies to improve calf gut health.
Milk Nutrition
Plane of Nutrition
After colostrum or TM feeding for the first days of life, calves are often transitioned to elevated (≥ 8 L or 1.2 kg of MR powder/d, 67% of Canadian producers) or conventional (≤ 6 L or 900 kg MR powder/d, 33% of Canadian producers) planes of milk nutrition (Winder et al., 2018). Conventional programs aim to encourage early starter intake to facilitate rumen development (Tamate et al., 1962), which may result in less susceptibility to health and production challenges during weaning. However, calves fed elevated planes of nutrition have improved animal welfare through reduced starvation-associated behaviours (De Paula Vieira et al., 2008) and increased potential to produce more milk during lactation, improved mammary development, reduced age at first calving (Soberon et al., 2012) and improved immune function (Ballou et al., 2015) compared to calves fed conventional levels of milk. A recent study by Haisan et al. (2019) demonstrated that all calves offered large volumes of milk were able to consume over 8 L of whole milk/d and up to 10 L/d using an automated feeder during the first week of life. Although this clearly demonstrates that elevated feeding programs are synergistic with the calf’s natural ability to consume large volumes of milk during early life, the majority of Canadian producers still limit calves to 4 L of milk/d from days 1-7 of life (Vasseur et al., 2010). At this time, all metabolizable nutrients are consumed directly from milk due to negligible starter intake and maintenance requirements alone equal ~3 L of milk/d; therefore, feeding only 4 L largely restricts energy for growth. This large restriction in metabolizable energy is likely why calves in the aforementioned study only gained 400 g/d during the first week of life when limit-fed 5 L/d compared to calves fed over 8 L/d, who gained up to 800 g/d (Haisan et al., 2019). 
Despite the well-known benefits of feeding elevated planes of nutrition, many producers do not adopt this practice as they perceive it as unfeasible without automated feeding. This is mainly due to concerns around feeding large volumes of milk in 2 meals/d, because previous research suggested that feeding a large volume of milk in a single feeding can lead to abomasal overflow of milk into the rumen (Berends et al., 2015) and reduced insulin sensitivity (Bach et al., 2013). However, a 2016 study (Ellingsen et al.) demonstrated that calves can consume 5-7 L of milk per meal without any overflow into the rumen. Furthermore, MacPherson et al. (2018) found that calves fed 8 L of milk over 2 or 4 meals/d did not display any differences in insulin sensitivity during a glucose tolerance test. Calves fed only 2 meals per day had a decreased rate of abomasal emptying, indicating that glucose delivery was slowed, which may have regulated insulin response. It is important to note that calves were fed 8 L/d over 2 meals beginning from the first week of life, and this may be a crucial metabolic developmental window in which the calf adapts to consuming high volumes of milk; however, further research regarding the longterm effects of this practice on calf metabolism and development is warranted.
Milk Replacer vs. Whole Milk Composition
In Canada, 50% of dairy producers feed calves milk replacer (Vasseur et al., 2010) as opposed to whole milk. Producers generally adopt MR feeding because the nutrition provided is consistent, and it is clean and convenient. However, previous work has shown advantages to feeding whole milk compared to MR, including lower mortality and morbidity rates (Godden et al., 2005), higher energy content and a balanced supply of nutrients (Davis and Drackley, 1998). There is growing interest in the macronutrient composition of MR as it contains more lactose (45 vs. 35%) and less fat (18 vs. 30%) compared to whole milk. Still, little information exists regarding how feeding MR - especially large volumes - may affect calf gut health. High fat consumption is essential in meeting the energy demands of the young calf and increased inclusion in liquid feed can reduce the odds of mortality by 3-fold in preweaned calves (Urie et al., 2018a). Furthermore, MR is typically formulated using animal- and plant-based fats that often differ greatly in FA profiles compared to whole milk, which can negatively affect calf productivity and health (Jenkins et al., 1985). Recent work by Welboren et al. (2019a) demonstrated that feeding MR with high fat and low lactose content during the first week of life tended to delay abomasal emptying compared to calves fed a traditional MR. This may be beneficial in delaying the digestion of nutrients to allow for better absorption and may have provided reasoning for calves fed a high fat MR experiencing a lesser rise in glucose and insulin concentrations as opposed to calves fed a traditional MR (Welboren et al., 2019a). This finding suggests that high lactose inclusion may negatively affect glucose homeostasis; however, whether this practice leads to the development of insulin resistance requires further investigation. In addition, high lactose inclusion in MR can drastically increase osmolality (~400-600 mOsm/L) compared to whole milk (300 mOsm/L), which can increase intestinal permeability and potentially disturb gut mucosal structure and function (Wilms et al., 2019). However, current research on this topic is lacking and/or conflicting (Welboren et al., 2019b), and it is clear that more research is required to identify calf metabolic and intestinal development responses as calves are progressively fed larger volumes of MR.
Weaning Transition
In nature, calves would consume > 10 L of milk/d over multiple small meals, with weaning occurring at 7-14 months of age (Reinhardt and Reinhardt, 1982). This is a stark contrast to the majority of weaning strategies in the dairy industry, in which weaning typically occurs around 9 weeks of age (Urie et al., 2018b). In an effort to limit feeding costs, encourage early starter intake and rumen development, many operations wean calves at 4-6 weeks of life. Unfortunately, the digestive tract of calves fed elevated planes of nutrition during the preweaning period are not equipped to digest large amounts of solid feed during the weaning and post-weaning periods. This often results in production and health challenges, likely due to the decreased digestibility of fiber, NDF, and gross energy (Terre et al., 2007; Hill et al., 2016; Dennis et al., 2018). Research has shown that the production challenges experienced during the weaning transition in calves fed elevated planes of milk pre-weaning can be improved by extending weaning from 6 to 8 weeks of life (Eckert et al., 2015; Meale et al., 2015). In addition, potential negative outcomes can be further mitigated by utilizing the “step-down” weaning method when weaning from elevated planes of milk. Specifically, research by Khan et al. (2007a,b) found that calves receiving elevated levels of milk at 20% of BW until d 23, followed by a step-down to 10% of BW from d 23 to d 44 had increased solid feed intake and weight gain compared to calves fed at 10% of BW until d 44. As such, this may be a feasible and efficient strategy to maximize weight gain while simultaneously achieving early weaning and rumen development. Moreover, the increasing implementation of automated feeding will likely play a large role in optimizing weaning strategies in the future. Automated feeding can be used to achieve linear declines in milk intake, which can result in increased performance compared to calves reduced at abrupt 2 L intervals (Welboren et al., 2019c), as well as to design individualized strategies based on starter intake.
The GIT undergoes significant changes during weaning, with the total volume of the rumen increasing from 30% to 70% of the entire forestomach (Warner et al., 1965) and short chain fatty acids (SCFA) accounting for 80% of the calf’s energy after weaning. The rumen transcriptome and microbiome also undergo rapid maturation, with increased expression of gut barrier (Malmuthuge et al., 2013) and metabolic genes (Connor et al., 2013) and substrates in calf starter shifting microbial populations (Meale et al., 2017). Calves are often fed high starch (> 30%) in calf starter in an effort to initiate rapid rumen development; however, this can result in ruminal acidosis due to the accumulation of SCFA. Recent work has found that it can take up to 5 weeks after weaning for the rumen environment of calves fed elevated planes of nutrition preweaning to be in a state that is not considered ruminal acidosis (Van Niekerk et al., unpublished data). Furthermore, severe acidosis may also affect the hindgut (Li et al., 2012), as evidenced by high levels of fecal starch in calves fed elevated planes of nutrition pre-weaning (Eckert et al., 2015; Van Niekerk et al., 2020). The site of fermentation may be shifted depending on the source of starch, with calves fed elevated levels of milk and whole corn in calf starter displaying decreased fecal pH for 2 weeks following weaning compared with calves fed flaked corn (Van Niekerk et al., 2020). These results suggest that whole corn may shift the site of fermentation to the lower gut, possibly resulting in hindgut acidosis. This is highly unfavourable, as it can lead to systemic inflammatory responses that negatively affect both calf production and health. At present, few studies have characterized the functional changes occurring in the lower gut during weaning. Further research regarding the combined impacts of pre-weaning planes of nutrition, source and level of starch in starter, and weaning strategy is needed. 
Conclusion
It is clear that nutritional management during the newborn, pre-weaning and weaning phases can largely impact growth performance, health and gut function and development. Although colostrum research has largely focused on improving passive transfer over the past few decades, colostrum and transition milk contain a multitude of bioactive molecules beyond IgG that can positively influence gastric development and metabolism. Furthermore, maximizing nutrient intake from milk or MR during early life is essential in supporting growth when starter intake is negligible; however, a large knowledge gap currently exists around how current MR formulations may affect calf gut development and metabolism when elevated planes of nutrition are fed. Weaning calves from elevated planes of nutrition can result in health and production challenges, which can be mitigated through the use of step-down weaning methods and may be further improved and individualized with the recent and rapid implementation of automated feeding. In conclusion, further research is needed to determine the functional changes and long-term consequences of differing nutritional strategies during the first days, weeks and months of the calf’s life in order to maximize calf health and productivity.
Published in the proceedings of the Animal Nutrition Conference of Canada 2020. For information on the event, past and future editions, check out https://animalnutritionconference.ca/.

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Michael A. Steele
Poultry Health Research Network
Poultry Health Research Network
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Treen Huo
Nano discovery
4 de noviembre de 2021

Nice article - colostrum feeding is extremely important to pass the immunity from mother cows to newborn calves.

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