Impact of Ruminal Transfaunation on Performance and Health of Fattening Lambs – A Review
Understanding the host impact on its symbiotic microbiota is crucial in redirecting the rumen microbiota and thus improving animal health and performance. Rumen fluid transplantation has been proposed as one of the promising methods for reshaping the symbiotic microbiota and enhancing host health and performance. The aim of this invited review is to summarize the impact of ruminal transfaunation on the health and performance of sheep especially fattening lambs. Rumen transfaunation using the ruminal fluid from a healthy donor animal to improve the rumen microbiota and treat a sick recipient animal was performed long before. The microbial populations and associated advantages of the rumen transfaunation have been explored in many studies before. Rumen fluid transplantation has been performed to confer benefits for animals by altering gastrointestinal tract microbiota. Ruminant scientists agree that restoring ruminal bacterial equilibrium of animals suffering from ruminal disorders like simple indigestion, acidosis, plant intoxication, and following surgical correction of a left-displaced abomasum, would aid rumen function recovery. In humans, the support of a healthy microbial community in the digestive tract is also recommended previously. In humans, digestive disorders have been treated with fecal microbiota transplantation. This review presents the impact of ruminal transfaunation on the gastrointestinal microbial ecology, production performance, antioxidant status and immune response of sheep especially fattening lambs.
Introduction
Ruminants are mammals (Class – Mammalia) in the Order Arteriodactyla (toed mammals and hooved) Suborder Ruminantia. The word ruminant, came from the Latin word ruminare, means to chew over gain hence the nomenclature of cud chewing [1]. The ruminant can be considered to be a superorganism because it has a symbiotic relationship of life between the cells of the animal›s body and the rumen microbes. The host animal has been affected by factors influencing the viability of microorganisms in the reticulo-rumen as well as anywhere along the gastro-intestinal tract [1]. Ruminants have a four-chambered stomach, consisting of the reticulum, rumen, omasum and abomasum. Ruminants typically eat quickly with minimal chewing. After being swallowed, feed enters the reticulum, which is continuous with the rumen. The rumen is the largest of the four stomach chambers and serves as a large mixing vat that is the site of microbial fermentation and nutrient absorption. Combined, the rumen and reticulum of an adult dairy cow can hold around 50 gallons of partially digested feed. The omasum, with its many leaves or laminae, regulates flow of digesta to the abomasum. The abomasum is the gastric, glandular compartment similar to the stomach of nonruminants (simple stomach animals) with secretion of acid (HCl) and pepsinogen and a pyloric sphincter that controls flow of digesta from the abomasum to the duodenum [1].
Rumination involves the partially digested feed (cud) is regurgitated by bringing the cud up to the esophagus, and then re-chewed in the mouth. Chewing during rumination is slower and more consistent than during eating. The cud is eventually re-swallowed and the process continues with another bolus regurgitated for cud chewing (crushing and grinding of particles by the molars). The rumination process stimulates saliva production to help buffer the rumen pH and decrease feed particle size, allowing it to pass from the reticulum into the omasum. As partially digested feed passes through the omasum, water is absorbed, reducing the volume of material that arrives in the abomasum. The abomasum, often referred to as the true stomach, produces acid and digestive enzymes similar to the stomach of non-ruminant animals, further breaking down the feed before it passes into the lower gastrointestinal tract for further digestion, absorption and ultimately elimination. Cud chewing increases surface area of the feed particles, in particular fibrous material, to enhance microbial digestion [1].
Gastrointestinal microbiota has an important role in the health and feed utilization of animals [2]. The symbiotic microbiota in the rumen facilitates the digestion by decomposing the ingesta and degrading the plant materials into different volatile fatty acids (VFAs), ammonia, etc., to supply the host with nutrient and energy [3]. Therefore, the improvement of rumen microbial ecology can possibly affect the digestion capability resulting in enhanced lamb feed efficiency and then production performance. Various methods have been performed into previous studies to redirect rumen microbiota. For instance, changing rumen pH [4], minimizing the rumen protozoa [5], changing animal diets [6], dietary supplementation of feed additives like probiotics, prebiotics and synbiotics [7] have been investigated in different studies. On the contrary, no one of the previously mentioned methods has shown harmonic positive effects, indicating that the previously mentioned methods to improve animal health and production performance by reshaping the symbiotic microbiota have not been achieved yet.
A balance of symbiotic bacteria is necessary for a healthy intestinal microbiome and related physiological homeostasis [8, 9]. In the case of ruminants, ruminal fluid transplantation has been known to transfer ruminal microbes from healthy donor animals to provide health benefits to the recipient ones [2]. Rumen fluid transplantation has been proposed as one of the promising methods for changing the symbiotic microbiota and improving host production performance [1]. Whether ruminal fluid transplantation can accelerate gastrointestinal transition, reshape gastrointestinal microbiota communities. In large ruminants, ruminal fluid transplantation has been developed to reduce the harmful effects of rumen acidosis [10], treat rumen function disorders [1], and improve health of cows with surgical correction of displaced abomasum [11]. In small ruminants, ruminal fluid transplantation has improved immunological and inflammatory reactivity while decreasing feed intake, nutrient digestibility, and growth performance [12]. However, ruminal fluid transplantation may not be appropriate for lambs during weaning, and research with calves suggests that fast changes in the gut microbiota during weaning may be hazardous [13]. These conflicting findings may be partially due to variations of the symbiotic bacteria (i.e., bacterial strains and types) as well as dosage.
Therefore, this review aimed at elucidating the impact of ruminal transfaunation on health and production performance of sheep especially fattening lambs. To prepare the review, we conducted a literature search with focus on the effect of ruminal transfaunation on health and performance of sheep using the following criteria: (1) peer-reviewed journal articles in English were included; (2) chapters in an edited book were selectively involved; (3) studies on cows and fattening calves were selectively included to verify and/ or support the data on sheep. The key words used during literature search included ruminal transfaunation, health, production performance, sheep.
Ruminal Transfauntion
Ruminal transfauntion is vital for animal health and feed consumption and also it has been established in the case of ruminants to transfer ruminal microorganisms from healthy donor animals to receivers to give health advantages [2]. Ruminal transfauntion has been presented as one of the potential approaches for changing the symbiotic microbiota and improving host performance [1]. Transfauntion of gastrointestinal microbiota improved gut barrier damage in pigs [14] and successfully treated sheep ruminal acidosis [10].
Concept of Rumen Microbiome (Symbiotic Microbiota)
The rumen can be showed as an anaerobic and methanogenic fermentation chamber that involves microorganisms that have the ability to use, and improve the productivity of, cellulolytic feeds (i.e. straw, silage, hay, and grass) [15]. The rumen microbiome, i.e., the community of microorganisms that found in the rumen, is characterized by its extensive diversity (encompassing bacteria, archaea, protozoa and fungi), high population density and complexity of interactions [16]. The continuous fermentation carried out by these microorganisms leads to ingested compounds being broken down into their subcomponents. There are three intersecting micro-environments found in the rumen that contain these microbes; the solid phase making up 70% of the microbial mass, the liquid phase making up 25% of the microbial mass, and the rumen epithelial cells and protozoa, containing 5% of the microbial mass [17]. The ruminal microbiota is a diverse and complex ecology that is critical to animal health and performance.
Diet, environment, age, and the host’s health state are all discovered to have a role in developing the rumen microbiota. Diet, in particular, can have a significant impact on rumen function by modifying microbial populations and fermentation activity [4, 18, 19, 20]. Roughage influences rumen development and the expression of genes involved in VFA absorption in rumen epithelial cells. As a result, one of the most important aspects, diet, has been adjusted in big feeding operations of ruminants to enhance feed efficiency. According to a review of the available research [19], nutrition has the greatest impact on ruminal microbiota, however comparison studies across species are needed. Scientists would use modern omics technologies to quickly identify the microbial makeup, functions in the gastrointestinal track (GIT), host-microbe interactions, and variables influencing GIT microbiota.
Another element influencing rumen bacteria is the host’s age. The main rumen bacteria, for example, differ between newborn, 2-month-old, 6-month-old, and 2-year- old cows [21]. Climate, temperature, humidity, topography, and herd management are all factors that influence the rumen microbiota-host relationship. When a host gets ill, its gut microorganisms and microbial activities may alter from
Types of Ruminal Bacteria (Table 1)
those found in healthy animals [22].
Physiological and Anatomical Properties of the Rumen
The rumen is a complex ecosystem in which nutrients absorbed by microbes like bacteria, protozoa, and fungus and then digested anaerobically. The major end products of fermentation are VFAs and microbial biomass, which are utilized by the host ruminant. The environment in the rumen promotes microorganisms in providing the enzymes needed to digest the nutrients [23]. The functional health of the reticle-rumen is a necessary condition for productive behaviour, which includes cattle health and animal welfare [24].
Ruminants have the ability to transform low-quality fibrous resources into human-useful goods like meat and milk. Ruminal microorganisms’ capacity to manufacture the enzymes required for fermentation processes enables ruminants to acquire the energy contained in forages more effectively [23], in contrast the ruminal fermentation process is inefficient since it generates various byproducts such as methane gas (Kingston-Smith et al., 2012) and excess ammonia [25].
Ruminants’ anatomical adaption allows them to utilize cellulose as an energy source without requiring external supplies of vitamin B complex or critical amino acids since ruminal bacteria may manufacture such products [25, 26]. The ruminant host receives nutrients from the bacteria to produce energy [27]. The ruminant digestive system is made up of four parts: the reticulum, the rumen, the omasum, and the abomasum. The rumen is primarily where the fermentation activities take place [28]. Microorganisms create the enzymes found in the rumen, which are needed to digest and ferment the food consumed by ruminants; consequently, the rumen is seen as a fermentation vat [29].
| Type of bacteria | Microorganism | Impact | Reference |
|---|---|---|---|
| Cellulose- degrading bacteria | Butyrivibrio fibrisolvens, Ruminococci albus, and Fibrobacter succinogenes | Essential for animal nutrition because they break down cellulose, this makes up the majority of these plants’ cell walls. | [30-32] |
| Lipolytic bacteria | Anaerovibrio lipolytica | Hydrolyze the lipids in the rumen, and breaking the ester bonds and releasing fatty acids. | [33] |
| Lactate-degrading bacteria | Selenomonas lactilytica and Megasphaera elsdenii | Metabolize lactic acid and limit its buildup, which helps to keep the pH in the right range. | - |
| Pectin-degrading bacteria | Lachnospira multiparus | Create and release pectinolytic enzymes into the ruminal environment. | [34] |
| Amylolytic bacteria | Bacteriodes ruminicola, Ruminobacter amylophilus , Selenomonas ruminantium, Succinomonas amylolítica and Streptococci bovis | Produce other VFAs such as formate, acetate, propionate, and succinate, and ferments glucose to provide acetate, formate, and ethanol as a final product. | [35-37] |
| Lactic acid- utilizing bacteria | Megasphaera elsdenii | Is the main species responsible for lactic acid metabolization; thus, it has an important role in the prevention of acidosis during the adaptation period when ruminants are fed diets high in concentrate. | [38] |
Table 1: The most common ruminal bacteria.
The ruminal ecosystem is made up of a diverse group of microorganisms that live in a symbiotic interaction in an anaerobic environment [39]. Ruminal bacteria, protozoa, and fungus make up the microbiota and bacterial populations are particularly sensitive to the rumen’s physicochemical features [36]. Bacteria, which make up the bulk of microorganisms that survive in anaerobic environments, are found in the rumen [40].
Function and Importance of the Rumen
Because the host is unable to manufacture cellulolytic enzymes, the microbiota is primarily responsible for complicated polysaccharide breakdown. Many microorganisms interact to digest complex substrates such as cellulose, starch, and proteins, resulting in energy, protein, and vitamins accessible to the host [41]. The most prevalent microorganisms in the rumen are bacteria [42] and also the rumen microbiota is mostly composed of bacteria [43]. Manipulation of microbiota has been explored in order to increase energy harvesting, minimize methane emissions, and prevent and cure rumen disorders [44, 45].
There are several methods for manipulating the ruminal microbiota, including probiotics, prebiotics, antibiotics, and microbiota transfaunation, which involves transferring rumen fluid from one animal (donor) to another. The ruminal microbiota is relatively stable in adult animals, owing to two factors: redundancy, which is the ability of numerous microbial species to perform the same job, and resilience, which is the ability to rebound from a disruption [46].
Impact of Ruminal Juice Transfauntion
Rumen microbiota transfaunation has long been employed by veterinarians and is commonly advised to restore ruminal equilibrium [47, 48]. Transfaunation has been demonstrated to aid cows suffering from abomasum displacement [11, 49], abomasum impaction, gangrenous mastitis [50] and dysbiosis (abnormalities in the normal microbiota composition) induced by antibiotic therapy [51]. However, Tankersley, et al. [52] reported that, the technique did not improve blood metabolites, reproductive performance, or the incidence of illnesses following calving. Interspecies rumen microbiota transfaunation (from bovine to small ruminants) has been demonstrated to promote a faster recovery of protozoa populations as well as physical qualities such as color, flavor, and consistency in sheep and goats with experimentally produced acute ruminal lactic acidosis [53, 54].
Impact of Ruminal Fluid Transfaunation on Nutrient Metabolism
As a result, ruminal microbiota is tightly correlated to host feed digestion and metabolism. Numerous studies have found that one or more types of ruminal microbiotas influence feed efficiency, nitrogen digestibility, and methane emission in ruminants [55, 56, 57]. In comparison to the reticulum, omasum, and abomasum, the adult rumen plays the most important role in the breakdown of ingested organic materials due to the presence of diverse bacteria. Rumen microorganisms can convert dietary carbohydrates to VFA, which can account for up to 80% of ruminant energy requirements [58]. Some rumen microorganisms also produce their own proteins for growth (referred to as microbial crude protein, MCP) by consuming energy and nitrogen from the meal. The MCP are digested and absorbed by the host in the small intestine, contributing to the host’s nutrition and wellbeing [27, 59]. Furthermore, certain microorganisms may create vitamins such as B and K. Numerous enzymes necessary for the production of vitamin B12 are present in rumen microorganisms but not in the human GIT microbiome [60].
Methanogens in the rumen, on the other hand, generate methane through a series of redox processes, and methane is a potent greenhouse gas [61]. As a result, rumen microorganisms have a high potential for contribution to animal husbandry, and some of them can be used in animal production [45]. The bacteria that live in the rumen impact the host metabolism by degrading dietary components, despite the fact that these microbes are not regarded to be host specific tissues. This microbiota assists in the digestion of the meal by secreting enzymes. The rumen microbiota has been shown to have an important effect on feed efficiency, milk output, and dairy cow components [56]. The role of microbial enzyme activity, for example, can enhance monosaccharide content [62]. Nitrogen and fiber digestion contribute significantly to feed efficiency, and it is also associated with rumen microorganisms that generate MCP and VFA for the host [59]. According to one study, Fibrobacter succinogenes, Butyrivibrio fibrisolvens, and Ruminococcus sp. are the most important ruminal bacterial species in terms of nitrogen use by the host [63]. Toll-like receptors (TLRs) in the epithelium, for example, may detect lipopolysaccharide and lipoprotein breakdown products from bacteria [64]. When TLR4, TLR5, and TLR9 are activated by lipopolysaccharide, the host secretes bacterial flagellin and other bioactive molecules (such as cholecystokinin), which alter dietary nitrogen digestion and absorption.
A recent study discovered that some bacteria impeded the digestion of neutral detergent fiber (NDF) in goats [65]. Several bacterial phyla, including Proteobacteria, and Tenericutes, as well as a few bacterial species, including Anaeroplasma, Campylobacter, and Clostridium, are also associated with apparent crude fiber digestibility in pigs [66]. Cellulolytic microorganisms are among the most common bacteria in the rumen, they influence host fiber digestibility by secreting cellulose and controlling VFA production and profile. Furthermore, VFA can both give energy and regulate the host’s intestinal barrier function. In its current form, transfaunation refers to the transfer of microorganisms such as bacteria, protozoa, fungus, and archaea from the rumen of a donor to the rumen of a recipient [67].
Medicinal Functions of Ruminal Transfaunation
Rumen transfaunation was later utilized as a therapy to improve calf health. Rumen transfaunation enhanced calf health and survival in a field research with a herd experiencing bloody diarrhea and the loss of preweaned calves [68]. Transfaunation is the technique of transferring rumen fluid containing microorganisms and nutrients from healthy animals into animals with poor rumen digestion. This procedure is thought to enhance rumen function and has been used as a biotic therapy for ketosis, anorexia, and numerous causes of dyspepsia such as rumen acidosis. As indicated in the review by Depeters and George [1], this procedure is recommended in various text books and practical guides on bovine medicine.
Simple Indigestion
Sudden changes in food contents can cause anorexia in ruminants [69], which is reflected in rumen pH alterations [70]. Anorexia (decrease in appetite) with ruminal hypo motility to atony (stasis) is a clinical indication of uncomplicated dyspepsia in dairy calves [70, 71]. Sudden changes in dietary components can cause anorexia in ruminants [69], which is reflected in variations in rumen pH (Merck and Co, 2010). Ruminal fluid transfaunation from a healthy donor animal to an animal suffering from mild indigestion is a widely suggested technique for dairy cattle and other ruminants [72]. Rumen transfaunation was found to be advantageous for sheep employed in biomedical research that had minor indigestion [72].
In their biomedical research, sheep were administered pelleted diets, which contributed to the development of subclinical rumen acidity. Ruminal fluid transfaunation successfully treated uncomplicated indigestion in sheep [72], furthermore improves cow health after calving, milk output, and animal health in a well-managed herd [52]. Transfaunation or refaunation is a popular medical treatment in animal medicine to cure ruminant indigestion [73].
Displaced Abomasum
Ruminal fluid transfaunation was employed as an adjuvant therapy after surgery, and cows were transfaunated following surgical correction of a left-displaced abomasum, treatments were administered immediately following surgery and again on the first postoperative day [11]. Ruminal fluid transfaunated cows showed greater dry matter intake and milk output compared to control cows on day 2 following surgery and for the next three days. Serum concentrations of B-hydroxybutyrate on days 3 and 5 post- surgery were considerably lower in transfaunated cows than control cows. Administration of rumen fluid to cows convalescing following surgical correction of left displaced abomasum showed favorable benefits [11].
Plant Intoxicants
Mimosine (amino-B-(N-[3-hydroxy-4-pyridone]) propionic acid) is a poisonous amino acid found in plants of the genera Leucaena and Mimosa [74, 75]. Mimosine inhibits protein synthesis and, when taken long-term by animals, results in decreased hair growth and loss with suspected antimitotic action. Mimosine was metabolized in the rumen to 3-hydroxy-4-pyridone [75]. The rumen microbiota in cattle and goats was capable of degrading mimosine but not its hazardous metabolite, 3, 4-dihydroxy pyridine. Leucaena, on the other hand, was not hazardous to ruminants because rumen microorganisms could breakdown both mimosine and 3, 4-dihydroxy pyridine [76]. Recently, rumen fluid from goats containing rumen bacteria capable of digesting sodium monofluoroacetate, a poisonous chemical found in Amorimia spp., ruminal transfaunation was utilized in order to prevent animal poisoning [77].
Tannins are polyphenolic chemicals found in plants and also they are antibacterial to some microbes and have been demonstrated to lower methane generation in sheep and goats [78]. Tannin intake can also be detrimental to animal health [79]. Tannins bind proteins, and research is being conducted to harness this binding feature to minimize protein breakdown in the rumen in order to improve nitrogen consumption by ruminants [80] and to prevent bloat in cattle grazing alfalfa [78].
Acidosis
It is generally recognized that ruminants’ rumens serve as critical sites for digestion and metabolism, and that the ruminal bacteria play a crucial role in these processes [81]. Ruminant health is significantly impacted by changes in the structure and function of the ruminal microbiota [82]. Ruminal acidosis can be caused by intake of fine particle size (diameter smaller than 0.07 in.) or highly concentrated feeds containing quickly fermented carbohydrates [83]. Such diets necessitate less chewing, resulting in reduced saliva production, which reduces buffering capacity [84]. Consumption of quickly digested carbohydrates increases rumen VFA production, as a result, lactic acid production. As a result, ruminal pH drops and the ruminal fauna shifts from primarily gram-negative to gram-positive organisms [85].
This illness is characterized clinically by ruminal atony, in appetence, and lethargy [86]. Transfaunation is the process of introducing healthy protozoa, VFA, and gram- negative bacteria from a clinically normal ruminant into the rumen of an in appetent sheep in order to repopulate the ruminal fauna and correct the pH. Transfaunation is commonly used to treat ruminal atony and anorexia in ruminant animals [11, 86]. Acute or clinical acidosis occurs when the ruminal pH goes below 5.0. Clinical symptoms may include decreased salivation, lethargy, decreased gastrointestinal motility, anorexia, and diarrhea [87]. Acute rumen acidosis represents an economically significant loss to the beef and milk production business. Ruminants have a complex stomach system, with the stomach being separated into four compartments, the biggest of which is the rumen. Clinical rumen acidosis is still the principal cause of illness and death in current ruminant production systems [71]. Reticulum-rumen function, which includes cattle health and animal welfare, is a necessary condition for productive behaviour [24].
Clinical ruminal acidosis occurs when the rumen’s fluid pH falls below 5.2 as a result of an excessive buildup of organic acids [88, 89]. The classic situation leading to clinical rumen acidosis is excessive feeding of quickly fermentable carbohydrates, sometimes known as “grain overload”. Excess grain consumption is not required for the development of the syndrome because any rapidly fermentable carbohydrate (apples and other fruits, bakery waste products, incompletely fermented brewery products, and standing green corn) can provide the necessary substrate for clinical disease development [71]. When the rate of generation of VFA and lactate exceeds the rate of absorption, the pH of the rumen begins to fall. Volatile fatty acids and lactate accumulate in the rumen fluid and are absorbed into the systemic circulation [90].
Previous research showed that ruminal acidosis, a typical ruminal digestive problem in dairy or beef cattle given large levels of readily fermentable carbohydrates can disrupt ruminal microbial homeostasis and rumen epithelial function and, finally, result in noticeable decreases in animal performance, which results in significant financial losses and adversely impacts the sustainability of the ruminant sector [88]. Ruminant scientists agree that restoring ruminal bacterial equilibrium with rumen acidosis would aid rumen function recovery [91, 92]. Ruminal transfaunation is a practical approach in production in which ruminal fluid containing healthy microbial flora and buffer systems is transferred from a healthy donor to receptors suffering from rumen disease [1]; it is also regarded a routine and successful treatment to rumen acidosis in bovine production systems.
A study looked at the benefits of ruminal transfaunation for sheep with ruminal acidosis and discovered that the sheep who received ruminal transfaunation recovered to normal health [72]. However, there is a scarcity of data on the dynamic changes in rumen fermentation and bacterial populations that occur after ruminal transfaunation in sheep with rumen acidosis, as well as its favorable effects on rumen epithelial shape and function [1].
Effect of Ruminal Transfauntion on Fattening Lambs
Ruminal transfaunation improved the mean blood levels of IgA and IL-6 in weaned lambs compared to control animals, however, it has lowered growth performance, nutritional digestibility, and feed intake [12]. Contrasting to previous research, transfection of gastrointestinal microbiota prevented rumen acidosis in sheep and reduced gut barrier damage in young piglets [14, 65]. Research with calves suggests that ruminal transfauntion may not be suitable for lambs during weaning and that fast changes in the gut flora during weaning may be hazardous [13].
Effect of Ruminal Transfauntion on Gastrointestinal Microbiota of Fattening Lambs
In order to provide the host with nutrients and energy, the symbiotic bacteria in the rumen breaks down the food that is consumed and breaks down plant components into various VFAs and ammonia. This process improves digestion. Therefore, increased sheep feed efficiency and therefore production may result from improved rumen microbial digestive capabilities. Various methods have been used in the past to reroute the rumen microbiota, such as altering animal diets [6], lowering rumen pH [4], and reducing rumen protozoa numbers [5]. Microbial transplantation has been considered as one of the potential approaches for remodelling the symbiotic microbiota in small animals [93, 94, 95, 96]. The recipient cows’ fermentation characteristics recovered to their former state immediately after transplanting [97], and their bacterial profiles returned to their original state, demonstrating that the host has a major influence on rumen microbiota re-establishment. In cows with dysbiosis brought on by antibiotics, tranfaunations improved richness and diversity, and the donors’ microbiota was able to invade the rumen [51]. In the same time, patients with dysbiosis brought on by antibiotic usage and Clostridium difficile infection can also greatly benefit from faecal microbiota transplantation in humans [98].
Compared to control animals receiving water, transfaunation given to lambs throughout their early lives improved the bacterial diversity [99]. After weaning, the gastrointestinal environment changes, creating opportunities for particular bacteria species to grow. This progressively alters the microbiota, and utilizing ruminal transfaunation to transfer a mature microbiome to the rumen just accelerates up this process [65, 100, 101].
There were no apparent changes in the pH of rumen fluid between control and transfaunated cows at any point of time, although the two groups’ pHs were more suited to rumen digestion during the course of the experiment than those of the non-transfaunated group [102]. The fermentation of the ingested food by the ruminant is entirely dependent on the microbial community [103, 104]. Most of the energy and protein required by the host are supplied by the fermentation process, mostly in the form of short chain fatty acids (SCFAs) and microbial proteins [46]. Microbial colonization may be influenced by a number of parameters, including nutrition and the environment [105]. When the microbiota is less stable and more basic, these adjustments can be more noticeable in subsequent colonization cycles [106]. A diversified and established microbial community in the rumen is more durable and resistant to disturbances as compared to less developed ecosystems.
When the disturbance is removed, the microbiota’s composition and function tend to recover to pre-treatment levels [107, 108]. However, in juvenile ruminants, the impact of modifications may last for some time after the modification is completed. Saro, et al. [106] showed that a long-term early life treatment may influence the composition of the rumen microbial community and that this effect can last for weeks after the intervention. Abecia, et al. [109] demonstrated that the treatment effect lasted after the alteration was removed in the early life of baby goats. Currently, numerous methods for influencing rumen fermentation through early life microbiota have been investigated, including diet types [110], weaning technique [111], rumen fluid inoculation [112], and different additives [106, 113].
Effect of Ruminal Transfauntion on Production Performance of Fattening Lambs
Effect of Ruminal Transfauntion on Body Weight and Body Weight Gain: Microbial transplantation has been considered as one of the potential approaches for modifying host performance and remodelling the symbiotic microbiota in small animals [93, 94, 95, 96]. Rumen fluid transplantation in fattening lambs decreased average daily gain in live weight and apparent digestibility of ether extract in 3 month old fattening lambs, and it decreased apparent digestibility of NDF and ADF in one year old lambs [12]. Yin, et al. [12] reported that the initial and final live weights were similar in the 3 month and one year fattening lambs exposed to ruminal fluid transfaunation in comparison with controls.
Effect of ruminal transfauntion on feed intake and feed conversion ratio: The feed intakes of transfaunated cows were higher than those of the non transfaunated ones; appetite differences may have contributed to the variability of rumen protozoa, pH values. Cows that received rumen fluid had significantly greater feed intakes, significantly greater daily milk yields, and significantly lower rumen fluid acidity. Because non-transfaunated animals subjected to indigestion after consuming concentrate may have rumen fluid pH that is low for several weeks [102]. However, rumen fluid transplantation in fattening lambs decreased average feed intake in 3 month old fattening lambs compared to control lambs [12]. On the other hand, cows that received rumen fluid had much higher feed intakes, higher daily milk outputs, and significantly lower rumen fluid acidity; furthermore, transfaunated cows also had significantly higher feed intakes than non-transfaunated cows [11].
Furthermore, rumen transfaunation enhanced the dry matter intake of treated bulls above deionized water-treated bulls [114]. Ruminant scientists agree that recovering the microbiota in the rumens of stressed and travelled cattle quickly results in enhanced animal health and performance following transportation [92]. After transportation, the bulls given 10 kg of rumen fluid consumed more feed than the control group [114]. Also, according to Galbat and Keshta [102], cows in the transfaunated group consumed much more feed on a daily and cumulative basis and produced significantly more milk than cows in the non-transfaunated group. In cattle, the feed intake improved as a result of the rumen fluid treatment. When compared to the control group, animals that received 1 liter of rumen fluid consumed considerably more feed on days 1 and 4 after ruminal transfusion [115]. Compared to the transfaunated cows, cows in the non-transfaunated group showed a lower protozoal counts and activity as well as reduced milk output [102].
Effect of Ruminal Transfauntion on Antioxidant Activity of Fattening Lambs
Free radicals, including reactive oxygen and nitrogen species (ROS and RNS), are chemically reactive substances that may destroy macromolecules including lipids, carbohydrates, proteins, and nucleic acids by oxidative damage [116]. Antioxidants help prevent cell deterioration by lowering free radicals [117]. In healthy animals, there is a balance between free oxygen radicals and the protective antioxidant system. Oxidative stress is the term used to describe the shift in the antioxidant system’s favoring of oxidants over free radicals. In many diseases, oxidative stress contributes to cellular and molecular tissue damage [116]. Malondialdehyde (MDA), the final product of lipid peroxidation, enzymatic antioxidants such as superoxide dismutase, glutathione peroxidase, and catalase, non-enzymatic antioxidants such as reduced glutathione, vitamins C and E, total antioxidant capacity (TAC), and total oxidant status (TOS) are all commonly used markers in determining oxidative stress in sheep [118].
The determination of oxidative stress has recently become significant in clinical practice as a complementing component [119]. Shearing has been shown to cause a considerable rise in blood MDA values, indicating the presence of oxidative stress in sheep [120]. The antioxidant indicators’ blood levels were unaffected by ruminal transfaunation, however, among the intestinal permeability indicators, the mean serum level of D-lactate dehydrogenase was greater in both ruminal transfaunation groups than in the control group [12].
Effect of Ruminal Tansfauntion on Immune Response of Fattening Lambs
When it comes to immunoglobulins in the weaned lambs, the ruminal transfaunation group’s mean blood levels of IgA and IL-6 were greater than those of the control groups in comparison [12]. Researchers found that the activation or inhibition of Toll-like receptor (TLR) by microbial signals in humans might influence the modulation of immune responses [121]. As a result, it was hypothesized that rumen microorganisms are critical for the development and control of the neonatal immune system, and that rumen microbes play an important role in sustaining long-term health and production. Malmuthuge, et al. [122] discovered that the gut microbiota and mucosal immune activities of lambs fed MR (milk replacer) or MR+S (milk replacer + starter) changed throughout the weaning transition. For ruminants, the earliest microbial sources and profiles may be essential in determining the microbe-immune system interaction and its implications for adult health in the early postnatal period. For weaned lambs, ruminal transfaunation has improved immunological and inflammatory reactivity [12].
Effect of Ruminal Transfauntion on Mortality of Fattening Lambs
Stresses such as decreased food digestibility, leaky gut epithelia, or immunological dysfunction can all cause an increase in morbidity and mortality during the weaning phase [123]. Post-weaning care of lambs is a prevalent problem, as evidenced by a 4.6 percent post weaning death rate for sheep [124]. As the animals adjust to solid diet during weaning, the gut microbiota progressively changes. This reconfiguration of the microbiota may increase the stress associated with weaning [125]. According to several studies like Blanton, et al. [126], Charbonneau, et al. [127], and Ahern and Maloy, [128], it involved a variety of interactions between bacteria that affect feed digestion, gastrointestinal integrity, and immunological reactivity [129]. Ruminal transfaunation may not be appropriate for lambs during weaning, and research with calves suggests that fast changes in the gut microbiota during weaning may be hazardous [125, 126, 127, 128, 129, 130, 131, 132, 133, 134, 135, 136].
Conclusion
Finally, it is important to mention that intervention strategies to improve the production performance and health of fattening lambs have been the focus of many published studies, which apply different approaches, including nutritional manipulation (i.e., pelleting of the total mixed ratio and diet formulation according to the metabolic condition of the lambs), as well as dietary supplementation of feed additives in the diet (e.g., prebiotics, synbiotics, probiotics, vitamins, minerals, etc.), improving of genetic traits of sheep by different methods such as selection, presenting fresh sires, inbreeding, crossbreeding and formation of new breed. Nevertheless, effectiveness of most of the interventions has been variable or inconsistent. More recently, innovative approaches have been explored, including reshaping the ruminal microbiome by ruminal transfaunation. However, no one of the previously mentioned methods has shown harmonic positive effects, indicating that the previously mentioned methods to improve animal health and production performance by reshaping the symbiotic microbiota have not been achieved yet and still need further research and study.
References
-
DePeters EJ, George LW (2014) Rumen transfaunation. Immunol Lett 162(2 Pt A): 69-76.
-
Falony G, Joossens M, Silva SV, Wang J, Darzi Y, et al. (2016) Population-level analysis of gut microbiome variation. Science 352(6285): 560-564.
-
Zhong RZ, Fang Y, Zhou DW, Sun XZ, Zhou CS, et al. (2018) Pelleted total mixed ration improves growth performance of fattening lambs. Animal Feed Science and Technology 242: 127-134.
-
Bevans DW, Beauchemin KA, Genswein KSS, McKinnon JJ, McAllister TA (2005) Effect of rapid or gradual grain adaptation on subacute acidosis and feed intake by feedlot cattle. J Anim Sci 83(5): 1116-1132.
-
Mosoni P, Martin C, Forano E, Morgavi DP (2011) Long- term defaunation increases the abundance of cellulolytic ruminococci and methanogens but does not affect the bacterial and methanogen diversity in the rumen of sheep. J Anim Sci 89(3): 783-791.
-
Wright AD, Franzolin R, St-Pierre B, Northwood K (2012) Analysis of rumen methanogen diversity in water buffaloes (Bubalus bubalis) under three different diets. Microbial Ecology 64: 131-139.
-
Mohammed A, Mahmoud M, Murugesan R, Cheng HW (2021) Effect of a synbiotic supplement on fear response and memory assessment of broiler chickens subjected to heat stress. Animals (Basel) 11(2): 427.
-
D’Argenio V, Salvatore F (2015) The role of the gut microbiome in the healthy adult status. Clinica Chimica Acta 451(Pt A): 97-102.
-
Sommer F, Anderson J, Bharti R (2017) The resilience of the intestinal microbiota influences health and disease. Nature Reviews Microbiology 15: 630-638.
-
Liu K, Wang L, Yan T, Wang Z, Xue B, et al. (2019) Relationship between the structure and composition of rumen microorganisms and the digestibility of neutral detergent fibre in goats. AJAS 32(1): 82-91.
-
Rager KD, George LW, House JK, DePeters EJ (2004) Evaluation of rumen transfaunation after surgical correction of left-sided displacement of the abomasum in cows. J Am Vet Med Assoc 225(6): 915-920.
-
Yin X, Ji S, Duan C, Ju S, Zhang Y, et al. (2021) Rumen fluid transplantation affects growth performance of weaned lambs by altering gastrointestinal microbiota, immune function and feed digestibility. Animal 15(1): 100076.
-
Meale SJ, Li SC, Azevedo P, Derakhshani H, DeVries TJ, et al. (2017) Weaning age influences the severity of gastrointestinal microbiome shifts in dairy calves. Sci Rep 7(1): 198.
-
Cheng SS, Ma X, Geng SJ, Jiang XM, Li Y, et al. (2018) Fecal microbiota transplantation beneficially regulates intestinal mucosal autophagy and alleviates gut barrier injury. mSystems 3(5): e00137-e00218.
-
Matthews C, Crispie F, Lewis E, Reid M, O’Toole PW, et al. (2019) The rumen microbiome: a crucial consideration when optimising milk and meat production and nitrogen utilisation efficiency. Gut Microbes 10(2): 115-132.
-
Mccann JC, Wickersham TA, Loor JJ (2014) High- throughput methods redefine the rumen microbiome and its relationship with nutrition and metabolism. Bioinform Biol Insights 8: 109-125.
-
Ishler AV, Heinrichs J, Varga G (1996) Understanding rumen function. From feed to milk, pp: 1-27.
-
Auffret MD, Dewhurst RJ, Duthie CA, Rooke JA, Wallace RJ, et al. (2017) The rumen microbiome as a reservoir of antimicrobial resistance and pathogenicity genes is directly affected by diet in beef cattle. Microbiome 5: 159.
-
Liu K, Xu Q, Wang L, Wang J, Guo W, et al. (2017) The impact of diet on the composition and relative abundance of rumen microbes in goat. AJAS 30(4): 531-537.
-
Pandit RJ, Hinsu AT, Patel SH, Jakhesara SJ, Koringa PG, et al. (2018) Microbiota composition, gene pool and its expression in Gir cattle ( Bos indicus ) rumen under different forage diets using metagenomic and metatranscriptomic approaches. Systematic and Applied Microbiology 41(4): 374-385.
-
Jami E, Israel A, Kotser A, Mizrahi I (2013) Exploring the bovine rumen bacterial community from birth to adulthood. ISME J 7(6): 1069-1079.
-
Clavel T, Neto JCG, Lagkouvardos I, Tait AER (2017) Deciphering interactions between the gut microbiota and the immune system via microbial cultivation and minimal microbiomes. Immunol Rev 279(1): 8-22.
-
Burns JC (2008) ASAS Centennial Paper: Utilization of pasture and forages by ruminants: a historical perspective. J Anim Sci 86(12): 3647-3663.
-
Van Vuuren AD, Calsamiglia S, Uden P (2012) Rumen health: A 360° analysis. Animal Feed Science Technology 172(1-2): 1-3.
-
Russell JB, Mantovani HC (2002) The bacteriocins of ruminal bacteria and their potential as an alternative to antibiotics. J Mol Microbiol Biotechnol 4(4): 347-355.
-
Cole NA, McLaren JB, Hutcheson DP (1982) Influence of Preweaning and B-Vitamin Supplementation of The Feedlot Receiving Diet on Calves Subjected to Marketing and Transit Stress. J Anim Sci 54(5): 911-917.
-
Russell JB, Rychlik JL (2001) Factors that alter rumen microbial ecology. Science 292(5519): 1119-1122.
-
Tharwat MF, Al-Sobayil A, Buczinski S (2012) Transabdominal ultrasonographic appearance of the gastrointestinal viscera of healthy camels (Camelus dromedaries). Research in Veterinary Science 93(2): 1015-1020.
-
Aschenbach JR, Penner GB, Stumpff F, Gäbel G (2011) Ruminant nutrition symposum: Role of fermentation acid absorption in the regulation of ruminal pH. J Anim Sci 89(4): 1092-1107.
-
Ivan M, Petit HV, Chiquette J, Wright ADG (2013) Rumen fermentation and microbial population in lactating dairy cows receiving diets containing oilseeds rich in C-18 fatty acids. Br J Nutr 109(7): 1211-1218.
-
Doreau BM, Fernandez I, Fonty G (2002) A comparison of enzymatic and molecular approaches to characterize the cellulolytic microbial ecosystems of the rumen and the cecum. J Anim Sci 80(3): 790-796.
-
Weimer PJ (1996) Why Don’t Ruminal Bacteria Digest Cellulose Faster? Journal of Dairy Science 79: 1496- 1502.
-
Fuentes MC, Calsamiglia S, Cardozo PW, Vlaeminck B (2009) Effect of pH and level of concentrate in the diet on the production of biohydrogenation intermediates in a dual-flow continuous culture. J Dairy Sci 92(9): 4456- 4466.
-
Duskova D, Marounek M (2001) Fermentation of pectin, glucose and activity of pectin-degrading enzymes in the rumen bacterium Lachnospira multiparus. Lett Appl Microbiol 33(2): 159-163.
-
Cotta MA (1988) Amylolytic activity of selected species of ruminal bacteria. Appl Environ Microbiol 54(3): 772- 776.
-
McAllister TA, Rode LM, Major DJ, Cheng KJ, Smith JGB (1990) Effect of ruminal microbial colonization on cereal grain digestion. Can J Anim Sci 70: 571-579.
-
Cotta MA (1992) Interaction of ruminal bacteria in the production and utilization of maltooligosaccharides from starch. Appl Environ Microbiol 58(1): 48-54.
-
Counotte GH, Prins RA (1981) Regulation of lactate metabolism in the rumen. Vet Res Commun 5(2): 101- 115.
-
Ozutsumi Y, Hayashi H, Sakamoto M, Itabashi H, Benno Y (2005) Culture-Independent Analysis of Fecal Microbiota in Cattle. Bioscience, Biotechnology, and Biochemistry 69(9): 1793-1797.
-
Pitta DW, Pinchak E, Dowd SE, Osterstock J, Gontcharova V, et al. (2010) Rumen bacterial diversity dynamics associated with changing from bermudagrass hay to grazed winter wheat diets. Microb Ecol 59(3): 511-522.
-
Russell JB, Muck RE, Weimer PJ (2009) Quantitative analysis of cellulose degradation and growth of cellulolytic bacteria in the rumen. FEMS Microbiol Ecol 67(2): 183-197.
-
Choudhury PK, Salem AZM, Jena R, Kumar S, Singh K, et al. (2015) Rumen microbiology: an overview. In: Puniya AK, et al. (Eds.), Rumen Microbiology: From Evolution to Revolution. Springer, New Dehli, India, 322: 3-16.
-
Williams AG, Coleman GS (1991) The Rumen Protozoa. The Journal of Eukaryotic Microbiology 42(1): 75.
-
Malmuthuge N, Guan LL (2017) Understanding host- microbial interactions in rumen: searching the best opportunity for microbiota manipulation. J Anim Sci Biotechnol 8: 1-8.
-
McCann JC, Elolimy AA, Loor JJ (2017) Rumen microbiome, probiotics, and fermentation additives. Vet Clin North Am Food Anim Pract 33(3): 539-553.
-
Weimer PJ (2015) Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations. Frontier in Microbiology 6: 296.
-
Brag S, Hansen HJ (1994) Treatment of ruminal indigestion according to popular belief in Sweden. Rev Sci Tech 13(2): 529-535.
-
Garry F, McConel C (2015) Indigestions in ruminants. In: Smith BP (Ed.), Large Animal Internal Medicine. Elsevier, Missouri, pp: 777-798.
-
Camara ACL, Afonso JAB, Costa NA, Mendonça CL, Souza MI, et al. (2010) Risk factors, clinical and laboratory findings and therapeutic evaluation in 36 cattle with displaced abomasum. Brazilian Journal of Veterinary Research and Animal Science 30: 453-464.
-
Rizzo H, Dantas AC, Guimaraes JA, Melo LHE, Oliveira CCM, et al. (2015) Clinical-surgical treatments of unilateral gangrenous mastitis in goats due to different types of scarring. Full Scientia 11(4): 1-9.
-
Ji S, Jiang T, Yan H, Guo C, Liu J, et al. (2018) Ecological restoration of antibiotic-disturbed gastrointestinal microbiota in foregut and hindgut of cows. Front Cell Infect Microbiol 8: 79.
-
Tankersley NS, DePeters EJ, Graham TW (2007) Case study: effects of water, fresh cow YMCP plus, and rumen fluid transfaunate supplementation following calving on milk yield, reproductive efficiency, and incidence of common health disorders in holstein cows. The Professional Animal Scientist 23: 513-520.
-
Leal MLR, Maruta CA, Ortolani EL (2007) Use of bicarbonate and L-lactate to correct systemic metabolic acidosis in cattle with acute ruminal lactic acidosis. Arq Bras Med Vet Zootec 59(4): 971-976.
-
Pereira PFV, Romao FTN, Penzeti EM, Sanches JFZ, Curti JM, et al. (2018) Value of transfaunation for the treatment of induced ruminal lactic acidosis in goats and sheep. Pesq Vet Bras 38(4): 670-678.
-
Wang H, Zheng H, Browne F, Roehe R, Dewhurst RJ, et al. (2017) Integrated Metagenomic Analyses of the Rumen Microbiome of Cattles Reveals Key Biological Mechanisms Associated with Methane Traits. Methods 124: 108-119.
-
Schären M, Frahm J, Kersten S, Meyer U, Hummel J, et al. (2018) Interrelations between the rumen microbiota and production, behavioral, rumen-fermentation, metabolic, and immunological attributes of dairy cows. Journal of dairy science 101(5): 4615-4637.
-
Elolimy AA, Arroyo JM, Batistel F, Iakiviak MA, Loor JJ (2018) Association of residual feed intake with abundance of ruminal bacteria and biopolymer hydrolyzing enzyme activities during the peripartal period and early lactation in Holstein dairy cows. J Anim Sci Biotechnol 9(1): 43.
-
Wolin MJ (1979) The rumen fermentation: a model for microbial interactions in anaerobic ecosystems. Advances in microbial ecology 3: 49-77.
-
Hall MB, Huntington GB (2008) Nutrient synchrony: Sound in theory, elusive in practice. J Anim Sci 86(Suppl 14): E287-E292.
-
Seshadri R, Leahy SC, Attwood GT, The KH, Lambie SC, et al. (2018) Cultivation and sequencing of rumen microbiome members from the Hungate1000 Collection. National biotechnology Journal 36(4): 359.
-
Patra A, Park T, Kim M, Yu Z (2017) Rumen methanogens and mitigation of methane emission by antimethanogenic compounds and substances. J Anim Sci Biotechnol 8: 1-13.
-
Ibrahim M, Anishetty S (2012) Ameta-metabolome network of carbohydrate metabolism: Interactions between gut microbiota and host. Biochem Biophys Res Commun 428(2): 278-284.
-
Wang L, Liu K, Wan Z, Xue B, Peng Q, et al. (2019) Bacterial community diversity associated with different utilization efficiencies of nitrogen in the gastrointestinal tract of goats. Frontier in microbial 10: 239.
-
Wells JM, Rossi O, Meijerink M, Van Baarlen P (2011) Epithelial crosstalk at the microbiota–mucosal 494 interface. Proceedings of the National Academy of Sciences 108 (Suppl 1): 4607-4614.
-
Liu J, Li H, Zhu W, Mao S (2019) Dynamic changes in rumen fermentation and bacterial community following rumen fluid transplantation in a sheep model of rumen acidosis: implications for rumen health in ruminants. FASEB J 33(7): 8453-8467.
-
Niu Q, Li P, Hao S, Zhang Y, Kim SW, et al. (2015) Dynamic distribution of the gut microbiota and the relationship with apparent crude fiber digestibility and growth stages in pigs. Sci Rep 5: 9938.
-
Hungate RE (1966) The rumen and its microbes. Academic Press, New York, USA.
-
Pounden WD, Hibbs JW (1949) Rumen inoculations in young calves. J Am Vet Med Assoc 114(862): 33-35.
-
Grunberg W, Constable PD (2009) Function and dysfuntion of the ruminant forestomach. In: Anderson DE, et al. (Eds.), Current veterinary therapy. Elsevier, pp: 12-19.
-
Merck (2010) Merck veterinary manual. 10th(Edn.), Merck Manuals, NJ, USA, 8: 199-200.
-
Radostits OM, Gay CC, Blood DC, Hinchcliff KW (2000) Bovine mastitis: In: Constable P, et al. (Eds.), Veterinary Medicine a Textbook of the Diseases of Cattle, Sheep, Pigs, Goats and Horses. 9th(Edn.), WB Saunders Company Ltd, London.
-
Jasmin BH, Boston RC, Modesto RB, Schaer TP (2011) Perioperative ruminal pH changes in domestic sheep (Ovis aries) housed in a biomedical research setting. J Am Assoc Lab Anim Sci 50(1): 27-32.
-
Smith BP (2014) Large animal internal medicine. 4th(Edn.), Elsevier Health Sciences.
-
Jones RJ, Megarrity RG (1986) Successful transfer of DHP- degrading bacteria from Hawaiian goats to Australian ruminants to overcome the toxicity of leucaena. Aust Vet J 63(8): 259-262.
-
Soedarjo M, Hemscheidt TK, Borthakur D (1994) Mimosine, a toxin in leguminous trees (Leucaena spp.), induces a mimosine-degrading enzyme activity in some rhizobium strains. Applied Environmental Microbiology 60(12): 4268-4272.
-
Quirk MF, Bushnell JJ, Jones RJ, Megarrity RG, Butler KL (2009) Live-weight gains on leucaena and native grass pastures after dosing cattle with rumen bacteria capable of degrading DHP, a ruminal metabolites from leucaena. Journal Agriculture Science (Cambridge) 111(1): 165- 170.
-
Duarte AL, Medeiros RMT, Correa FR (2013) Poisoning by Amorimia spp. in ruminants. Ciência Rural Santa Maria 43(7): 1294-1301.
-
Patra AK, Saxena J (2011) Exploitation of dietary tannins to improve rumen metabolism and ruminant nutrition. J Sci Food Agric 91(1): 24-37.
-
Belenguer A, Hervás G, Ruiz DRY, Toral PG, Ezquerro C, et al. (2010) Preliminary study of the changes in rumen bacterial populations from cattle intoxicated with young oak (Quercus oyrenaica) leaves. Animal production science 50: 228-234.
-
Getachew G, DePeters EJ, Pittroff W, Putnam DH, Dandekar AM (2006) Review: does protein in alfalfa need protection from rumen microbes? The Professional Animal Scientist 22(5): 364-373.
-
Hoover WH, Stokes SR (1991) Balancing carbohydrates and proteins for optimum rumen microbial yield. J Dairy Sci 74(10): 3630-3644.
-
Wolin MJ (1981) Fermentation in the rumen and human large intestine. Science 213: 1463-1468.
-
Heinrichs J, Kononoff P (1996) Evaluating particle size of forages and TMRs using the Penn State particle size separator. College of Animal science 814: 1-14.
-
Sudweeks EM, Ely LO, Mertens DR, Sisk LR (1981) Assessing minimum amounts and form of roughages in ruminant diets: roughage value index system. Journal of Animal Science 53: 1406-1411.
-
Goad DW, Goad CL, Nagaraja TG (1998) Ruminal microbial and fermentative changes associated with experimentally induced subacute acidosis in steers. J Anim Sci 76(1): 234-241.
-
Smith BP (2009) Large animal internal medicine: diseases of the alimentary system. In: Murray MJ, (Eds.), Large animal internal medicine. 4th(Edn.), New York (NY), USA.
-
Slyter LL (1976) Influence of acidosis on rumen function. Journal of Animal Science 43: 910-929.
-
Owens FN, Secrist DS, Hill WJ, Gill DR (1998) Acidosis in cattle: a review. J Anim Sci 76(1): 275-286.
-
Nagaraja TG, Lechtenberg KF (2007) Acidosis in feedlot cattle. Vet Clin North Am Food Anim Pract 23(2): 333- 350.
-
Johnson B DVM (1991) Nutritional and dietary interrelationships with diseases of feedlot cattle. Veterinary Clinics of North America: Food Animal Practice 7(1): 133-142.
-
Cole NA, Hutcheson DP (1985) Influence of realimentation diet on recovery of rumen activity and feed intake in beef steers. J Anim Sci 61(3): 692-701.
-
Fluharty FL, Loerch SC, Dehority BA (1996) Effects of feed and water deprivation on ruminal characteristics and microbial population of newly weaned and feedlot- adapted calves. J Anim Sci 74(2): 465-474.
-
Manichanh C, Reeder J, Gibert P, Varela E, Llopis M, et al. (2010) Reshaping the gut microbiome with bacterial transplantation and antibiotic intake. Genome Res 20(10): 1411-1419.
-
Willing BP, Vacharaksa A, Croxen M, Thanachayanont T, Finlay BB (2011) Altering host resistance to infections through microbial transplantation. PLoS One 6: e26988.
-
Hamilton MJ, Weingarden AR, Unno T, Khoruts A, Sadowsky MJ (2013) High-throughput DNA sequence analysis reveals stable engraftment of gut microbiota following transplantation of previously frozen fecal bacteria. Gut Microbes 4(2): 125-135.
-
Liou AP, Paziuk M, Luevano JM, Machineni SJ, Turnbaugh PJ, et al. (2013) Conserved shifts in the gut microbiota due to gastric bypass reduce host weight and adiposity. Sci Transl Med J 5(178): 178ra41.
-
Weimer PJ, Stevenson DM, Mantovani HC, Man SL (2010) Host specificity of the ruminal bacterial community in the dairy cow following near-total exchange of ruminal contents. Journal of Dairy Science 93: 5902-5912.
-
Vrieze A, Nood EV, Holleman F, Salo J, Arvi J, et al. (2012) Transfer of intestinal microbiota from lean donors increases insulin. YGAST 143: 913-916.
-
Barbieri ID, Hegarty RS, Silveira C, Gulino LM, Oddy VH, et al. (2015) Programming rumen bacterial communities in newborn Merino lambs. Small Ruminant Research 129: 48-59.
-
Li SS, Zhu A, Benes V, Costea PI, Hercog R, et al. (2016) Durable coexistence of donor and recipient strains after fecal microbiota transplantation. Science 352(6285): 586-589.
-
Ji SK, Yan H, Jiang T, Guo CY, Liu JJ, et al. (2017) Preparing the gut with antibiotics enhances gut microbiota reprogramming efficiency by promoting xenomicrobiota colonization. Front Microbiol 8: 1208.
-
Galbat SA, Keshta HG (2020) Evaluation of rumen transfaunation after treatment of rumen acidosis in cows. Current Science International 9: 625-632.
-
Huws SA, Creevey CJ, Oyama LB, Mizrahi I, Denman SE, et al. (2018) Addressing global ruminant agricultural challenges through understanding the rumen microbiome: past, present, and future. Front Microbiol 9: 2161.
-
Morais S, Mizrahi I (2019) Islands in the stream: from individual to communal fiber degradation in the rumen ecosystem. FEMS Microbiol Rev 43(4): 362-379.
-
Zhu Z, Kristensen L, Difford GF, Poulsen M, Noel SJ, et al. (2018) Changes in rumen bacterial and archaeal communities over the transition period in primiparous Holstein dairy cows. Journal of Dairy Science 101: 9847- 9862.
-
Saro C, Hohenester UM, Bernard M, Lagree M, Martin C, et al. (2018) Effectiveness of interventions to modulate the rumen microbiota composition and function in pre- ruminant and ruminant lambs. Frontier in Microbiology 9: 1273.
-
Shade A, Peter H, llison SD, Baho DL, Berga M, et al. (2012) Fundamentals of microbial community resistance and resilience. Frontier in Microbiology 3: 417.
-
Kittelmann S, Patino CSP, Seedorf H, Kirk MR, Ganesh S, et al. (2014) Two different bacterial community types are linked with the low-methane emission trait in sheep. PLoS One 9(7): e103171.
-
Abecia LG, Fernandez GM, Waddams K, García AIM, Pinloche E, et al. (2018) Analysis of the rumen microbiome and metabolome to study the effect of an antimethanogenic treatment applied in early life of kid goats. Front Microbiol 9: 2227.
-
Zhang C, Li MM, Al-Marashdeh O, Gan LP, Zhang CY, et al. (2019) Performance, rumen fermentation, and gastrointestinal microflora of lambs fed pelleted or unpelleted total mixed ration. Animal Feed Science and Technology, 253: 22-31.
-
Mao H, Zhang Y, Yun Y, Ji W, Jin Z, et al. (2021) Weaning age affects the development of the ruminal bacterial and archaeal community in Hu lambs during early life. Front Microbiol 12: 636865.
-
Yu SB, Zhang GY, Liu ZB, Wu P, Yu ZT, et al. (2020) Repeated inoculation with fresh rumen fluid before or during weaning modulates the microbiota composition and co-occurrence of the rumen and colon of lambs. BMC Microbiol 20: 29.
-
Wang T, Jiao JX, Wang HC, Degen AA, Gou NN, et al. (2021) The effects of supplementing sweet sorghum with grapeseeds on dry matter intake, average daily gain, feed digestibility and rumen parameters and microbiota in lambs. Animal Feed Science and Technology 272: 114750.
-
Penu CLOL, Fitzpatrick LA, Zerby HN, Parker AJ (2016) Treating Bos indicus bulls with rumen transfaunation after 24 hours of transportation does not replete muscle glycogen. Animal Production Science 56(10): 1738-1744.
-
Steiner S, Linhart N, Neidl A, Baumgartner W, Tichy A, et al. (2020) Evaluation of the therapeutic efficacy of rumen transfaunation. Journal Animal Physiology and Animal Nutrition (Berl) 104(1): 56-63.
-
Ercan N, Fidancı UR (2012) Urine 8-hydroxy-2’- deoxyguanosine (8-OHdG) levels of dogs in pyoderma. Vet J 59(3): 163-168.
-
Kleczkowski M, Klucinski W, Sikora J, Zdanowicz M, Dziekan P (2003) Role of antioxidants in the protection against oxidative stress in cattle --nonenzymatic mechanism (Part 2). Pol J Vet Sci 6(4): 301-308.
-
Celli P (2010) The role of oxidative stress in small ruminants’ health and production. Revista Brasileira de Zootecnia 39: 348-363.
-
Castillo C, Hernandez J, Bravo A, Alonso ML, Pereira V, et al. (2005) Oxidative status during late pregnancy and early lactation in dairy cows. Vet J 169(2): 286-292.
-
Fidan AF, Kucukkurt I, Eryavuz A, Cigerci IH, Yardımcı M, et al. (2009) Effects of shearing procedures on oxidant antioxidant status in Chios sheep. Revue de Medecine Veterinaire 160(7): 349-355.
-
Spiljar M, Merkler D, Trajkovski M (2017) The immune system bridges the gut microbiota with systemic energy homeostasis: focus on TLRs, mucosal barrier, and SCFA. Frontier in immunology 8: 1353.
-
Malmuthuge N, Li M, Goonewardene LA, Oba M, Guan LL (2013) Effect of calf starter feeding on gut microbial diversity and expression of genes involved in host immune responses and tight junctions in dairy calves during weaning transition. J Dairy Sci 96(5): 3189-3200.
-
Moussaoui N, Jacobs JP, Larauche M, Biraud M, Million M, et al. (2017) Chronic early-life stress in rat pups alters basal corticosterone, intestinal permeability, and fecal microbiota at weaning: influence of sex. J Neurogastroenterol Motil 23(1): 135-143.
-
Campbell AJD, Broekhuizen A, Curtis K, Croker KP, Behrendt KP, et al. (2013) A survey of post-weaning mortality of sheep in Australia and its association with farm and management factors. Animal Production Science 54(6): 783-790.
-
Meale SJ, Li S, Azevedo P, Derakhshani H, Plaizier JC, et al. (2016) Development of ruminal and fecal microbiomes are affected by weaning but not weaning strategy in dairy calves. Front Microbiol 7: 582.
-
Blanton LV, Charbonneau MR, Salih T, Barratt MJ, Venkatesh S, et al. (2016) Gut bacteria that prevent growth impairments transmitted by microbiota from malnourished children. Science 351(6275): 10.
-
Charbonneau MR, O’Donnell D, Blanton LV, Totten SM, Davis JCC, et al. (2016) Sialylated milk oligosaccharides promote microbiota-dependent growth in models of infant undernutrition. Cell 164(5): 859-871.
-
Ahern PP, Maloy KJ (2020) Understanding immune- microbiota interactions in the intestine. Immunology 159(1): 4-14.
-
Cersosimo LM, Radloff W, Zanton GI (2019) Microbial inoculum composition and pre-weaned dairy calf age alter the developing rumen microbial environment. Front Microbiol 10: 1651.
-
Bruna PS, Bessegatto JA, Alfieri AA, Lisboa JAN, Weese JS, et al. (2021) Transfaunation of the ruminal fluid from cows alters ruminal microbiota structure but not dominant protozoa in healthy sheep. Small Ruminant Research 194: 106283.
-
Smith AHK, Marshall AH, Moorby JM (2013) Breeding for genetic improvement of forage plants in relation to increasing animal production with reduced environmental footprint. Animal 1: 79-88.
-
Malik MI, Rashid MA, Yousaf MS, Naveed S, Javed K, et al. (2021) Rumen morphometry and sorting behavior of fattening male goat fed pelleted and unpelleted TMR with two levels of wheat straw. Small Ruminant Research 196: 106316.
-
Constable P, Hinchcliff KW, Done S, Gruenberg W (2016) Veterinary Medicine. A Textbook of the Diseases of Cattle, Horses, Sheep, Pigs, and Goats, 1th(Edn.), Saunders Elsevier, Philadelphia 2.
-
Sasson G, Benshabat SK, Seroussi E, Doron- Faigenboim A, Shterzer N, et al. (2017) Heritable bovine rumen bacteria are phylogenetically related and correlated with the cow’s capacity to harvest energy from its feed. mBio 8(4): e703-00717.
-
Yu Z, Morrison M (2004) Improved extraction of PCR-quality community DNA from digesta and fecal samples. Biotechniques 36: 808-812.
-
Lin L, Xie F, Sun D, Liu J, Zhu W, et al. (2019) Ruminal microbiomehost crosstalk stimulates the development of the ruminal epithelium in a lamb model. Microbiome 7(1): 83.
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