J. Dairy Sci. 2007. 90:4346-4355. doi:10.3168/jds.2006-885
© 2007 American Dairy Science Association ®
Effect of Milk Allowance on Concentrate Intake, Ruminal Environment, and Ruminal Development in Milk-Fed Holstein Calves
N. B. Kristensen1,
J. Sehested,
S. K. Jensen and
M. Vestergaard
Department of Animal Health, Welfare and Nutrition, Faculty of Agricultural Sciences, University of Aarhus, DK-8830 Tjele, Denmark
1 Corresponding author: nbk{at}agrsci.dk
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ABSTRACT
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The aim of the present experiment was to test the hypothesis that a barley-based concentrate would induce an acidic ruminal environment in young calves and that increased milk allowance would alleviate this condition. Eight Holstein calves ruminally cannulated at d 7 ± 1 of age were used to study the effect of variation in barley-based starter concentrate intake induced by 4 different milk allowances (3.10, 4.84, 6.60, and 8.34 kg of milk replacer/d; 123 g of dry matter/kg of milk) on the ruminal environment, blood variables, and fore-stomach development from wk 2 to 5 of age. Twelve ruminal fluid samples were collected during a weekly 24-h sampling in 4 consecutive weeks. Blood samples were collected by venipuncture between 1200 and 1300 h on ruminal sampling days. Rumen papillae development and visceral organ mass were recorded at slaughter. A linear treatment x week effect was observed for concentrate intake, with the calves fed the lowest milk allowance having the fastest increase in concentrate intake whereby these calves reached the same ME intake in wk 5 compared with calves with the highest milk allowance. Effects on ruminal variables were dominated by week of sampling, with minor differences among treatments. Ruminal pH was below 5.5 for 5 to 13 h/d and all calves with concentrate intake above 20 g of dry matter/d were observed to have a daily ruminal pH minimum at pH 5.5 or lower. The ruminal concentration of total volatile fatty acids (VFA) increased from 71 to 133 ± 9 mmol/L in wk 2 to 5 and was characterized by a relatively high molar proportion of propionate, increasing from 34 to 40 mol/100 mol of VFA in wk 2 to 5. In addition, the presence of ethanol and propanol as well as numerous VFA esters points to a ruminal environment with a relatively high hydrogen pressure. Plasma glucose and insulin responded to the highest milk allowance in wk 2 to 4. Plasma VFA and ketone bodies increased with the lowest milk allowance in wk 4 to 5. At slaughter, empty wet weights of the rumen + reticulum and omasum as well as mass of digesta in these compartments were found to decrease linearly and perirenal fat was found to increase linearly with milk allowance, indicating that the milk allowance changed the body composition of the calves. Lengths of ruminal papillae in the atrium and ventral ruminal sac were not affected by treatment. We concluded that the ruminal environment of young calves fed a barley-based starter concentrate was characterized by a low ruminal pH and high VFA concentration regardless of the milk allowance.
Key Words: calf • ruminal environment • starter concentrate • milk allowance
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INTRODUCTION
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Early weaning of dairy calves is practiced for convenience and for economic reasons. Specially formulated starter concentrates with high palatability and high contents of easily fermentable carbohydrates are used to stimulate adaptive changes in epithelia of the fore-stomachs. Volatile fatty acids, and especially butyrate, are known to stimulate the development of ruminal papillae in young calves (Sander et al., 1959), whereas ruminal fill stimulates muscular development and ruminal volume (Flatt et al., 1958; Tamate et al., 1962). The ruminal environment is influenced by diet; however, the general awareness of the negative influence of subacute ruminal acidosis on health and production in both growing and dairy cattle (Nagaraja and Chengappa, 1998; Owens et al., 1998; Stone, 2004) has not translated into special precautions for protecting the juvenile rumen of the young calf against low ruminal pH. Ingestion of corn-based starter concentrates was followed by ruminal pH measurements of approximately 5.5 (Anderson et al., 1987), which is considered borderline for subacute ruminal acidosis (Nordlund et al., 2004), and at this pH, cell swelling and decreased electrolyte transport were observed in ovine ruminal epithelium (Gaebel et al., 1989). The substitution of corn with barley in Northern Europe might also exaggerate the condition because of the increased ruminal degradation rate of barley starch compared with cornstarch (Nocek and Tamminga, 1991). Our hypotheses were 1) that a typical European calf starter with 50% steam-rolled barley would induce ruminal fermentation in young calves characterized by a pH lower than usually recommended in cattle, and 2) that increased milk allowance via a lower solid feed intake would alleviate the negative influence of the high starch concentrate on ruminal environment and ensure a more gradual induction of ruminal fermentation. The objective of the study was to characterize the ruminal environment and jugular blood variables from wk 2 to 5 of age as well as mass, content, and morphometric measures of gastrointestinal tract compartments at 5 wk of age in Holstein calves.
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MATERIALS AND METHODS
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The present experiment complied with Danish Ministry of Justice Law Number 382 (June 10, 1987), Act Number 726 (September 9, 1993), concerning experiments with animals and care of experimental animals.
Animals and Feeding
Eight Danish Holstein male calves delivered by multiparous cows and implanted with a ruminal cannula at d 7 ± 1 of age (polyvinyl chloride cannula: 20 mm o.d., 14 mm i.d., fixed inner flange and adjustable outer flange both 50 mm, length 60 mm, screw cap; Hammershøj Maskinteknik, Hammershøj, Denmark) were used in the study. The day before cannulation, solid feed was withdrawn in the afternoon and the calves were not fed milk on the morning of surgery. The calves were anesthetized by intramuscular injection of xylazine (0.15 mg/kg of BW) and ketamine (10 mg/kg of BW) and intubated for artificial ventilation with oxygen during the surgical procedure. The calves were treated with nonsteroidal antiinflammatory drugs and antibiotics for 3 and 5 d postsurgery, respectively.
Calves were kept in the nursing area of the dairy barn and fed colostrum only until d 4, when they were moved to a climate-controlled room maintained at 20°C lit from 0600 to 2200 h. Calves were kept in individual pens (1.50 x 1.65 m) with partitions that allowed pairwise contact between calves. Milk feeding, at 0800 and 1500 h on d 4 to 11, was 4.74 kg of milk replacer (123 g of DM/kg of milk replacer; Table 1
) divided into 2 equally sized portions. Milk replacer was fed in nipple-buckets and the calves had access to the buckets for 20 min at each feeding throughout the study. Milk temperature was recorded at every feeding (mean, 37°C; SD, 2°C).
Calves were blocked by birth weight and randomly allocated to 4 experimental treatments within 2 blocks. Treatments were 4 milk replacer allowances (3.10, 4.84, 6.60, and 8.34 kg of milk replacer/d; 123 g of DM/kg; Table 1
). Milk feeding was gradually adjusted at d 12 and 13, and from d 14 (first sampling) milk feeding remained fixed at the level given by the individual treatment. From d 4 calves had ad libitum access to concentrate and hay (Table 1) fed in excess of daily intake in 2 separate wall-mounted buckets. Orts were removed and weighed every morning. Each pen had an individual bowl drinker with open water surface, and a rubber mat and wood shavings were used as bedding. Bedding was replaced twice daily and water bowls cleaned as needed.
Experimental Samplings
All calves were sampled on the same days at the age of 14, 21, 28, and 35 ± 1 d; samplings are hereafter referred to by age of the calves in weeks (2, 3, 4, and 5). A total of 12 ruminal fluid samples were obtained from the ventral ruminal sac with a suction strainer (Bar Diamond, Parma, ID) by sampling every 2 h from 0400 to 0200 h the following morning. Ruminal fluid pH was measured immediately after sampling each calf (IQ 240, IQ Scientific Instruments Inc., Carlsbad, CA). Immediately after reading pH, a subsample of ruminal fluid was stabilized with 5% metaphosphoric acid and frozen at –20°C.
A blood sample was obtained from the jugular vein between 1200 and 1300 h by venipuncture with a heparin vacuette (Greiner BioOne GmbH, Kremsmuenster, Austria). Samples were placed on ice, and plasma was harvested by centrifugation at 3,000 x g for 20 min at 4°C. Plasma was stored below –20°C until analysis. Body weights were recorded 1 or 2 times per week on different days from sampling.
Slaughter, Tissue Sampling, and Scoring of Ruminal Papillae
The calves were euthanized by captive bolt stunning and exsanguination 1 to 2 d after sampling in wk 5. The gastrointestinal tract, liver, and kidneys were harvested immediately and viscera-free carcass weight was determined (including head, hide, feet, and tail). The gastrointestinal tract was separated by strings and dissected into the reticulorumen, omasum, abomasum, and small and large intestine. The kidneys were dissected into organ and perirenal fat. Total weights and weights of contents and empty organs were measured and recorded. The reticulorumen was rinsed in tap water and examined for papillary aggregation, edema, and necrosis in the atrium and cranial part of the ventral ruminal sac. Two individual operators measured the length of 5 randomly selected papillae at the floor of the atrium and cranial part of the ventral ruminal sac with a ruler.
Analytical Procedures
Ruminal fluid was analyzed for glucose (glucose oxidase) and L-lactate (L-lactate oxidase; YSI 7100 analyzer, YSI Inc., Yellow Springs, OH). Ruminal fluid VFA was analyzed by gas chromatography (Kristensen et al., 1996). Ammonia in the ruminal fluid was determined by using NADPH-dependent glutamate dehydrogenase (AM 1015, Randox Laboratories Ltd., Crumlin, UK) following 1:10 to 1:30 dilution with a 100 mM phosphate buffer. Alcohols and esters were determined in ruminal fluid by headspace GC-MS as described by Kristensen et al. (2007).
Plasma VFA were analyzed as described by Kristensen (2000) except that a mass spectrometer was used as detector (Trace DSQ, Thermo Electron, Austin, TX). Glucose and L-lactate in plasma were determined as described for ruminal fluid. Plasma 3-hydroxybutyrate was determined with a kit based on D-3-hydroxybutyrate dehydrogenase (Ranbut, Randox Laboratories Ltd.). Plasma acetone was determined by the headspace GC-MS method used for ruminal fluid and is the sum of acetone and acetoacetate in the samples because of the complete decarboxylation of acetoacetate during incubation at 100°C. Plasma ammonia was determined by the procedure described for ruminal fluid but omitting the dilution step. Insulin was determined according to the procedure described by Løvendahl and Purup (2002). Plasma IGF-I was determined as described by Frystyk et al. (1995).
Feed samples were dried at 60°C for 48 h in a forced-air oven. Organic matter was determined as DM – crude ash, where crude ash was determined after combustion at 525°C for 6 h. Crude fat was determined as petroleum ether extract following acid hydrolysis (Stoldt, 1952). Neutral detergent fiber was determined as described by Mertens (2002). Crude protein was determined as N x 6.25 and N determined as described by Hansen (1989). Starch was determined according to the following modification of the procedure described by Salomonsson et al. (1984): 30 mg of dry sample (equivalent to 7 to 8 mg of starch) ground through a 0.5-mm screen or 5 to 30 mg of pure starch for calibration was weighed into 13-mL culture tubes, suspended in 10 mL of acetate buffer (0.1 M; pH 5.0), and incubated for 70 min at 100°C with 50 µL of thermostable 
-amylase (3,000 U/ mL; Megazyme Int., Bray, Ireland). After cooling to below 60°C, 50 µL of amyloglucosidase (3,260 U/mL; Megazyme Int.) was added to samples and the mixture was incubated overnight at 60°C. Samples were incubated for 30 min at 100°C, cooled to room temperature, centrifuged at 3,000 x g for 30 min at 20°C, and the supernatant was assayed for glucose with the YSI 7100 analyzer (YSI Inc.). Samples incubated without enzymes were used to correct for nonstarch glucose in the samples. In vitro digestibility of hay OM was determined by the method described by Tilley and Terry (1963). In vitro enzyme digestibility of starter-concentrate OM was determined as described by Weisbjerg and Hvelplund (1993).
Statistical Analysis
Ruminal variables with 12 samplings within sampling day (i.e., time) were considered as repeated measures and analyzed by using the autoregressive order 1 structure in the mixed models procedure of SAS (SAS Institute, 2001). The model included the effects of block, treatment, week, and time and the interactions of treatment x week, treatment x time, week x time, and treatment x week x time. The calf x treatment interaction was designated as a random effect. Orthogonal polynomial contrasts were used to estimate the linear, quadratic, and cubic effects of treatment and week as well as their interactions. All variables with only one weekly observation were analyzed similarly, but with a reduced model not containing the effects of time. Variables with one observation per calf (birth weight, final weight, and slaughter data) were analyzed by using the GLM procedure of SAS with orthogonal polynomial contrasts to estimate the linear, quadratic, and cubic effects of treatment. All values are given as means ± SE. Significance was declared at P < 0.05.
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RESULTS AND DISCUSSION
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BW, Feed Intake, and ADG
Weight at birth, final BW, and age at slaughter were not different among treatments, but there was a linear effect of milk allowance on visceral-free carcass weight (Table 2). A treatment x week interaction was observed for concentrate intake (Table 2 and Figure 1), reflecting efficient substitution of milk with concentrate with treatment 3.10. The observed effects of milk allowance on concentrate intake are in agreement with previous studies (Jasper and Weary, 2002; Brown et al., 2005; Von Keyserlingk et al., 2006). Interactions between treatment and week were observed for ME intake, reflecting that treatment 3.10 moved from the lowest ME intake in wk 2 to be at the same level as treatment 8.34 in wk 5, and that the largest increase with treatment 8.34 was observed from wk 2 to 3. For the other treatments ME intake increased linearly with week.
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Table 2. Birth weight, final weight, visceral free carcass weight, feed intake, ME intake, and ADG of Holstein calves fed 4 different milk allowances during wk 2 to 5 of age
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A linear treatment x week interaction was observed for ADG, reflecting lower daily gain with the 2 lowest milk allowances (treatments 3.10 and 4.84) during the first 2 wk and similar daily gain among all treatments in the last 2 wk of the study. Treatment effects on ADG were relatively small compared with previous studies (Diaz et al., 2001; Jasper and Weary, 2002; Bartlett et al., 2006). This might be partly explained by the relatively short experimental period of the present study, the fact that no concentrate was offered in some studies (Diaz et al., 2001; Bartlett et al., 2006), and that milk allowance in the present study changed body composition, as indicated by the increased mass of visceral-free carcass weight and perirenal fat with increasing milk allowance (see below).
A linear treatment x quadratic week interaction (P < 0.05) was observed for hay intake; however, the numerical differences among treatments were within 20 g of hay DM/d, and the increase in daily hay intake from wk 2 to 5 was approximately 30 g (Table 2). Hay intake as a percentage of total concentrate + hay intake was 5 to 10 ± 2% and was not affected by treatment or week.
Ruminal pH
Ruminal pH was more similar among treatments than expected. A linear treatment x week interaction (P < 0.05) for ruminal pH was observed, indicating that calves with high milk allowance had higher ruminal pH during the first 2 wk and that all treatments approached the same level during the last 2 wk of the study (Table 3). Two calves in wk 2 and 1 of these 2 calves in wk 3 had a concentrate intake below 20 g of DM/d, and only these calves appeared to contribute to the apparent difference among treatments in the first part (wk 2 and 3) of the study. There was a linear treatment x week effect for duration of ruminal pH <6.2, caused by treatments 6.60 and 8.34 initially having a few hours below this pH value and approaching the same level as the other treatments at the last samplings. For all treatments, the duration of ruminal pH <6.2 was above 12 h in wk 5. The duration of ruminal pH <5.8 and <5.5 was not different among treatments (7 to 18 ± 3 and 5 to 13 ± 4 h, respectively) and was not affected by week. The daily minimum ruminal pH was not affected by treatment or week (5.14 to 5.66 ± 0.17 and 5.21 to 5.57 ± 0.15, respectively). There was no correlation between concentrate intake and severity of ruminal pH depression with concentrate intakes above 20 g of DM/d. Increased milk allowance did therefore not alleviate the concentrate-induced acidification of the rumen in milk-fed calves. Ruminal pH was affected by sampling time; however, there was no week x time interaction (P = 0.14), and generally the diurnal variation in ruminal pH was relatively small. Ruminal pH was highest during the late evening and night for the first 2 wk of sampling and lowest during this time the last 2 sampling weeks. The pH values recorded in the present study were within the range of values previously reported in young calves (Anderson et al., 1987; Lesmeister and Heinrichs, 2004). Data from Lesmeister and Heinrichs (2004) indicated a more gradual decrease in ruminal pH compared with the present study, but this might have been caused by a higher concentrate intake during the first week of the present study and the inclusion of a more rapidly fermenting starch source (barley) in the present study compared with the aforementioned study.
Ruminal VFA
There was a cubic effect of week on total ruminal VFA concentration, reflecting a relatively large increase in ruminal VFA from wk 3 to 4 (Table 3); however, by wk 2 ruminal concentrations of VFA were already close to the range usually observed in lactating dairy cows (83 to 162 mmol/L; Seymour et al., 2005). There was an effect of sampling time on ruminal VFA, indicating that VFA concentrations decreased in the samples obtained from 0400 to 0800 h, especially in wk 4 and 5. In each week, the total VFA concentration and pH were correlated (r = –0.93, –0.63, –0.88, and –0.83 for wk 2 to 5, respectively). Molar proportions of all VFA except isobutyrate were affected by week, by interactions between week and treatment, or both. The molar proportion of ruminal acetate decreased and the molar proportion of ruminal propionate increased linearly with week. The molar proportion of ruminal propionate was considerably higher than found in dairy cows, even considering the linear relationship between ruminal pH and the molar proportion of propionate typically observed (Figure 2). In 26 out of the 32 calf x sampling day combinations, the molar proportion of ruminal propionate was equal to or higher than 35 mol/100 mol. Ruminal defaunation has previously been shown to increase ruminal VFA concentrations and the molar proportion of propionate (Eadie et al., 1970; Nagaraja et al., 1992), and although protozoa were not enumerated in the present study, the fermentation profile was generally in agreement with a defaunated rumen.
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Figure 2. Ruminal propionate (mol/100 mol) related to ruminal pH in literature data from ruminal cannulated dairy cows [(•; Huhtanen et al., 2002); ( ; Rabelo et al., 2001); ( ; Knowlton et al., 1998); ( ; Dhiman et al., 2002); ( ; Murphy et al., 2000); (•; Broderick et al., 1999); ( ; Reis et al., 2001); ( ; Akay and Jackson, 2001); ( ; Kristensen, 2001); ( ; Mowrey et al., 1999); ( ; Casper et al., 1999)] and mean observations within sampling day for individual calf x day observations from the present study (open hexagon).
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The interaction between treatment and week for butyrate reflected the fact that treatments 4.84 and 8.34 were followed by higher butyrate compared with the other treatments in wk 2 and that the butyrate concentration was low with treatment 6.60 in wk 3 (3.0 ± 0.2 mol/100 mol). The linear treatment x week interaction for isovalerate reflected the fact that isovalerate remained at a relatively low level for treatments 3.10 and 4.84 throughout the study and that isovalerate was relatively high initially, with treatments 6.60 and 8.34 approaching the level of the other treatments at the sampling in wk 5. The interactions between treatment and week observed for valerate indicated that the relative ranking of the treatments 6.60 < 8.34 < 4.84 < 3.10 was found in all weeks except for wk 2, when treatment 3.10 had the lowest level of valerate along with treatment 6.60. The cubic treatment x week interaction observed for caproate indicated that the levels with treatments 3.10 and 4.84 gradually merged and increased compared with the other treatments.
Ruminal Alcohols and VFA Esters
Headspace analysis of ruminal fluid revealed the presence of ethanol and propanol as well as multiple VFA esters, of which ethyl acetate and propyl acetate were included in the standards and quantified (Table 3). Esters identified but not quantified included methyl acetate, methyl propionate, methyl butyrate, ethyl propionate, ethyl butyrate, ethyl valerate, propyl propionate, and propyl butyrate. Ruminal concentrations of ethanol, propanol, ethyl acetate, and propyl acetate were affected by sampling time, reflecting diurnal patterns inverse to the pattern of ruminal pH. A quadratic treatment x cubic week interaction was observed for propanol, reflecting a relatively large variation during the first 2 wk, with the highest concentrations following the lowest milk allowance, and merging of the levels across treatments in the last 2 wk. Alcohols can be synthesized in the rumen by bacteria (Lauková and Marounek, 1992) and fungi (Teunissen et al., 1992) and have previously been shown to accumulate under acidic ruminal conditions (Allison et al., 1964). Production of alcohols is an electron sink in fermentation (Teunissen et al., 1992), and the consistent presence of alcohols in the rumen of the calves in the present study is in good agreement with the high molar proportion of propionate; both variables indicate that the hydrogen pressure was relatively high. Although the maximal ruminal concentrations of ethanol (8 mmol/L) observed in the present study were as high as that observed by Allison et al. (1964) following induction of ruminal acidosis, the mean concentrations of alcohols and esters were below the levels observed in dairy cows fed corn silage containing natural levels of ethanol and propanol (Kristensen et al., 2007). However, the headspace analysis revealed the presence of many more esters than included in the standard, and the total concentration of VFA esters might have been higher in the calves compared with dairy cows. Esters of VFA might be important in the rumen by affecting the activity of various microorganisms in the rumen, similar to the way ester-producing yeasts affect the growth of molds in coculture (Fredlund et al., 2004). Ruminal epithelium might also be challenged by the presence of large amounts of VFA esters because of their lipophilic nature and presumed fast absorption rate. Ethyl acetate has been shown to induce chromosome malsegregation in yeast (Zimmermann et al., 1985). However, other studies have demonstrated an increased Na transport by isolated small intestinal mucosa, presumably because of intracellular hydrolysis of the ethyl acetate that supplies acetate as an oxidative substrate for the cell (Esposito et al., 1976). Esters of VFA will presumably be hydrolyzed upon absorption by the rumen epithelial esterases, as is apparent in other species (Coopman et al., 2005), although the exact identity and properties of the rumen epithelial esterases are not known.
Ruminal Ammonia, L-Lactate, and Glucose
The ruminal ammonia concentration decreased linearly with week (Table 3), in agreement with the findings of Lesmeister and Heinrichs (2004). Ruminal ammonia was affected by sampling time, but the numerical differences among sampling days were minor and the pattern was not consistent among weeks. There was a tendency for an interaction between treatment and week for ruminal ammonia, indicating that ammonia levels were numerically related to milk allowance during the first weeks of the study, with all treatments merging at a relatively low level in the last week of the study. Ruminal concentrations of L-lactate and glucose were low (Table 3), and the observed effects were numerically minor despite some indications of slightly higher values recorded in wk 4.
Jugular Blood Plasma Variables
A quadratic treatment x week interaction was observed for plasma glucose (Table 4), reflecting an increased glucose concentration with treatment 8.34 for the first 3 wk. Plasma lactate was not affected by treatment or week. A quadratic time x linear week interaction was observed for acetate, reflecting increased acetate concentration with treatment 3.10 in wk 4 and 5 (Figure 3). The interaction between treatment and week observed for propionate reflected a similar pattern as observed for acetate. For butyrate and 3-hydroxybutyrate, treatment 4.84 had higher levels during wk 4 and 5 compared with the other treatments. With treatment 3.10, plasma concentrations of acetone increased already from wk 3. For plasma ammonia there was a treatment x week interaction, reflecting higher plasma levels in wk 2 for all treatments except treatment 6.60 compared with the following weeks. The effects of treatment and week observed for insulin reflected a pattern similar to that observed for glucose (r = 0.66), with increased concentrations in wk 2 and 3 for treatment 8.34. The effect on IGF-I was dominated by the linear increase with week; however, the cubic treatment x linear week effect reflected slightly increased IGF-I with treatment 8.34 in wk 3 and 4. Plasma concentrations of acetate, propionate, butyrate, 3-hydroxybutyrate, and acetone correlated with concentrate intake (r = 0.72 to 0.88; P < 0.01). Plasma concentrations of VFA and 3-hydroxybutyrate have previously been shown to respond to the presence of VFA in the rumen (Kristensen and Harmon, 2004). Diabetes increases (Knowles et al., 1974) and propionate infusion decreases plasma acetate (Kristensen et al., 2000); however, the concerted increase in both ketogenic and glucogenic VFA as well as 3-hydroxybutyrate and acetone + acetoacetate in the present study points to the conclusion that total absorption of fermentation products increased with concentrate intake. Furthermore, data on both feed intake and plasma VFA concentrations suggest that ruminal fermentation can make a relatively large contribution to the metabolism of the calf already within the first 2 wk of life.
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Table 4. Jugular blood plasma variables of Holstein calves fed 4 different milk allowances during wk 2 to 5 of age
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If the general morphological development of ruminal epithelium is correlated with the functional development of ketogenesis in ruminal epithelium, we would expect to find a low ketogenic activity early on in ruminal development (for a discussion, see Baldwin et al., 2004). In studies with steers in which rumen epithelial metabolism of butyrate was suppressed by intraruminal infusion of valerate, the 3-hydroxybutyrate:butyrate ratio in peripheral plasma decreased from 49 with a normal valerate level to 21 with a high valerate level (Kristensen and Harmon, 2005). In the present study, the 3-hydroxybutyrate:butyrate ratio in blood plasma was 53 ± 14 and not affected by treatment or week; the high ratio indicates that the ruminal epithelium was capable of metabolizing ruminal butyrate without any delay for adaptation. This is in line with the observations by Lane et al. (2002) showing that expression of genes encoding ketogenic enzymes in ruminal epithelium are not affected by the presence of VFA in the rumen of lambs. Thus, although it is generally assumed that the morphological and metabolic development of ruminal epithelium in the young calf are linked, the present study adds to the pool of data (Baldwin, et al., 2004) questioning whether the metabolic adaptation of ruminal epithelium is reflected by the morphological adaptation.
Organs and Digesta
Wet weights of the rumen + reticulum, omasum, and total stomach decreased linearly with intake of milk replacer (Table 5). The weights of the abomasum and kidneys were not affected by treatment. The cubic effect of treatment on liver weight reflected a smaller liver with treatment 4.84. The weight of perirenal fat increased linearly with milk allowance, indicating a general increase in body fat content with increased milk allowance. Wet weights of digesta in the rumen + reticulum, omasum, and total stomach decreased linearly with milk allowance, showing that the body composition was affected by treatment. The weight of digesta in the abomasum was not affected by treatment. Length of papillae in the atrium or ventral ruminal sac was not affected by treatment. There were no visual signs of epithelial ulceration or necrosis with any treatment. However, some papillary aggregation was observed with all treatments, and edema at the tip of the papillae was observed with treatments 4.84, 6.60, and 8.34, in agreement with the acidic ruminal environment observed in the present study as previously described by Huntington (1988).
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Table 5. Weights of organs and digesta and length of ruminal papillae of Holstein calves fed 4 different milk allowances during wk 2 to 5 of age
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CONCLUSIONS
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Young calves fed a traditional barley-based starter concentrate were found to be subjected to acidic ruminal conditions, a high molar proportion of propionate, and the presence of alcohols and VFA esters in ruminal fluid as soon as daily concentrate intake was more than 20 g of DM/d. The relatively large variation in concentrate intake induced by different milk allowances had small effects on the ruminal environment, but the low milk allowance was followed by increased blood concentrations of VFA and ketone bodies as well as an increased mass of digesta content and weights of the rumen + reticulum and omasum.
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ACKNOWLEDGEMENTS
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We gratefully acknowledge Janne Adamsen and Birgit H. Løth for their skillful technical assistance and the staff of the intensive care unit at the Danish Institute of Agricultural Sciences for care of the calves during the study. Kasper B. Poulsen is acknowledged for IGF-I analyses. We would also like to thank Kirstine F. Jørgensen for assisting with morphometric measures at slaughter as well as a group of students from the Royal Veterinary and Agricultural University in Copenhagen for assistance during some of the samplings (Victoria Jenny Kerstin Andersson, Elise Bostad, Kira Langkjer Jürgensen, Eva Johanna Caroline Larsson, Helle Lahrmann, Helle K. Jensen, Charlotte Amdi, Trine Jensen, Sussi Thomasen, Nicolaj Nielsen, and Bente Correll Jensen). Funding for the present study was provided by the Danish Cattle Federation (no. 01.18) and the Danish Institute of Agricultural Sciences.
Received for publication December 22, 2006.
Accepted for publication May 29, 2007.
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REFERENCES
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Akay, V., and J. A. Jackson, Jr. 2001. Effects of nutridense and waxy corn hybrids on the rumen fermentation, digestibility and lactational performance of dairy cows. J. Dairy Sci. 84:1698–1706.[Abstract]
Allison, M. J., J. A. Bucklin, and R. W. Dougherty. 1964. Ruminal changes after overfeeding with wheat and the effect of intraruminal inoculation on adaptation to a ration containing wheat. J. Anim. Sci. 23:1164–1171.[Abstract/Free Full Text]
Anderson, K. L., T. G. Nagaraja, and J. L. Morrill. 1987. Ruminal metabolic development in calves weaned conventionally or early. J. Dairy Sci. 70:1000–1005.[Abstract/Free Full Text]
Baldwin, R. L., K. Vi, R. McLeod, J. L. Klotz, and R. N. Heitmann. 2004. Rumen development, intestinal growth and hepatic metabolism in the pre- and postweaning ruminant. J. Dairy Sci. 87:E55–E65.[Abstract/Free Full Text]
Bartlett, K. S., F. K. McKeith, M. J. Vandehaar, G. E. Dahl, and J. K. Drackley. 2006. Growth and body composition of dairy calves fed milk replacers containing different amounts of protein at two feeding rates. J. Anim. Sci. 84:1454–1467.[Abstract/Free Full Text]
Broderick, G. A., R. G. Koegel, M. J. C. Mauries, E. Schneeberger, and T. J. Kraus. 1999. Effect of feeding macerated alfalfa silage on nutrient digestibility and milk yield in lactating dairy cows. J. Dairy Sci. 82:2472–2485.[Abstract]
Brown, E. G., M. J. Vandehaar, K. M. Daniels, J. S. Liesman, L. T. Chapin, D. H. Keisler, and M. S. Weber Nielsen. 2005. Effect of increasing energy and protein intake on body growth and carcass composition of heifer calves. J. Dairy Sci. 88:585–594.[Abstract/Free Full Text]
Casper, D. P., H. A. Maiga, M. J. Brouk, and D. J. Schingoethe. 1999. Synchronization of carbohydrate and protein sources on fermentation and passage rates in dairy cows. J. Dairy Sci. 82:1779–1790.[Abstract]
Coopman, V. A., J. A. Cordonnier, and C. A. De Meyere. 2005. Fatal workplace accident involving ethyl acetate: A distribution study. Forensic Sci. Int. 154:92–95.[CrossRef][Medline]
Dhiman, T. R., M. S. Zaman, I. S. MacQueen, and R. L. Boman. 2002. Influence of corn processing and frequency of feeding on cow performance. J. Dairy Sci. 85:217–226.[Abstract]
Diaz, M. C., M. E. Van Amburgh, J. M. Smith, J. M. Kelsey, and E. L. Hutten. 2001. Composition of growth of Holstein calves fed milk replacer from birth to 105-kilogram body weight. J. Dairy Sci. 84:830–842.[Abstract]
Eadie, J. M., J. Hyldgaard-Jensen, S. O. Mann, R. S. Reid, and F. G. Whitelaw. 1970. Observations on the microbiology and biochemistry of the rumen in cattle given different quantities of a pelleted barley ration. Br. J. Nutr. 24:157–177.[CrossRef][Medline]
Esposito, G., A. Faelli, and V. Capraro. 1976. Effect of ethyl acetate on the transport of sodium and glucose in the hamster small intestine in vitro. Biochim. Biophys. Acta 426:489–498.[Medline]
Flatt, W. P., R. G. Warner, and J. K. Loosli. 1958. Influence of purified materials on the development of the ruminant stomach. J. Dairy Sci. 41:1593–1600.[Abstract/Free Full Text]
Fredlund, E., U. Ä. Druvefors, N. Olstorpe, V. Passoth, and J. Schnürer. 2004. Influence of ethyl acetate production and ploidy on the anti-mould activity of Pichia anomala. FEMS Microbiol. Lett. 238:133–137.[Medline]
Frystyk, J., B. Dinesen, and H. Ørskov. 1995. Non-competitive time-resolved immunoflurometric assays for determination of human insulin-like growth factor I and II. Growth Regul. 5:169–176.[Medline]
Gaebel, G., M. Bell, and H. Martens. 1989. The effect of low mucosal pH on sodium and chloride movement across the isolated rumen mucosa of sheep. Q. J. Exp. Physiol. 74:35–44.[Abstract/Free Full Text]
Hansen, B. 1989. Determination of nitrogen as elementary N, an alternative to Kjeldahl. Acta Agric. Scand. 39:113–118.
Huhtanen, P., A. Vanhatalo, and T. Varvikko. 2002. Effects of abomasal infusions of histidine, glucose, and leucine on milk production and plasma metabolites of dairy cows fed grass silage. J. Dairy Sci. 85:204–216.[Abstract]
Huntington, G. B. 1988. Acidosis. Pages 474–480 in The Ruminant Animal: Digestive Physiology and Nutrition. D. C. Church, ed. Prentice-Hall, Englewood Cliffs, NJ.
Jasper, J., and D. M. Weary. 2002. Effects of ad libitum milk intake on dairy calves. J. Dairy Sci. 85:3054–3058.[Abstract/Free Full Text]
Knowles, S. E., I. G. Jarrett, O. H. Filsell, and F. J. Ballard. 1974. Production and utilization of acetate in mammals. Biochem. J. 142:401–411.[Medline]
Knowlton, K. F., B. P. Glenn, and R. A. Erdman. 1998. Performance, ruminal fermentation, and site of starch digestion in early lactation cows fed corn grain harvested and processed differently. J. Dairy Sci. 81:1972–1984.[Abstract]
Kristensen, N. B. 2000. Quantification of whole blood short-chain fatty acids by gas chromatographic determination of plasma 2-chloroethyl derivatives and correction for dilution space in erythrocytes. Acta Agric. Scand., Sect. A 50:231–236.[CrossRef]
Kristensen, N. B. 2001. Rumen microbial sequestration of [2-13C]acetate in cattle. J. Anim. Sci. 79:2491–2498.[Abstract/Free Full Text]
Kristensen, N. B., A. Danfær, V. Tetens, and N. Agergaard. 1996. Portal recovery of intraruminally infused short-chain fatty acids in sheep. Acta Agric. Scand., Sect. A 46:26–38.
Kristensen, N. B., and D. L. Harmon. 2004. Splanchnic metabolism of VFA absorbed from the washed reticulorumen of steers. J. Anim. Sci. 82:2033–2042.[Abstract/Free Full Text]
Kristensen, N. B., and D. L. Harmon. 2005. Effects of adding valerate, caproate, and heptanoate to ruminal buffers on splanchnic metabolism in steers under washed-rumen conditions. J. Anim. Sci. 83:1899–1907.[Abstract/Free Full Text]
Kristensen, N. B., S. G. Pierzynowski, and A. Danfær. 2000. Portal-drained visceral metabolism of 3-hydroxybutyrate in sheep. J. Anim. Sci. 78:2223–2228.[Abstract/Free Full Text]
Kristensen, N. B., A. Storm, B. M. L. Raun, B. A. Røjen, and D. L. Harmon. 2007. Metabolism of silage alcohols in lactating dairy cows. J. Dairy Sci. 90:1364–1377.[Abstract/Free Full Text]
Lane, M. A., R. L. Baldwin, and B. W. Jesse. 2002. Developmental changes in ketogenic enzyme gene expression during sheep rumen development. J. Anim. Sci. 80:1538–1544.[Abstract/Free Full Text]
Lauková, A., and M. Marounek. 1992. Physiological and biochemical characteristics of staphylococci isolated from the rumen of young calves and lambs. Zentralbl. Mikrobiol. 147:489–494.[Medline]
Lesmeister, K. E., and A. J. Heinrichs. 2004. Effects of corn processing on growth characteristics, rumen development, and rumen parameters in neonatal dairy calves. J. Dairy Sci. 87:3439–3450.[Abstract/Free Full Text]
Løvendahl, P., and H. M. Purup. 2002. Technical note: Time-resolved fluoro-immunometric assay for intact insulin in livestock species. J. Anim. Sci. 80:191–195.[Abstract/Free Full Text]
Mertens, D. R. 2002. Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: Collaborative study. J. AOAC Int. 85:1217–1240.[Medline]
Mowrey, A., M. R. Ellersieck, and J. N. Spain. 1999. Effect of fibrous by-products on production and ruminal fermentation in lactating dairy cows. J. Dairy Sci. 82:2709–2715.[Abstract]
Murphy, M., M. Åkerlind, and K. Holtenius. 2000. Rumen fermentation in lactating cows selected for milk fat content fed two forage to concentrate ratios with hay or silage. J. Dairy Sci. 83:756–764.[Abstract]
Nagaraja, T. G., and M. M. Chengappa. 1998. Liver abscesses in feedlot cattle: A review. J. Anim. Sci. 76:287–298.[Abstract/Free Full Text]
Nagaraja, T. G., G. Towne, and A. A. Beharka. 1992. Moderation of ruminal fermentation by ciliated protozoa in cattle fed a high-grain diet. Appl. Environ. Microbiol. 58:2410–2414.[Abstract/Free Full Text]
Nocek, J. E., and S. Tamminga. 1991. Site of digestion of starch in the gastrointestinal tract of dairy cows and its effect on milk yield and composition. J. Dairy Sci. 74:3598–3629.[Abstract]
Nordlund, K. V., N. B. Cook, and G. R. Oetzel. 2004. Investigation strategies for laminitis problem herds. J. Dairy Sci. 87:E27–E35.[Abstract/Free Full Text]
NRC. 2001. Nutrient requirements of the young calf. Pages 214–233 in Nutrient Requirements of Dairy Cattle. 7th rev. ed. Natl. Acad. Press, Washington, DC.
Owens, F. N., D. S. Secrist, W. J. Hill, and D. R. Gill. 1998. Acidosis in cattle: A review. J. Anim. Sci. 76:275–286.[Abstract/Free Full Text]
Rabelo, E., S. J. Bertics, J. Mackovic, and R. R. Grummer. 2001. Strategies for increasing energy density of dry cow diets. J. Dairy Sci. 84:2240–2249.[Abstract]
Reis, R. B., F. San Emeterio, D. K. Combs, L. D. Satter, and H. N. Costa. 2001. Effects of corn particle size and source on performance of lactating cows fed direct-cut grass-legume forage. J. Dairy Sci. 84:429–441.[Abstract]
Salomonsson, A. C., O. Theander, and E. Westerlund. 1984. Chemical characterization of some Swedish cereal whole meal and bran fractions. Swedish J. Agric. Res. 14:111–117.
Sander, E. G., R. G. Warner, H. N. Harrison, and J. K. Loosli. 1959. The stimulatory effect of sodium butyrate and sodium propionate on the development of rumen mucosa in the young calf. J. Dairy Sci. 42:1600–1605.[Abstract/Free Full Text]
SAS Institute. 2001. SAS System for Windows. Release 8.2 (TS 02MO). SAS Inst. Inc., Cary, NC.
Seymour, W. M., D. R. Campbell, and Z. B. Johnson. 2005. Relationships between rumen volatile fatty acid concentrations and milk production in dairy cows: A literature study. Anim. Feed Sci. Technol. 119:155–169.[CrossRef]
Stoldt, W. 1952. Vorslag zur vereinheitlichung der fettbestimmung in lebensmitteln. Fette Seifen 54:206–207.[CrossRef]
Stone, W. C. 2004. Nutritional approaches to minimize subacute ruminal acidosis and laminitis in dairy cattle. J. Dairy Sci. 87(E Suppl.):E13–E26.[Abstract/Free Full Text]
Tamate, H., A. D. McGilliard, N. L. Jacobson, and R. Getty. 1962. Effect of various dietaries on the anatomical development of the stomach in the calf. J. Dairy Sci. 45:408–420.[Abstract/Free Full Text]
Teunissen, M. J., E. P. W. Kets, H. J. M. Op den Camp, J. H. J. Huis in’t Veld, and G. D. Vogels. 1992. Effect of coculture of anaerobic fungi isolated from ruminants and non-ruminants with methanogenic bacteria on cellulytic and xylanolytic enzyme activities. Arch. Microbiol. 157:176–182.[Medline]
Tilley, J. M. A., and R. A. Terry. 1963. A two-stage method for the in vitro digestion of forage crops. J. Br. Grassl. Soc. 18:104–111.
Von Keyserlingk, M. A. G., F. Wolf, M. Hötzel, and D. M. Weary. 2006. Effects of continuous versus periodic milk availability on behavior and performance of dairy calves. J. Dairy Sci. 89:2126–2131.[Abstract/Free Full Text]
Weisbjerg, M. R., and T. Hvelplund. 1993. Bestemmelse af nettoener-giindhold (FEK) i råvarer og kraftfoderblandinger. Forsknings- rapport nr. 3. Statens Husdyrbrugsforsøg. (in Danish). National Institute of Animal Science, Tjele, Denmark.
Zimmermann, F. K., V. W. Mayer, I. Scheel, and M. A. Resnick. 1985. Acetone, methyl ethyl ketone, ethyl acetate, acetonitrile and other polar aprotic solvents are strong inducers of aneuploidy in Saccharomyces cerevisiae. Mutat. Res. 149:339–351.[Medline]
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ABSTRACT
INTRODUCTION
