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The Journal of Nutrition Vol. 128 No. 3 March 1998,
pp. 624-632
Division of Nutrition Pathology, Institute of Animal Breeding, University, 3012 Berne, Switzerland
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ABSTRACT |
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Abstract
Introduction
Methods
Results
Discussion
References
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Bovine colostrum contains various essential nutrients, antibodies, hormones and growth factors that are important for nutrient supply, host defense, growth and for general neonatal adaptation. We have studied effects of colostrum fed for different durations on selected metabolic and endocrine traits in the first week of life in calves. Calves were fed colostrum twice daily for 3 d (group C6) or colostrum only as their first meal (group C1), followed by milk replacer up to d 7, or they were only fed milk replacer but no colostrum (group M). Plasma concentrations of immunoglobuline G and activities of enzymes (
-glutamyltransferase, aspartate-aminotransferase, lactate-dehydrogenase, glutamate-dehydrogenase) increased in groups C6 and C1 after first feeding, but not in group M. Postprandial plasma glucose concentrations on d 2 increased significantly more in groups C6 and C1 than in group M. Plasma triglycerides on d 2 and plasma phospholipid and cholesterol concentrations on d 7 were significantly higher in group C6 than in groups C1 and M. Plasma insulin concentrations on d 2 tended (P = 0.07) to increase more postprandially in group C6 than in group M and postprandial plasma glucagon concentrations on d 1 increased more in groups C6 and C1 than in group M and remained elevated on d 2 only in group C6. Plasma cortisol concentrations decreased postprandially in all three groups and were highest on d 2 and d 7 in group M. Plasma triiodthyronine and thyroxine concentrations decreased in the first week of life in all calves, whereas plasma prolactin concentrations were greatest on d 7 in group C6. In conclusion, various metabolic and endocrine traits were influenced by whether colostrum was fed and the duration of colostrum feeding.
Newborns must adapt to various environmental factors after birth, including nutrition, which changes from a primarily carbohydrate-based energy supply during the fetal period to a high fat and relatively low carbohydrate nutritional energy supply in colostrum (Aynsley-Green 1988 Colostrum intake influences the functional development of the neonatal intestine and absorption of nutrients, partly due to effects of various colostral growth factors, such as insulin-like growth factor I (IGF-I)5 and epidermal growth factor and colostral enzymes (Berseth et al. 1983 Colostrum intake also has systemic effects on metabolism and endocrine status of neonates. Nutritional and non-nutritional factors affect protein synthesis (Burrin et al. 1995 In neonatal calves fed colostrum for different durations or fed only milk replacer (UFA-100 without antibiotics, UFA AG, Sursee, Switzerland), we studied effects of colostrum intake on gastrointestinal development and on the somatotropic axis (Hammon and Blum 1997a Husbandry, feeding and experimental procedures
INTRODUCTION
Abstract
Introduction
Methods
Results
Discussion
References
, Ferré et al. 1986, Girard 1986, Odle 1997). Bovine colostrum contains various essential nutrients and supplies newborn calves with energy, immunoglobulins and bioactive factors such as growth factors, hormones and cytokines (Campana and Baumrucker 1995, Grosvenor et al. 1993, Koldovsky 1989, Roy 1980, Stott and Fellah 1983).
, Bird et al. 1996, Hammon and Blum 1997a, Hamosh 1996, Odle et al. 1996, Simmen et al. 1990, Xu 1996). Thus orally administered recombinant human IGF-I stimulates the mitotic rate of small enterocytes in neonatal calves (Baumrucker et al. 1994b), enhances gut growth in neonatal piglets (Burrin et al. 1996) and total gut weight increases after IGF-I infusion in rats (Read et al. 1992). Thus biologically active substances are important for maturation of the gastrointestinal tract of the neonate after birth.
), and colostrum intake influences the somatotropic axis in neonatal calves (Hammon and Blum 1997b). Delaying colostrum intake in neonatal calves for 24 h after birth impaired assimilation and utilization of some colostral components and resulted in altered metabolic and endocrine responses in the first week of life (Hadorn et al. 1997).
and 1997b). The present study adds to these investigations. Our goal was to investigate whether systemic metabolic and endocrine changes after birth are dependent on the duration of colostrum supply.
MATERIAL AND METHODS
Abstract
Introduction
Methods
Results
Discussion
References
-glutamyltransferase (GT, EC 2.3.2.2), insulin, cortisol, triiodthyronine (T3) and thyroxine (T4). Tubes (10 ml) containing dipotassium-EDTA (1.8 g/L blood) and the protease inhibitor aprotinin (10 KIU/L blood; Sigma, St. Louis, MO) were used to collect blood for determination of glucagon. Tubes (4 ml) containing dipotassium-EDTA (1.8 g/L blood) and sodium fluoride (3 g/L blood) were used to collect blood for determination of lactic acid. Tubes (10 ml) without anticoagulants were used for later determination of immunoglobulin G (IgG), aspartate-aminotransferase (AST, EC 2.6.1.1), lactate-dehydrogenase (LDH, EC 1.1.1.27), glutamate-dehydrogenase (GLDH, EC 1.4.1.3) and prolactin (PRL).
Laboratory methods
Analyses in blood plasma or serum.
Glucose, triglyceride and cholesterol concentrations were measured enzymatically; GT AST and LDH activities were measured using kits (No. 07-3671-6, 07-3679-1, 07-3663-5, 07-3655-4, 07-3641-4, 07-3657-0, respectively) from Hoffmann-La-Roche (Basle, Switzerland); phospholipids and lactic acid enzymatically with kits (No. 61-491, 61-192, respectively) from Bio-Mérieux (Marcy l' Etoile, France); NEFA enzymatically with a kit (994-75409) from Wako Chemicals (Neuss, Germany); and GLDH with a kit (124-311) from Boehringer (Ingelheim, Germany) using an automatic analyzer (Cobas Mira, Hoffmann-La-Roche, Basle, Switzerland).
). Inter- and intraassay coefficients of variation for the determination of these hormones were <15 and 10%, respectively.
).
Analyses in colostrum and milk replacer.
Gross energy was measured using an adiabatic bomb calorimeter, crude protein by determination of nitrogen using the Kjeldahl method and crude fat following Soxleth extraction, using standard methods (Weende analysis). Concentrations of nitrogen-free extracts (primarily lactose) were calculated. AST, GT, LDH and GLDH activities were measured in casein-deprived colostrum and milk replacer (obtained after addition of rennin) (Vacher and Blum 1993) as described for blood samples.
Statistics
Values of metabolic traits and hormones in blood plasma are expressed as means ± SEM. After subtraction of basal (prefeeding) values, the areas under the concentration curves were calculated as a measure of total incremental or decremental changes (
0-7 h) of metabolites and hormones concentrations to evaluate net effects of morning feeding on d 1, d 2 and d 7. Furthermore, mean concentrations on d 1, d 2 and d 7 were calculated using areas under the concentration curve without subtraction of basal (prefeeding) values and divided by the studied time period.
0-7 h) on d 1, d 2 and d 7 were evaluated by paired t test (P < 0.05) using the SAS program package release 6.11 (SAS Institute 1993).
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RESULTS |
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Abstract
Introduction
Methods
Results
Discussion
References
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Feeding of newborn calves.
Initial colostrum (milking 1) fed to calves was from their respective dams. Subsequent colostrum (milkings 2-6) fed was from pooled milk, which was prepared separately for each milking, respectively, before the study was started and stored at -20°C. Dry matter, gross energy, crude protein, crude fat, lactose, IgG and enzymes of colostrum and milk replacer (UFA-100 without antibiotics, UFA AG, Sursee, Switzerland) are listed in Table 1. Colostrum contained much higher amounts of IGF-I than milk replacer (Hammon and Blum 1997b). Intake of gross energy of the first feeding was 3.3 times greater and of the sixth feeding was 2.2 times greater in group C6 than group M. Intake of crude protein of the first feeding was six times greater and of the sixth feeding 2.2 times greater in group C6 than group M.
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Metabolic profiles. Serum IgG concentrations (Table 2) in groups C6 and C1 increased (P < 0.001) on d 1 after colostrum intake, were higher (P < 0.001) on d 2 than on d 1 and decreased from d 2 up to d 7 in both groups. Concentrations postprandially decreased on d 2 in group C6 and on d 7 in groups C6 and C1. Concentrations remained very low in group M during the first week. Serum IgG concentrations were higher (P < 0.01) in groups C6 and C1 during the first week than in group M. On d 7, basal concentrations were higher (P < 0.05) in group C6 than group C1.
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Enzyme profiles.
On d 1 plasma
Hormone profiles.
Plasma insulin concentrations (Fig. 2) after feed intake significantly increased in group C6 on d 1 and d 2 and in group C1 on d 2. Mean concentrations on d 2 tended to be higher (P = 0.07) in group C6 than in group M.
Plasma IgG concentrations were much higher after colostrum intake than in calves fed only milk replacer. On d 7 the calves fed colostrum six times had higher IgG concentrations than calves fed colostrum only once. As seen in previous studies (Hadorn and Blum 1997 We thank H. Schnyder for supplying us with neonatal calves and U. Hadorn for assistance in the animals experiments. We thank R. Bruckmaier, Div. of Nutrition Pathology, Inst. of Animal Breeding, Univ. of Berne, Switzerland, for consulting with us concerning statistical analyses. The excellent laboratory assistance of C. Morel and Y. Zbinden, Div. of Nutrition Pathology, Inst. of Animal Breeding, Univ. of Berne, Switzerland is greatly acknowledged.
Manuscript received 26 August 1997. Initial reviews completed 10 October 1997. Revision accepted 1 December 1997.
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Fig 1.
Blood plasma glucose concentrations in calves fed different amounts of colostrum or milk replacer: group C6 was fed colostrum six times (milkings 1-6 on d 1-d 3) and then milk replacer, group C1 was fed colostrum only once (first milking on d 1) and group M was fed only milk replacer (no colostrum). Arrows mark time of feeding. Values are means ± SEM, n = 6 (groups C6 and C1) or n = 5 (group M).
GT activity (Table 3) increased (P < 0.05) after colostrum intake in groups C6 and C1 but remained unchanged after milk replacer intake in group M. Basal levels of GT activity in groups C6 and C1 increased on d 2 and declined on d 7 to d 1 values but remained low in group M in the first week. The postprandial activity rise and mean activity on d 1 were higher (P < 0.05) in groups C6 and C1 than in group M (mean activity: 12.7 ± 1.7, 18.6 ± 3.7 and 0.2 ± 0.0 µkat/L, respectively), whereas on d 2 and d 7 basal activities were higher (P < 0.05) in group C6 than group M.
View this table:
Table 3.
Blood plasma or serum concentrations of -glutamyltransferase (GT), lactate-dehydrogenase (LDH), glutamate-dehydrogenase (GLDH) and aspartate-aminotransferase (AST) in the first week of life of neonatal calves fed colostrum six
times (C6), fed colostrum only on the first meal (C1) or fed only milk replacer
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Fig 2.
Blood plasma insulin concentrations in calves fed different amounts of colostrum or milk replacer: group C6 was fed colostrum six times (milkings 1-6 on d 1-d 3) and then milk replacer, group C1 was fed colostrum only once (first milking on d 1) and group M was fed only milk replacer (no colostrum). Arrows mark time of feeding. Values are means ± SEM, n = 6 (groups C6 and C1) or n = 5 (group M).
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Fig 3.
Blood plasma glucagon concentrations in calves fed different amounts of colostrum or milk replacer: group C6 was fed colostrum six times (milkings 1-6 on d 1-d 3) and then milk replacer, group C1 was fed colostrum only once (first milking on d 1) and group M was fed only milk replacer (no colostrum). Arrows mark time of feeding. Values are means ± SEM, n = 6 (groups C6 and C1) or n = 5 (group M).
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Fig 4.
Blood plasma cortisol concentrations in calves fed different amounts of colostrum or milk replacer: group C6 was fed colostrum six times (milkings 1-6 on d 1-d 3) and then milk replacer, group C1 was fed colostrum only once (first milking on d 1) and group M was fed only milk replacer (no colostrum). Arrows mark time of feeding. Values are means ± SEM, n = 6 (groups C6 and C1) or n = 5 (group M).
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Fig 5.
Profile of blood plasma cortisol concentrations in calves fed different amounts of colostrum or milk replacer: group C6 was fed colostrum six times (milkings 1-6 on d 1-d 3) and then milk replacer, group C1 was fed colostrum only once (first milking on d 1) and group M was fed only milk replacer (no colostrum). Blood samples were taken every 20 min for 8 h on d 7. Arrows mark time of feeding. Values are means ± SEM, n = 6 (groups C6 and C1) or n = 5 (group M).
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Table 4.
Blood plasma or serum concentrations of 3.5.3 
-triiodthyronine (T3), thyroxine (T4), and prolactin (PRL) in the first week of life of neonatal calves fed colostrum six times (C6), fed colostrum only on the first meal (C1) or fed only milk replacer (M)1
DISCUSSION
Abstract
Introduction
Methods
Results
Discussion
References
, Stott and Fellah 1983), feeding first colostrum is very important for the IgG status in newborn calves. Additional colostrum feeding seems to elevate plasma IgG concentrations for a prolonged time, as also described by Morin et al. (1997).
GT (Vacher and Blum 1993) and a rapid rise of plasma GT activity on d 1 in groups C6 and C1 reflected colostrum absorption, in accordance with previous studies (Baumrucker et al. 1994a, Hadorn and Blum 1997). Other enzymes, such as AST, LDH and GLDH, too, were present in higher amounts in first colostrum than in milking 6 and milk replacer. Plasma enzyme activities increased on d 1 after colostrum but not after milk replacer intake. Kurz and Willett (1991), too, described increased activities of GT and AST after colostrum intake. It seems possible that absorption of these colostral enzymes may be an important cause of enhanced blood enzyme activities in our newborn calves on d 1 of life. However, plasma AST activity in calves fed only milk replacer was higher on d 2 than on d 1. Therefore, reasons other than colostrum intake may contribute to enhanced activities of some enzymes in blood after birth.
). Colostral lipase improved fat digestion in human newborns (Hamosh 1997). This may be one of several causes for enhanced fat absorption in colostrum-fed calves, too. Fat is the main energy source for the newborn (Ferré et al. 1986, Leat 1967). High amounts of ingested fat and increased fat absorption thus would contribute to an improved energy status in colostrum-fed calves. Although not statistically different, plasma NEFA concentrations were 70% higher in C6 calves than in M calves at d 2 of age. On the other hand, calves in this study did not show an increase of plasma NEFA concentrations as found recently in food-deprived neonatal calves (Hadorn et al. 1997).
, Tivey et al. 1994). Elevated plasma glucose concentrations on d 2 also may have been a consequence of enhanced glucose absorption capacity from the gut by colostrum feeding as shown in the same calves (Hammon and Blum 1997a).
, Girard 1986). Plasma lactate, the concentrations of which were high after birth, may have served as an important substrate for gluconeogenesis. Colostrum expectedly provided more gluconeogenic substrates than did milk replacer. In human newborns, gluconeogenesis from lactic acid, glycerol and alanine increased within the first 8 h of life (Ferré et al. 1986), and in neonatal colostrum-fed pigs, gluconeogenesis too was enhanced by colostrum feeding (Lepine et al. 1989). Concentrations of essential amino acids and especially of glutamic acid were elevated in colostrum-fed calves (Hammon, H. M. and Blum, J. W., unpublished data) and likely served as gluconeogenic substrates and possibly enhanced the secretion of glucagon. Gluconeogenesis may have been enhanced by glucagon, the plasma concentrations of which increased more on d 1 and d 2 after colostrum than after milk replacer intake. Possibly the demand for glucose via gluconeogenesis was greater in C6 calves because these calves were still fed colostrum with a higher fat and lower carbohydrate content compared with C1 and M calves, which were fed a milk replacer containing less fat and more carbohydrates. A plasma glucagon rise after colostrum intake also was reported in pigs, rats and humans (Ferré et al. 1986, Lepine et al. 1989) but to our knowledge has not yet been shown in calves. Higher glucose concentrations on d 2 in colostrum-fed calves were possibly also a consequence of higher gluconeogenesis rate due to colostrum feeding (Girard 1986).
and Lee et al. (1995). Higher insulin concentrations on d 2 in C6 calves, i.e., greater insulin responses to colostrum feeding, may have been because of higher fat and especially energy intake. There were no significant postprandial increases in plasma insulin concentrations on d 7 even though there was a substantial numerical increase after feeding in group C6. Greater insulin responses to colostrum feeding and prolonged effects of colostrum feeding on insulin secretion were shown previously (Hadorn et al. 1997). A link between insulin and glucagon seems to exist in newborn calves, which are characterized by relatively high levels of plasma insulin and glucagon if fed intensively with colostrum (Lepine et al. 1989).
, Hadorn et al. 1997, Kurz and Willett 1991, Lee et al. 1995). Interestingly, cortisol concentrations on d 2 and on d 7 were elevated in calves fed only milk replacer relative to those fed colostrum, a finding not previously reported. In neonatal pigs, cortisol concentrations were highest in food-deprived neonates and lowest in those fed colostrum (Lepine et al. 1989). Cortisol is part of the glucoregulatory endocrine system and stimulates gluconeogenesis in liver. It seems possible that in neonates not fed colostrum, cortisol is important for glucose homeostasis. Whether colostrum intake reduces the stress level and, as a consequence the cortisol level, remains to be evaluated.
, Kahl et al. 1977, Ronge and Blum 1988). Studies of Grongnet et al. (1985), who showed an influence in neonatal calves on the thyroid status dependent on the intensity of colostrum feeding, were not confirmed by our study. However, T3 levels were twice as high in group M as in groups C6 or C1 at d 2 of age although this difference was not significant. Whether the T3 decline in plasma after birth is influenced by colostrum intake is speculative and needs further investigation.
, Lee et al. 1995). This was also the case in our study, but on d 7 basal PRL concentrations were higher in calves fed colostrum six times than in calves in the other groups. The physiologic importance of this finding is not clear. However, Baumrucker and Blum (1994) reported higher PRL concentrations in newborn calves fed IGF-I together with milk replacer.
) indicated that anabolic metabolism was enhanced in calves fed colostrum twice per day for 3 d, supporting previous studies (Blum et al. 1997, Hadorn et al. 1997). Reasons for improved anabolic metabolism could be the high amounts of colostrum components, which provide substrates for gluconeogenesis and for protein synthesis (Ferré et al. 1986, Girard 1986, Lepine et al. 1989 and 1991). Additionally, colostrum provides biologically active substances, some with growth promoting potential and that contribute to maturation of the gastrointestinal tract (Baumrucker et al. 1994b, Burrin et al. 1995, Odle et al. 1996). Our data support previous findings that colostrum intake not only improves passive immunity, but in addition has marked effects on metabolism and on the hormonal status.
ACKNOWLEDGMENTS
1
Part of this study was presented at the Symposium on Milk Synthesis, Secretion and Removal in Ruminants, April 26-27, 1996, University of Berne, Berne, Switzerland [Hammon, H. & Blum J. W. (1996) Effects of feeding different amounts of colostrum on metabolic and endocrine traits in neonatal calves. In: Symposium on Milk Synthesis, Secretion and Removal in Ruminants (Blum, J. W. & Bruckmaier, R. M., eds.), p. 77. University of Berne, Berne, Switzerland.].
FOOTNOTES
2
Supported by Swiss National Science Foundation Grant 32-36140.92.
3
The costs of publication of this article were defrayed in part
by the payment of page charges. This article must therefore be hereby marked "advertisement"
in accordance with 18 USC section 1734 solely to indicate this fact.
4
To whom correspondence should be addressed.
5
Abbreviations used: AST, aspartate-aminotransferase (EC 2.6.1.1); BW, body weight; GLDH, glutamate-dehydrogenase (EC 1.4.1.3); group C6, calves fed colostrum six times; group C1, calves fed colostrum once; group M, calves fed no colostrum; GT, -glutamyltransferase (EC 2.3.2.2); IGF-I, insulin-like growth factor I; IgG, immunoglobulin G; LDH, lactate-dehydrogenase (EC 1.1.1.27); NEFA, non-esterified fatty acids; PRL, prolactin; T3, 3.5.3-triiodthyronine; T4, thyroxine.
LITERATURE CITED
Abstract
Introduction
Methods
Results
Discussion
References
-glutamyl transferase in blood.
Domest. Anim. Endocrinol.
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11:393-403
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-tocopherol status in the neonatal calves. J. Nutr. 127: 2024-2029, 1997. -glutamyltransferase activities in calves. J. Vet. Med. Ser. A (in press). -glutamyl-transferase activity in first colostrum of dairy cows.
Milk Sci. Int.
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48:423-426
0022-3166/98 $3.00 ©1998 American Society for Nutritional Sciences
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