- Email: [email protected]
Effect of bovine serum albumin on passive transfer of immunoglobulin G1 to newborn calves
Veterinary Immunology and Iln,nunopatholog),, 37 ( 1993) 32 l-327 Elsevier Science Publishers
321
B.V., Amsterdam
Effect of bovine serum albumin on passive transfer of immunoglobulin Gl to newborn calves Thomas E. Besserand Dian Osbom Department of VeterinaryMicrobiology and Pathology, WashingtonState University,Pullman, WA 99164-7040, USA (Accepted 9 September 1992)
ABSTRACT Besser, T.E. and Osbom, D., 1993. Effect of bovine serum albumin on passive transfer of immunoglobulin Gl to newborn calves. Vet.Immunol. Immunopathol., 37: 321-327. The molecular mechanism in the intestine of newborn calves that results in transfer of intact colostral immunoglobulin from the lumen to the circulation also is capable of transferring a variety of nonimmunoglobulin macromolecules. If the capacity of this mechanism is limited, transfer of a large amount of non-immunoglobulin protein may interfere with transfer of immunoglobulin. In this experiment, efficiency of IgG 1 transfer in newborn calves was reduced from 59 to 36% by the addition of bovine serum albumin (37 mg ml-’ ) to colostral whey, while the addition of a similar mass of amino acids in the form of acid hydrolyzed casein (37 mg ml-‘) did not detectably alter IgGl transfer. Reduced IgGl absorption effkiency in calves fed colostrum with added bovine serum albumin is consistent with a limited capacity for the macromolecular transport mechanism in the intestine of newborn calves.
INTRODUCTION
Passive transfer of maternal antibody to newborn calves is important for resistanceto infectious diseaseduring the neonatal period (reviewed by Gay, 1983). Calves are born nearly agammaglobulinemic, but during the first day of life are capableof transferring intact immunoglobulin from ingestedcolostrum to the intestinal lymph, which then entersthe circulation. The molecular mechanism in newborn calves that transfers intact colostral immunoglobulin from the lumen acrossthe intestinal epithelium to the circulation is also capable of transferring immunoglobulins from other species,non-immunoglobulin proteins normally found in colostrum such as/Mactoglobulin and casein (Bangham et al., 1958; Pierce, 1961), and non-immunoglobulin macromolecules such as bovine serum albumin (Balfour, 1959) and polyvinylpyrroliCorrespondenceto: Thomas E. Besser, Department Washington
State University,
Pullman,
0 1993 Elsevier Science Publishers
of Veterinary WA 99 164-7040, USA.
Microbiology
B.V. All rights reserved 0165-2427/93/$06.00
and Pathology,
32’
T.E. HESSER AND
D. OSBORN
done (Hardy, 1969). If the total capacity of this transport mechanism is limited. it is possible that non-immunoglobulin protein in colostrum could reduce the amount of immunoglobulin absorbed. This experiment was designed to determine if bovine serum albumin, a non-immunoglobulin protein that is known to be transported across the newborn calf intestine, would limit colostral immunoglobulin G 1 transport. MATERIALS
AND METHODS
Calves Sixteen newborn male Holstein calves were studied over a 2 day period. At birth, calves were removed from their dam before natural suckling occurred, weighed, and assigned to experimental treatment groups. The appropriate colostrum feeding treatment was given to each calf at 1 h after birth by esophageal tube feeder. Blood samples were obtained from each calf for IgGl analysis before colostrum feeding and at 6 and 12 h after colostrum feeding.
Plasma volume Plasma volumes were measured using Evans blue dye at 12 h after colostrum feeding (McEwan et al., 1968).
Immunoglobulin analysis IgGl concentrations in calf serum samples and in colostrum were determined by radial immunodiffusion (Besser et al., 1985 ). Efficiency of IgG 1 absorption was calculated according to the method of Husband et al. ( 1973)) using the formula Efficiency
(%) =
[Calf plasma ( IgG 1) x Calf plasma vol. ] Efficiency (O/o) = (Mass IgG 1 ingested) x 100%
Colostrum Colostral whey rather than whole colostrum was used as an IgG 1 source to feed all calves in this experiment. Fresh first-milking colostrum was treated to extract whey. First, fat was removed by centrifugation (3000 xg, 30 min, 4°C Beckman 52-21, JA-14 rotor). Casein was then clotted with rennin ( 1 mg rennin per 750 ml colostrum, 30°C for 1 h) and pelleted by centrifugation ( 15000 xg, 30 min, 4°C centrifuge and rotor as in I). Supernatant whey was pooled and frozen until warmed for calf feedings. A single pool of colostral
TRANSFER
OF IMMUNOGLOBULIN
G I TO CALVES
323
whey containing 42 mg ml- ’ IgG 1 was usedto make the colostrum treatment solutions. Experimental treatments Calves were randomly assigned to one of four groups receiving different colostrum treatments. Bovine serum albumin (United States Biochemical Corporation, Cleveland, OH) and hydrolyzed casein (Acid-hydrolyzed casein, C-9386, Sigma Chemical Company, St. Louis, MO) were obtained. Colostrum treatments consisted of colostral whey (37.5 ml kg-’ body weight) to which was added an equal volume of a solution containing water only for Group 1, bovine serum albumin (74 mg ml-‘) in water for Group 2, hydrolyzed casein ( 74 mg ml- ’ ) in water for Group 3, and bovine serum albumin (74 mg ml-’ ) and hydrolyzed casein (74 mg ml- ’ ) in water for Group 4. Therefore, eachcalf received a total feedingvolume of 75 ml kg-’ body weight. IgGl concentration measured in the colostrum treatments as fed to calves averaged20.9mgml-’ (SE 1.5mgml-‘).
Fig. 1. SDS-PAGE electrophoretogram of colostral whey treatments fed to calves. Bands in Lane S are molecular weight standards (kD). Lanes marked l-4 contain colostral whey with: ( 1) added distilled water; (2) added bovine serum a!bumin in distilled water; (3) added hydrolyzed casein in distilled water; (4) added bovine serum albumin and hydrolyzed casein in distilled water, respectively. Stain is Coomassie brilliant blue.
324
T.E. BESSER AND
D. OSBORN
Analysis of colostrum treatments supplemented with hydrolyzed casein by polyacrylamide gel electrophoresis in the presenceof sodium dodecyl sulfate (SDS-PAGE) did not reveal any residual non-hydrolyzed casein, while SDSPAGE of colostrum treatments supplemented with bovine serum albumin demonstrated the presenceof bovine serum albumin of the appropriate molecular size (Fig. 1). Colostrum treatments lacking bovine serum albumin supplementation contained 44-50 mg ml-’ total protein, while those supplemented with bovine serum albumin contained 83-84 mg ml-’ total protein, as determined by the Biuret procedure (Peters et al., 1982). These data were interpreted to indicate that the casein hydrolysate was essentially free of intact macromolecular protein. Experimental
design
The experimental design was a 2 x 2 randomized complete block, with two independent factors (bovine serum albumin and casein treatments to colostral whey), and four calves per block. Data was analyzed by an analysis of variance procedure (Proc GLM, SAS User’s Guide: Statistics, Ver. 5, SAS Institute, Cary, NC). Plasma volume was included in the model as a co-variate to evaluatethe possibility that the treatments might have different effects on plasma volume expansion, indirectly affecting the IgG 1 concentrations. RESULTS
Effjkiency
of IgGl absorption
Bovine serum albumin added to colostral whey inhibited absorption of IgG 1 to serum by newborn calves (PC 0.0 1)) while the same mass of amino acids, in the form of hydrolyzed casein, did not affect IgG 1absorption (Fig. 2 ). The averageefficiency of absorption of IgG 1 to plasma in calvesfed colostral whey with added bovine serum albumin was 36%, compared with 59% in calves in groups without added bovine serum albumin. No significant interaction between the effects of bovine serum albumin and casein was detected. Plasma volume
Becausethe absorption of bovine serum albumin might tend to expand plasma volume and dilute absorbedIgG 1, plasma volumes were measured at 12 h after colostrum treatment administration. Plasma volumes in the calves averaged8.9% of body weight (range 7.4-l 2.5%), and did not differ significantly between treatment groups. Therefore, plasma volume expansion did not causedecreasedserum IgG 1 concentration in calves fed colostrum treatments supplemented with bovine serum albumin.
TRANSFER
OF IMMlINOC~LOBlILIN
Cl TO C.ALVES
325
r
3
L Control
CaCIeln
Treatment
BSA
BSA
+
caasin
Croup
Fig. 2. Serum IgG I concentrations resulting from colostrum whey feedings lo newborn calves. .Addition of intact bovine strum albumin (BS.4) to (tic colostral whey rcsullcd in dccrcascd IgG I absorption to strum. white addition of hydrolyzed cascin (Cascin) had no cffcct. (Error bars. standard deviation within each group. II. four within each group.) DISCUSSION
Interference with colostral IgG 1 absorption by the presence of bovine serum albumin is consistent with the hypothesis that the macromolecular transport system in the intestine of the neonatal calf has a limited capacity, which can be exhausted by both immunoglobulin and non-immunoglobulin protein. The reduction in efficiency of immunoglobulin absorption per gram of albumin is similar in magnitude to the reduction in efficiency of immunoglobulin absorption per gram of additional colostral immunoglobulin (Besser et al., 1985 ). For example, calves in bovine serum albumin treatment groups in the present experiment received an average of 149 grams of protein (bovine serum albumin + IgG 1) in their colostral whey, and absorbed IgG 1 with a mean efficiency of 36%, similar to the absorptive efficiency for IgGl of 33% previously demonstrated in calves fed 140-200 g colostral IgGl (Besser et al., 1985 ). Calves fed colostrum unsupplemented with bovine serum albumin in this experiment averaged a 34 g protein ( IgG 1) intake, and absorbed with an average efficiency of 59%, somewhat better than the 48% efficiency previously demonstrated in calves fed < 84 g colostral IgG 1 (Besser et al., 1985 ). Other investigators have reported both enhancement and inhibition of immunoglobulin transfer by serum albumin, Leary and Lecce ( 1979) showed serum albumin enhanced porcine IgG uptake by enterocytes in ligated intestinal loops. However, this result may have been simply owing to albumin providing the minimal protein concentration required for significant uptake of IgG in piglets (Smith et al., 1979). Pierce et al. ( 1967b) showed that human serum albumin (5.2 g per 100 ml) in colostrum inhibited transfer of bovine
326
T.E. BESSEK AND
D. CFiBOKN
colostral IgG to the serosal surface by everted piglet intestines. However, the overall protein transfer rate in that experiment was very low, suggesting that the in vitro preparation was not representative of the absorptive process in intact piglets. The same authors found that human serum albumin (6.3 g per 100 ml) did not inhibit absorption of bovine colostral gammaglobulin (6.4 g per 100 ml), but fed the mixtures to newborn pigs at a rate of only 2% of body weight (Pierce et al., 1967a). In comparison with the present study, all previous studies in which serum albumin did not inhibit IgG 1 transport involved relatively small amounts of colostrum and/or albumin which may not have reached the limits of the transport mechanism. There is substantial calf-to-calf variability in colostral IgG 1 absorption, even in experiments where calves are fed measured doses from a single colostrum pool at a standard time after birth (Besser et al., 1983; Lee et al., 1983; Besser and Gay 1986). Some of this variability could result from interference by non-immunoglobulin protein, of which (non-hydrolyzed) caseins are the only candidates naturally present in colostrum in sufficient amounts to potentially limit IgG1 absorption. Consistent with this possibility, calves in this experiment fed colostral whey without bovine serum albumin supplementation had less variability in serum IgG 1 concentration (coefficient of variation: 7.5%) than did calves fed whole colostrum in previous experiments (coefficients of variation of 20.7%, Besser et al., 1983; 35.5%, Lee et al., 1983; and 25.9%, Besser et al., 1990).
REFERENCES Balfour. W.E. and Comline. R.S.. 1959. The specificity of intestinal absorption of large molccults by the newborn calf. J. Physiol.. 148: 77P-781’. Bangham. D.R.. Ingram. P.L.. Roy. J.H.B.. Shillam, K.W.G. and Terry. R.J., 1958. The absorption of “‘I-labelled strum and colostral protein from the gut of the young calf. Proc. R. Sot. (London) BI49: 184-191. Bcsser. T.E. and Gay. C.C., 1986. Septiccmic colibacillosis and failure of passive transfer of colostral immunoglobulin in calves. Vet. Clinics N. r\m.. Food .Anim. Pratt.. I: -145-459. Bcsscr. T.E.. Gay. C.C. and McGuirc, T.C.. l9S3. Serum IgG concentrations acquired by calves fed dam’s versus pooled colostrum. VIDO: Proc. Fourth Int Symp on Neonatal Diarrhea. October. pp. 379-387. Bcsscr. T.E.. Szenci. 0. and Gay. C.C.. 1990. Dccrcascd colostral immunoglobulin absorption in calves with postnatal respiratory acidosis. J. Am. Vet. Med. Assoc.. 196: I239- 1243. Bcsser, T.E.. Garmedia. A.E.. McGuirc. T.C. and Gay. C.C.. 1985. Effect of colostral immunoglobulin G I and immunoglobulin M concentrations on immunoglobulin absorption in calxs. J. Dairy Sci., 68: 2033-2037. Gay, C.C.. 1983. Failure of passive transfer of colostrul immunoglobulins and neonatal discasc in calves: .A review. VIDO: Proc. Fourth Int Symp on Neonatal Diarrhea. October. pp. 346364. Hardy. R.N.. 1969. The influcncc of specific chemical factors in the sol\,cnt on the absorption
TRANSFER
OF IMMUNOGLOBULIN
GI TO CALVES
327
of macromolecular substancesfrom the small intestine of the newborn calf. J. Physiol., 204: 607-632. Husband, A.J., Brandon, M.R. and Lascelles,A.K., 1973. The effects of corticosteroids on absorption and endogenous production of immunoglobulins in calves.Aust. J. Exp. Biol. Med. Sci., 5 1: 707-7 10. Leary, H.L. and Lecce, J.G., 1979. The preferential transport of immunoglobulin Gl by the small intestine of the neonatal pig. J. Nutr., 109: 458-466. Lee, R.B., Besser,T.E., Gay, C.C. and McGuire, T.C., 1983. The influence of method of feeding colostrum on IgG concentrations acquired by calves.VIDO: Proc. Fourth Int Symp on Neonatal Diarrhea, October, pp. 372-378. McEwan, A.D., Fisher, E.W. and Selman, I.E., 1968. The effect of colostrum on the volume and composition of the plasma of calves. Res. Vet. Sci., 9: 284-286. Peters, T., Beamonte, G.T. and Dourmas, B.T., 1982. Protein in urine, serum, and CSF. In: W.R. Faulkner and S. Meites (Editors), Selectedmethods in clinical chemistry, vol. 9, Am. Assoc.Clin. Chem., Washington, DC, pp. 3 17-325. Pierce, A.E., 1961. Further studies on proteinuria in the newborn calf. J. Physiol., 156: 136149. Pierce, A.E. and Smith, M.W., 1967a. The intestinal absorption of pig and bovine lactoglobulins and human serum albumin by the newborn pig. J. Physiol. (Lond.), 190: I-l 8. Pierce, A.E. and Smith, M.W., 1967b. The in vitro transfer of bovine lactoglobulins acrossthe intestine of newborn pigs. J. Physiol. (Lond.), 190: 19-34. Smith, M.W., Burton, K.A. and Munn, E.A., 1979. Vacuolation and non-specific protein transport by the newborn pig intestine. In: W.A. Hemmings (Editor), Protein transmission through living membranes. Elsevier, Amsterdam, pp. 197-2 12.
321
B.V., Amsterdam
Effect of bovine serum albumin on passive transfer of immunoglobulin Gl to newborn calves Thomas E. Besserand Dian Osbom Department of VeterinaryMicrobiology and Pathology, WashingtonState University,Pullman, WA 99164-7040, USA (Accepted 9 September 1992)
ABSTRACT Besser, T.E. and Osbom, D., 1993. Effect of bovine serum albumin on passive transfer of immunoglobulin Gl to newborn calves. Vet.Immunol. Immunopathol., 37: 321-327. The molecular mechanism in the intestine of newborn calves that results in transfer of intact colostral immunoglobulin from the lumen to the circulation also is capable of transferring a variety of nonimmunoglobulin macromolecules. If the capacity of this mechanism is limited, transfer of a large amount of non-immunoglobulin protein may interfere with transfer of immunoglobulin. In this experiment, efficiency of IgG 1 transfer in newborn calves was reduced from 59 to 36% by the addition of bovine serum albumin (37 mg ml-’ ) to colostral whey, while the addition of a similar mass of amino acids in the form of acid hydrolyzed casein (37 mg ml-‘) did not detectably alter IgGl transfer. Reduced IgGl absorption effkiency in calves fed colostrum with added bovine serum albumin is consistent with a limited capacity for the macromolecular transport mechanism in the intestine of newborn calves.
INTRODUCTION
Passive transfer of maternal antibody to newborn calves is important for resistanceto infectious diseaseduring the neonatal period (reviewed by Gay, 1983). Calves are born nearly agammaglobulinemic, but during the first day of life are capableof transferring intact immunoglobulin from ingestedcolostrum to the intestinal lymph, which then entersthe circulation. The molecular mechanism in newborn calves that transfers intact colostral immunoglobulin from the lumen acrossthe intestinal epithelium to the circulation is also capable of transferring immunoglobulins from other species,non-immunoglobulin proteins normally found in colostrum such as/Mactoglobulin and casein (Bangham et al., 1958; Pierce, 1961), and non-immunoglobulin macromolecules such as bovine serum albumin (Balfour, 1959) and polyvinylpyrroliCorrespondenceto: Thomas E. Besser, Department Washington
State University,
Pullman,
0 1993 Elsevier Science Publishers
of Veterinary WA 99 164-7040, USA.
Microbiology
B.V. All rights reserved 0165-2427/93/$06.00
and Pathology,
32’
T.E. HESSER AND
D. OSBORN
done (Hardy, 1969). If the total capacity of this transport mechanism is limited. it is possible that non-immunoglobulin protein in colostrum could reduce the amount of immunoglobulin absorbed. This experiment was designed to determine if bovine serum albumin, a non-immunoglobulin protein that is known to be transported across the newborn calf intestine, would limit colostral immunoglobulin G 1 transport. MATERIALS
AND METHODS
Calves Sixteen newborn male Holstein calves were studied over a 2 day period. At birth, calves were removed from their dam before natural suckling occurred, weighed, and assigned to experimental treatment groups. The appropriate colostrum feeding treatment was given to each calf at 1 h after birth by esophageal tube feeder. Blood samples were obtained from each calf for IgGl analysis before colostrum feeding and at 6 and 12 h after colostrum feeding.
Plasma volume Plasma volumes were measured using Evans blue dye at 12 h after colostrum feeding (McEwan et al., 1968).
Immunoglobulin analysis IgGl concentrations in calf serum samples and in colostrum were determined by radial immunodiffusion (Besser et al., 1985 ). Efficiency of IgG 1 absorption was calculated according to the method of Husband et al. ( 1973)) using the formula Efficiency
(%) =
[Calf plasma ( IgG 1) x Calf plasma vol. ] Efficiency (O/o) = (Mass IgG 1 ingested) x 100%
Colostrum Colostral whey rather than whole colostrum was used as an IgG 1 source to feed all calves in this experiment. Fresh first-milking colostrum was treated to extract whey. First, fat was removed by centrifugation (3000 xg, 30 min, 4°C Beckman 52-21, JA-14 rotor). Casein was then clotted with rennin ( 1 mg rennin per 750 ml colostrum, 30°C for 1 h) and pelleted by centrifugation ( 15000 xg, 30 min, 4°C centrifuge and rotor as in I). Supernatant whey was pooled and frozen until warmed for calf feedings. A single pool of colostral
TRANSFER
OF IMMUNOGLOBULIN
G I TO CALVES
323
whey containing 42 mg ml- ’ IgG 1 was usedto make the colostrum treatment solutions. Experimental treatments Calves were randomly assigned to one of four groups receiving different colostrum treatments. Bovine serum albumin (United States Biochemical Corporation, Cleveland, OH) and hydrolyzed casein (Acid-hydrolyzed casein, C-9386, Sigma Chemical Company, St. Louis, MO) were obtained. Colostrum treatments consisted of colostral whey (37.5 ml kg-’ body weight) to which was added an equal volume of a solution containing water only for Group 1, bovine serum albumin (74 mg ml-‘) in water for Group 2, hydrolyzed casein ( 74 mg ml- ’ ) in water for Group 3, and bovine serum albumin (74 mg ml-’ ) and hydrolyzed casein (74 mg ml- ’ ) in water for Group 4. Therefore, eachcalf received a total feedingvolume of 75 ml kg-’ body weight. IgGl concentration measured in the colostrum treatments as fed to calves averaged20.9mgml-’ (SE 1.5mgml-‘).
Fig. 1. SDS-PAGE electrophoretogram of colostral whey treatments fed to calves. Bands in Lane S are molecular weight standards (kD). Lanes marked l-4 contain colostral whey with: ( 1) added distilled water; (2) added bovine serum a!bumin in distilled water; (3) added hydrolyzed casein in distilled water; (4) added bovine serum albumin and hydrolyzed casein in distilled water, respectively. Stain is Coomassie brilliant blue.
324
T.E. BESSER AND
D. OSBORN
Analysis of colostrum treatments supplemented with hydrolyzed casein by polyacrylamide gel electrophoresis in the presenceof sodium dodecyl sulfate (SDS-PAGE) did not reveal any residual non-hydrolyzed casein, while SDSPAGE of colostrum treatments supplemented with bovine serum albumin demonstrated the presenceof bovine serum albumin of the appropriate molecular size (Fig. 1). Colostrum treatments lacking bovine serum albumin supplementation contained 44-50 mg ml-’ total protein, while those supplemented with bovine serum albumin contained 83-84 mg ml-’ total protein, as determined by the Biuret procedure (Peters et al., 1982). These data were interpreted to indicate that the casein hydrolysate was essentially free of intact macromolecular protein. Experimental
design
The experimental design was a 2 x 2 randomized complete block, with two independent factors (bovine serum albumin and casein treatments to colostral whey), and four calves per block. Data was analyzed by an analysis of variance procedure (Proc GLM, SAS User’s Guide: Statistics, Ver. 5, SAS Institute, Cary, NC). Plasma volume was included in the model as a co-variate to evaluatethe possibility that the treatments might have different effects on plasma volume expansion, indirectly affecting the IgG 1 concentrations. RESULTS
Effjkiency
of IgGl absorption
Bovine serum albumin added to colostral whey inhibited absorption of IgG 1 to serum by newborn calves (PC 0.0 1)) while the same mass of amino acids, in the form of hydrolyzed casein, did not affect IgG 1absorption (Fig. 2 ). The averageefficiency of absorption of IgG 1 to plasma in calvesfed colostral whey with added bovine serum albumin was 36%, compared with 59% in calves in groups without added bovine serum albumin. No significant interaction between the effects of bovine serum albumin and casein was detected. Plasma volume
Becausethe absorption of bovine serum albumin might tend to expand plasma volume and dilute absorbedIgG 1, plasma volumes were measured at 12 h after colostrum treatment administration. Plasma volumes in the calves averaged8.9% of body weight (range 7.4-l 2.5%), and did not differ significantly between treatment groups. Therefore, plasma volume expansion did not causedecreasedserum IgG 1 concentration in calves fed colostrum treatments supplemented with bovine serum albumin.
TRANSFER
OF IMMlINOC~LOBlILIN
Cl TO C.ALVES
325
r
3
L Control
CaCIeln
Treatment
BSA
BSA
+
caasin
Croup
Fig. 2. Serum IgG I concentrations resulting from colostrum whey feedings lo newborn calves. .Addition of intact bovine strum albumin (BS.4) to (tic colostral whey rcsullcd in dccrcascd IgG I absorption to strum. white addition of hydrolyzed cascin (Cascin) had no cffcct. (Error bars. standard deviation within each group. II. four within each group.) DISCUSSION
Interference with colostral IgG 1 absorption by the presence of bovine serum albumin is consistent with the hypothesis that the macromolecular transport system in the intestine of the neonatal calf has a limited capacity, which can be exhausted by both immunoglobulin and non-immunoglobulin protein. The reduction in efficiency of immunoglobulin absorption per gram of albumin is similar in magnitude to the reduction in efficiency of immunoglobulin absorption per gram of additional colostral immunoglobulin (Besser et al., 1985 ). For example, calves in bovine serum albumin treatment groups in the present experiment received an average of 149 grams of protein (bovine serum albumin + IgG 1) in their colostral whey, and absorbed IgG 1 with a mean efficiency of 36%, similar to the absorptive efficiency for IgGl of 33% previously demonstrated in calves fed 140-200 g colostral IgGl (Besser et al., 1985 ). Calves fed colostrum unsupplemented with bovine serum albumin in this experiment averaged a 34 g protein ( IgG 1) intake, and absorbed with an average efficiency of 59%, somewhat better than the 48% efficiency previously demonstrated in calves fed < 84 g colostral IgG 1 (Besser et al., 1985 ). Other investigators have reported both enhancement and inhibition of immunoglobulin transfer by serum albumin, Leary and Lecce ( 1979) showed serum albumin enhanced porcine IgG uptake by enterocytes in ligated intestinal loops. However, this result may have been simply owing to albumin providing the minimal protein concentration required for significant uptake of IgG in piglets (Smith et al., 1979). Pierce et al. ( 1967b) showed that human serum albumin (5.2 g per 100 ml) in colostrum inhibited transfer of bovine
326
T.E. BESSEK AND
D. CFiBOKN
colostral IgG to the serosal surface by everted piglet intestines. However, the overall protein transfer rate in that experiment was very low, suggesting that the in vitro preparation was not representative of the absorptive process in intact piglets. The same authors found that human serum albumin (6.3 g per 100 ml) did not inhibit absorption of bovine colostral gammaglobulin (6.4 g per 100 ml), but fed the mixtures to newborn pigs at a rate of only 2% of body weight (Pierce et al., 1967a). In comparison with the present study, all previous studies in which serum albumin did not inhibit IgG 1 transport involved relatively small amounts of colostrum and/or albumin which may not have reached the limits of the transport mechanism. There is substantial calf-to-calf variability in colostral IgG 1 absorption, even in experiments where calves are fed measured doses from a single colostrum pool at a standard time after birth (Besser et al., 1983; Lee et al., 1983; Besser and Gay 1986). Some of this variability could result from interference by non-immunoglobulin protein, of which (non-hydrolyzed) caseins are the only candidates naturally present in colostrum in sufficient amounts to potentially limit IgG1 absorption. Consistent with this possibility, calves in this experiment fed colostral whey without bovine serum albumin supplementation had less variability in serum IgG 1 concentration (coefficient of variation: 7.5%) than did calves fed whole colostrum in previous experiments (coefficients of variation of 20.7%, Besser et al., 1983; 35.5%, Lee et al., 1983; and 25.9%, Besser et al., 1990).
REFERENCES Balfour. W.E. and Comline. R.S.. 1959. The specificity of intestinal absorption of large molccults by the newborn calf. J. Physiol.. 148: 77P-781’. Bangham. D.R.. Ingram. P.L.. Roy. J.H.B.. Shillam, K.W.G. and Terry. R.J., 1958. The absorption of “‘I-labelled strum and colostral protein from the gut of the young calf. Proc. R. Sot. (London) BI49: 184-191. Bcsser. T.E. and Gay. C.C., 1986. Septiccmic colibacillosis and failure of passive transfer of colostral immunoglobulin in calves. Vet. Clinics N. r\m.. Food .Anim. Pratt.. I: -145-459. Bcsscr. T.E.. Gay. C.C. and McGuirc, T.C.. l9S3. Serum IgG concentrations acquired by calves fed dam’s versus pooled colostrum. VIDO: Proc. Fourth Int Symp on Neonatal Diarrhea. October. pp. 379-387. Bcsscr. T.E.. Szenci. 0. and Gay. C.C.. 1990. Dccrcascd colostral immunoglobulin absorption in calves with postnatal respiratory acidosis. J. Am. Vet. Med. Assoc.. 196: I239- 1243. Bcsser, T.E.. Garmedia. A.E.. McGuirc. T.C. and Gay. C.C.. 1985. Effect of colostral immunoglobulin G I and immunoglobulin M concentrations on immunoglobulin absorption in calxs. J. Dairy Sci., 68: 2033-2037. Gay, C.C.. 1983. Failure of passive transfer of colostrul immunoglobulins and neonatal discasc in calves: .A review. VIDO: Proc. Fourth Int Symp on Neonatal Diarrhea. October. pp. 346364. Hardy. R.N.. 1969. The influcncc of specific chemical factors in the sol\,cnt on the absorption
TRANSFER
OF IMMUNOGLOBULIN
GI TO CALVES
327
of macromolecular substancesfrom the small intestine of the newborn calf. J. Physiol., 204: 607-632. Husband, A.J., Brandon, M.R. and Lascelles,A.K., 1973. The effects of corticosteroids on absorption and endogenous production of immunoglobulins in calves.Aust. J. Exp. Biol. Med. Sci., 5 1: 707-7 10. Leary, H.L. and Lecce, J.G., 1979. The preferential transport of immunoglobulin Gl by the small intestine of the neonatal pig. J. Nutr., 109: 458-466. Lee, R.B., Besser,T.E., Gay, C.C. and McGuire, T.C., 1983. The influence of method of feeding colostrum on IgG concentrations acquired by calves.VIDO: Proc. Fourth Int Symp on Neonatal Diarrhea, October, pp. 372-378. McEwan, A.D., Fisher, E.W. and Selman, I.E., 1968. The effect of colostrum on the volume and composition of the plasma of calves. Res. Vet. Sci., 9: 284-286. Peters, T., Beamonte, G.T. and Dourmas, B.T., 1982. Protein in urine, serum, and CSF. In: W.R. Faulkner and S. Meites (Editors), Selectedmethods in clinical chemistry, vol. 9, Am. Assoc.Clin. Chem., Washington, DC, pp. 3 17-325. Pierce, A.E., 1961. Further studies on proteinuria in the newborn calf. J. Physiol., 156: 136149. Pierce, A.E. and Smith, M.W., 1967a. The intestinal absorption of pig and bovine lactoglobulins and human serum albumin by the newborn pig. J. Physiol. (Lond.), 190: I-l 8. Pierce, A.E. and Smith, M.W., 1967b. The in vitro transfer of bovine lactoglobulins acrossthe intestine of newborn pigs. J. Physiol. (Lond.), 190: 19-34. Smith, M.W., Burton, K.A. and Munn, E.A., 1979. Vacuolation and non-specific protein transport by the newborn pig intestine. In: W.A. Hemmings (Editor), Protein transmission through living membranes. Elsevier, Amsterdam, pp. 197-2 12.