The importance of passive transfer of colostral immunity on morbidity, mortality rate, and production has been well documented in calves.1–6 Currently, the prevalence of FPI in dairy heifer calves in the United States is reported as 19.2%.7 Method of colostral administration has been reported to be one of the more important factors that affect passive transfer of colostral immunity.8,9 Colostrum can be administered to calves by OET, NB, or nursing. In 2007 it was reported10 that 59% of dairy operations in the United States hand-fed colostrum from a bucket or NB, 4.3% fed colostrum by OET, and the remainder allowed calves to nurse from the dam.
Studies evaluating the effects of the method of colostral administration on passive immunity have varied in designs, results, and conclusions. Adams et al8 reported that colostral immunoglobulin absorption efficiency was improved when calves were fed through an NB, compared with OET, from 20 to 32 hours after first feeding, presumably because of closure of the esophageal groove directing the colostrum to the abomasum. However, it is not clear from the study whether the differences between the immunoglobulin absorption efficiencies between the NB and the OET group from 20 to 32 hours after first feeding were significantly different. However, the same study8 found no significant differences between serum IgG concentrations from calves fed equal amounts of colostral IgG mass by use of an NB or OET. A limitation to the study by Adams et al8 was that the calves enrolled in the study were of 4 dairy breeds (Holstein, Aryshire, Jersey, and Guernsey) that were fed a total colostrum volume of 10% of their weights, divided into 3 feedings: within 1 hour after birth, at 12 hours after birth, and at 24 hours after birth. Because the calves in that study8 received large total volumes of colostrum during the 24-hour period, all calves achieved adequate passive immunity. The comparison of efficiency of absorption between the NB and OET groups in the study by Adams et al8 was also confounded by the significant breed and season effects. Lateur-Riwett and Breukink11 investigated the anatomic site in which colostrum was deposited, the time it stayed in the forestomachs, and whether it was possible to stimulate esophageal groove closure (by teasing calf to suck on the handler's fingers) when colostrum was administered by OET. The study11 concluded that sufficient absorption of colostral immunoglobulins (on the basis of serum immunoglobulin concentrations at 24 hours after ingestion of colostrum) occurred in tubefed calves in the absence of closure of the esophageal groove because of the rapid flow of colostrum from the forestomachs to the abomasum and small intestine. The drawback in the study by Lateur-Riwett and Breukink11 was that there was no comparison group of calves fed by NB and the 3 Dutch Holstein-Friesian calves enrolled in the study were fed unreported volumes of colostrum by OET, 3 times after birth (8, 12, and 16 hours of age). In a study by Kaske et al,12 colostrum feeding by NB was compared with OET feeding on the basis of 24-hour postsuckle serum immunoglobulin concentration in Holstein-Friesian calves; however, volume of colostrum fed to calves in each group was not standardized. One group of calves was fed 4 L of colostrum through an OET, and the comparison group of calves was fed 2 L through an NB. Additionally, calves that did not ingest the 2 L offered through an NB were fed the remainder of the colostrum by an OET. Similarly, for calves in the OET group that could not swallow the tube or that vigorously resisted tubing, 200 mL of colostrum was fed by NB prior to further OET feeding.12 Therefore, in that study,12 ascertainment of the true effect of feeding method on postsuckle serum immunoglobulin concentrations was further confounded by the overlap in feeding methods.
Prevalence of FPI of colostral immunoglobulins was 61.4%, 19.3%, and 10.8% for dairy calves which nursed from their dams, were fed from an NB, and were fed by OET, respectively.9 Although higher prevalence of FPI was reported in calves fed colostrum by NB, compared with OET in a study by Besser et al,9 calves were only fed once by OET, whereas multiple feedings (immediately after birth followed by feeding every 12 hours for 48 hours) of colostrum were offered to the calves that were fed by NB. In a recent study13 comparing OET with NB feeding, Holstein calves fed small volumes of a colostrum replacer (1.5 L) by NB had higher AEA of colostral immunoglobulins, compared with calves fed a similar volume by OET. Godden et al13 found no differences in serum IgG concentrations and AEA between calves fed larger volumes (3 L) colostrum replacer by NB or OET. However, calves that did not voluntarily ingest 3 L of colostrum through an NB were fed the remainder of the colostrum by OET13; again, the overlap in feeding method confounded determination of the effect of feeding method on AEA of colostrum immunoglobulins and postsuckle serum IgG concentration.
Given the limitations of previous studies designs, the high FPI rate in dairy heifer calves, and the preference by most producers to administer colostrum by NB in the United States, we hypothesized the following: AEA of IgG would be lower in calves fed colostrum by NB, compared with OET; serum immunoglobulin (IgG, IgM, and IgA) concentrations at 48 hours after ingestion of colostrum would be lower in calves fed colostrum by NB, compared with OET; and FPI rates in calves fed colostrum by NB would be higher than in calves fed by OET. The objectives of the study reported here were to compare the AEA of IgG, serum immunoglobulin concentration at 48 hours after ingestion of colostrum, and FPI rates between calves fed colostrum by NB and OET.
Materials and Methods
Animals—Dairy bull calves (n = 26) acquired from a single dairy in northern California (northern Solano County) were separated immediately from their dams after parturition and prior to nursing and were delivered to the University of California-Davis Animal Science Research facility. Upon arrival at the facility, calves were weighed, identified by use of ear tags, and housed in single calf hutches. To allow procedures to be performed effectively, calves were delivered to the facility in 3 groups, a few days apart. Ten calves were delivered initially, followed by a second group of 10 calves and lastly 6 calves. Only calves delivered via normal parturition were enrolled in the study. Calf enrollment began in January 2010 and ended in February 2010, with enrollment being completed in 17 days. The study was approved by the University of California-Davis Institutional Animal Care and Use Committee.
Procedures—The time of birth of each calf was recorded, and age was expressed in hours. Calves were eligible to be paired together for this study if they were born within 30 minutes of each other. For each calf pair, a coin toss was used to allocate 1 calf into the OET (n = 13) or NB (13) group; following that allocation, the other calf was allocated to the other study group. Calves were enrolled in the study between the ages of 4 and 8 hours at the commencement of the procedures. Serum samples were collected from calves prior to each feeding of colostrum. Stored (stored through freezing) pooled colostrum collected from a single dairy farm was used for feeding each group of calves. An aliquot of colostrum (20 mL) was collected prior to each feeding for subsequent measurement of immunoglobulin concentration. Calves allocated to the NB group were allowed to voluntarily ingest up to 4 L of warm colostrum within a 20-minute period. The volume that each calf in the NB group voluntarily ingested within this period was then designated as the volume that was immediately fed by OET to the similarly aged calf. The time required for a calf in the NB group to ingest up to 4 L of colostrum within the 20-minute time limit was recorded. The time required for its cohort calf to be fed the identical volume of colostrum by OET was not recorded but typically took 3 to 6 minutes. Time for feeding by each method was not included in the analysis. Subsequently, a pair of similarly aged (age difference, < 30 minutes) calves received a similar volume of colostrum with comparable immunoglobulin concentrations. All calves were fed colostrum only once. Thereafter, calves were fed 2 L of milk replacera every 12 hours. All calves survived to at least 48 hours of age. Serum samples were collected at 48 hours of age for determination of serum immunoglobulin concentrations. Serum and colostrum samples were stored in cryogenic vialsb at −20°C until immunoglobulin concentration measurement. Colostral and serum immunoglobulin concentrations were determined within 3 months after sample collection.
Determination of serum and colostral immunoglobulin concentration—An indirect quantitative ELISA was used to measure IgG, IgM, and IgA in calf serum and in the colostrum fed to each pair of calves as previously described14 with some modifications in the procedure. Briefly, sheep anti-bovine immunoglobulins (IgG, IgM, and IgA)c were prepared by diluting 1:100 in 50mM calcium carbonate bufferd (pH, 9.0) followed by adding 100 μL of the diluted solution into a 96-well microtiter plate.e The solution was then incubated with gentle agitation by use of an agitatorf for 1 hour and stored overnight at 4°C. The plates were then washed 5 times with Tris-buffered saline solution (50mM Tris and 0.14M NaCl; pH, 8)g with a plate washer.h Nonspecific binding was blocked with 300 μL of Tris-buffered saline solution and 1.35% gelatini and incubation with gentle agitation by use of an agitator at room temperature (approx 22°C) for 1 hour followed by washing the plates 5 times with Tris-buffered saline solution with a plate washer.
Bovine standardsj for IgG, IgM, and IgA were prepared by serial dilutions in Tris-buffered saline solution and 1.35% gelatin to produce standard curves that would predict serum immunoglobulin concentration ranging from 0 to 3,000 mg/dL and colostral samples with immunoglobulin concentration ranging from 0 to 300 g/L. Bovine reference serumk and diluent (25mM Tris, 150mM NaCl, 2mM KCl, and 1.35% fish skin gelatin; pH, 7.4) were included as positive and negative controls, respectively. Serum samples for determination of IgG, IgM, and IgA were diluted 1:20,000, 1:2,000, and 1:1,000, respectively, with Tris-buffered saline solution and 1.35% gelatin. Colostrum samples for determination of IgG, IgM, and IgA were diluted 1:100,000, 1:50,000, and 1:50,000, respectively, with Tris-buffered saline solution and 1.35% gelatin. Following dilution, 100 μL of the diluted standards and samples were added in triplicates to the microtiter plates containing the sheep anti-bovine immunoglobulins (IgG, IgM, and IgA) followed by gentle agitation with an agitator. The plates were then washed 5 times with Tris-buffered saline solution with a plate washer. Following washing of the plates, 100 μL of sheep anti-bovine horseradish peroxidase conjugatel diluted 1:50,000 in horseradish peroxidase diluent and stabilizerm was added to the wells followed by incubation with gentle agitation at room temperature for 1 hour. The plates were then washed 5 times with Tris-buffered saline solution. This was followed by addition of 100 μL of 3, 3′, 5, 5′ tetramethyl benzidinen to the plate wells and incubation at room temperature in the dark for 20 minutes. Finally, the reaction was quenched and color stabilized by the addition of 100 μL of 0.5M sulfuric acid.o Absorbance for the samples was determined by use of a plate reader at 450 nm.p
The ELISA absorbance values were highly correlated with the dilution of each of the bovine immunoglobulin standards with coefficients of determination (R2) of 0.998, 0.973, and 0.999 for IgG, IgM, and IgG, respectively. The minimum detectable immunoglobulin concentration by use of this method was 6 mg/dL for each class of immunoglobulin. Calves with serum IgG concentration < 1,000 mg/dL at 48 hours of age were considered to have FPI.9
AEA determination—Apparent efficiency of absorption estimates efficiency of immunoglobulin absorption prior to cessation of the intestinal absorption.15 Apparent efficiency of absorption for IgG was determined as previously described15,16 by use of the following formula:
As previously reported by other investigators, a plasma volume of 9.9% was considered for the Holstein breed.15 Apparent efficiency of absorption for IgM and IgA was not determined.
Data analysis—Previous studies17 found serum IgG concentrations ranging from 16 to 234 mg/dL (mean, 64 mg/dL) in calves prior to ingestion colostrum; hence, sample size was calculated on the basis of detecting a minimal serum IgG concentration of 200 mg/dL, assumed baseline FPI of 1%, assumed arbitrary risk of 1.5 above baseline for FPI in calves fed by NB, power (1 − β) of 0.8, and α = 0.05. The sample size required was at least 10 calves in each group. To account for an approximately 10% dropout rate in each group from the study, 13 calves were enrolled in each group. All statistical analyses were performed with standard statistical software.q Initial data analysis to check normality via the Shapiro-Wilk test was performed before comparisons between the 2 groups. Descriptive statistics included mean ± SD and median and IQR, where appropriate, for calf birth weight, colostral IgG concentration, age of calf at feeding, precolostral serum immunoglobulin (IgG, IgM, and IgA) concentration, serum immunoglobulin (IgG, IgM, and IgA) concentration at 48 hours of age, AEA, and volume of colostrum ingested. Mean colostral immunoglobulin concentrations were compared with a t test. Serum immunoglobulin (IgG, IgM, and IgA) concentrations at 48 hours of age and the AEA between the 2 independent groups were compared by use of a Wilcoxon rank sum test18 (values of P < 0.05 were considered significant). Proportion of calves with FPI after ingestion of colostrum between the NB and OET groups were compared by means of a Fisher exact test. A follow-up conditional stepwise logistic regression predicting a calf having FPI at 48 hours as a function of birth weight, colostral IgG concentration, age of calf at feeding, method of administering colostrum, and volume of colostrum ingested was performed. Initial inclusion of the independent variables into the logistic regression model was set at P < 0.10, whereas values of P < 0.05 were considered significant for final comparisons.
Results
Data for comparison between the 2 groups were not normally distributed except the colostral immunoglobulin concentration and age of the calves at feeding colostrum. Thus, the median is reported for all parameters determined except colostral immunoglobulin concentration and age of the calves at feeding colostrum. Mean ± SD of age of calves prior to feeding colostrum was 6.1 ± 2.1 hours and 6.2 ± 1.8 hours for the NB and OET groups, respectively, and was not significantly (P = 0.842) different between the groups. Median birth weight of calves fed by the NB and OET was 38.6 kg (84.9 lb; IQR, 19.5 kg [42.9 lb]) and 44.5 kg (97.9 lb; IQR, 18.2 kg [40.0 lb]), respectively, and was not significantly (P = 0.612) different between the 2 groups. Mean ± SD colostral immunoglobulin concentration of IgG, IgM, and IgA for the NB group was 45.2 ± 8.3 g/L (95% CI, 39.3 to 51.2 g/L), 2.7 ± 0.9 g/L (95% CI, 2.1 to 3.3 g/L), and 3.0 ± 0.51 g/L (95% CI, 2.1 to 3.4 g/L), respectively. Mean ± SD colostral immunoglobulin concentration of IgG, IgM, and IgA for the OET group was 46.8 ± 6.6 g/L (95% CI, 42.0 to 51.5 g/L), 2.9 ± 1.3 g/L (95% CI, 1.9 to 3.8 g/L), and 3.4 ± 0.9 g/L (95% CI, 2.8, 4.0 g/L), respectively. There were no significant differences in colostral concentrations of IgG (P = 0.502), IgM (P = 0.715), and IgA (P = 0.119) between the NB and OET groups. Median volume of colostrum ingested by the NB-fed calves was 2.2 L. Volume of colostrum ingested by calves through the NB ranged between 1 and 4 L. Only 3 calves ingested 4 L of colostrum through the NB within 20 minutes. Median time to ingest 4 L of colostrum by the 3 calves was 10 minutes (IQR, 1 minute). Only 2 calves in each group were not classified as having FPI. Proportion of calves with FPI (11/13 in each group) between groups fed by NB and OET were not significantly (P = 1.0) different. Median precolostral serum immunoglobulin concentrations for the NB group were 104.5 mg/dL (IQR, 173 mg/dL) for IgG, 18.1 mg/dL (IQR, 33 mg/dL) for IgM, and 8.2 mg/dL (IQR, 74 mg/dL) for IgA. Median precolostral serum immunoglobulin concentrations for the OET group were 168.6 mg/dL (IQR, 122 mg/dL) for IgG, 23.6 mg/dL (IQR, 26 mg/dL) for IgM, and 16.4 mg/dL (IQR, 92 mg/dL) for IgA. There were no differences in precolostral IgG (P = 0.231), IgM (P = 0.887), and IgA (P = 0.780) between the NB and OET groups. Median immunoglobulin concentrations for the NB group at 48 hours were 658.1 mg/dL (IQR, 556.5 mg/dL) for IgG, 45.2 mg/dL (IQR, 36 mg/dL) for IgM, and 23.3 mg/dL (IQR, 25 mg/dL) for IgA. Median immunoglobulin concentrations for the OET group at 48 hours were 725.1 mg/dL (IQR, 690.5 mg/dL) for IgG, 45.0 mg/dL (IQR, 28 mg/dL) for IgM, and 19.0 mg/dL (IQR, 17 mg/dL) for IgA. There were no differences in serum IgG (P = 0.508), IgM (P = 0.611), and IgA (P = 0.584) concentrations between the NB and OET groups at 48 hours. Median AEA for the NB and OET groups was 24.2% and 19.3%, respectively, and was not different (P = 0.556) between calves fed by NB and OET. Only volume of colostrum ingested was a significant (P = 0.021) variable determining FPI at 48 hours as determined by the logistic regression. Birth weight, colostral IgG concentration, age of calf at feeding, and method of administering colostrum were not significant (P > 0.05) variables determining FPI at 48 hours of age. No second-order interactions between the independent variables were significant.
Discussion
On the basis of AEA of IgG, results of the present study indicated no significant differences in the efficiency of absorption of colostral immunoglobulins when age-matched calves were fed colostrum with similar immunoglobulin concentration through an NB or OET at 48 hours of age. Reported advantages and disadvantages of either feeding method are most likely to be of minimal practical relevance in achieving adequate passive transfer of immunity in calves. The study design allowed control of the potential pitfall of comparing absorption of colostral immunoglobulins, whereby colostrum was fed with both feeding methods in the same calf.12,13 Additionally, the study design minimized influence of breed, season, sex, and age on efficiency of IgG absorption. The volume of colostrum was the only factor determining FPI at 48 hours of age. This was expected because each similarly aged pair of calves received colostrum with similar immunoglobulin concentration, but the volume among the pairs differed. A total of 150 to 200 g of colostral IgG has been recommended for adequate transfer of colostral immunity in dairy bull calves.19 Considering the low mean colostral immunoglobulin concentration, the low median volume of colostrum ingested by the calves, and the fact that calves were only fed once, a high prevalence of FPI in calves in this study was expected. It is anticipated that producers feeding calves using an NB are more likely to feed colostrum at least once if calves ingest insufficient volume on the first feeding or provide sufficient volume by OET. It should be noted that the results of the present study are most applicable to calves fed a maximum of 4 L of colostrum. The 20 minutes allowed for each calf to nurse from a bottle was arbitrarily considered a typical time a producer would spend feeding a newborn dairy calf by an NB.
The AEAs for IgG reported in the present study were consistent with those in previous studies16 when calves were fed colostrum but were lower than AEAs in recent studies13 when calves were fed a commercial colostrum replacer. Only AEA for IgG was calculated in the present study because IgG is the predominant immunoglobulin (85% to 90% of total immunoglobulin)20 in bovine colostrum. Thus, its absorption will more likely reflect efficiency of absorption of immunoglobulins, compared with IgM or IgA. It should be noted that only bull calves were enrolled in the present study because of the perceived lower value of bull calves and the high likelihood of FPI on the basis of the design of the study. Sex of a calf may influence AEA, with heifer calves reported to have higher serum immunoglobulin concentration, compared with bull calves.21 However, other studies22 found no differences in AEA of immunoglobulins between male and female Bos indicus and Bos taurus calves. Colostral immunoglobulin concentrations comprise IgG (85% to 90%), IgM (7%), and IgA (3%).20 The results of the present study indicated a higher mean colostral IgA concentration, compared with IgM. Both IgM and IgA are largely derived from local synthesis by plasmocytes in the mammary gland23 and are more likely to differ among individual cows, possibly explaining this finding.
A perceived practical advantage of administering colostrum by NB includes reduced risk of aspiration by the calf, compared with feeding by OET. Time saving is the advantage for administering colostrum by OET, compared with feeding by NB. Newborn calves may vigorously resist OET,12 increasing the risk of pharyngeal or esophageal trauma. Results of the present study indicate that the reported advantage of enhanced immunoglobulin absorption due to closure of the esophageal groove in calves fed colostrum by NB is of little importance relative to serum immunoglobulin concentration at 48 hours of age.8,13 Likewise, the potential delay in absorption of colostral immunoglobulins due to administration of colostrum in the forestomachs when calves are fed by OET appears to be of limited importance relative to 48-hour serum immunoglobulin concentration in dairy calves.11–13 It is important to note that several factors affect passive transfer of immunity. These include colostral immunoglobulin concentration,9,19,24 volume of colostrum administered,9 age of calf at colostral feeding,25–27 stage of lactation,28–30 breed of cow,28,30 postnatal respiratory acidosis due to dystocia,31 storage of colostrum,14,32 delay of colostral collection,33 pooling of colostrum,34 pasteurization of colostrum,35–37 and use of colostrum replacers.38–40
The major limitation of the present study is that calves were only raised to 48 hours of age. Larger studies are required to compare the effect of colostral administration methods on morbidity and mortality rates in dairy calves. Results of such large studies will have more applicable recommendations in the dairy industry.
ABBREVIATIONS
| AEA | Apparent efficiency of absorption |
| CI | Confidence interval |
| FPI | Failure of passive transfer of immunity |
| IQR | Interquartile range |
| NB | Nipple bottle |
| OET | Oroesophageal tubing |
20–20 Blue calf milk replacer, Farmer's Warehouse Co Inc, Keyes, Calif.
Cryogenic vial, Corning Inc, Corning, NY.
Sheep anti-bovine IgG, IgM, IgA purified, Bethyl Laboratories, Montgomery, Tex.
Calcium carbonate, Fisher Scientific, Fair Lawn, NJ.
Fisher immunolon IV microtiter plates, Fisher Scientific, Fair Lawn, NJ.
Orbitron rotator I, Boekel Scientific, Feasterville, Pa.
Tris-buffered saline solution, Fischer Scientific, Fair Lawn, NJ.
Biotek plate washer, Biotek Instruments, Winooski, Vt.
Fish skin gelatin, Sigma-Aldrich Laboratories, St Louis, Mo.
Bovine IgG, IgM, IgA purified, Bethyl Laboratories, Montgomery, Tex.
Bovine reference serum (IgG, IgM, IgA), Bethyl Laboratories, Montgomery, Tex.
Sheep anti-bovine HRP conjugate, Bethyl Laboratories, Montgomery, Tex.
Stab-ELISA-r, Cygnus Technologies, Southport, NC.
Enzyme substrate TMB, Moss Inc, Pasadena, Md.
Sulfuric acid, Sigma-Aldrich Laboratories, St Louis, Mo.
Biotek Powerwave HT, Biotek Instruments, Winooski, Vt.
SAS, version 9.2, SAS Institute Inc, Cary, NC.
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