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Serum Immunoglobulin Concentrations and Health of Dairy Calves in Two Management Systems from Birth to 12 Weeks of Age
Serum Immunoglobulin Concentrations and Health of Dairy Calves in Two Management Systems from Birth to 12 Weeks of Age P
ABSTRACT
Fifteen dairy calves were kept with their dams for 5 d after birth and thereafter were fed milk from a nipple pail in individual pens (nursed calves). Another 15 calves were separated from their dams immediately after birth, placed in individual pens, and fed from an open pail (weaned calves). These calves received colostrum for the first three feedings. Serum Ig concentrations and the health of the calves were monitored from birth to 12 wk of age. The serum Ig concentrations developed identically for calves in both groups. A 30-min delay in intake of first colostrum decreased total Ig concentrations in serum by about 2 mg/ml. Occurrence of diarrhea was three times greater for the weaned calves than for the nursed calves. Serum Ig concentrations did not explain the differences in the diarrhea Occurrence between the groups. In conclusion, the newborn calves in both management systems acquired equal passive immunity, although the time of first colostrum consumption played an important role. Open pail feeding may increase the incidence of prolonged diarrhea compared with that from nipple feeding. (Key words: calf, immunoglobulins, management, health)
Abbreviation key: T24 = total serum Ig concentration at 24 h of age. INTRODUCTION
Bovine calves are born practically agammaglobulinemic; therefore, the acquisition of
Received June 6, 1994. Accepted June 23, 1995 1995 J Dairy Sci 78:2737-2744
h RAJALA and HELl CASTREN College of Veterinary Medicine Department of Animal Hygiene PO Box 6 00581 Helsinki, Finland
passive immunity by colostrum ingestion is crucial in protecting the newborn from neonatal infections. Calves that fail to attain adequate passive immunity are more susceptible to diseases and mortality than are those with high concentrations of Ig in serum (14, 25). Dairy calves in Finland are usually raised in individual pens and fed milk or milk replacer from an open pail from birth to weaning. However, research shows that suckling and the presence of the dam can have a positive effect on the extent of passive immunity in a newborn calf (11, 29, 33). Feeding methods can significantly influence the incidence of diarrhea in neonatal calves (37). Loose housing systems are becoming more common in Finland, and dairy producers tend to leave the newborn calf unattended with its ,dam in the calving pen. The amount of Ig absorbed from the intestine of the calf depends on the amount of ingested colostrum, the concentration of Ig in colostrum, and the absorption efficiency of the gut. The age of the calf at first feeding and the method of colostrum feeding affect the efficiency of absorption and, therefore, the extent of passive immunity (2, 24, 29, 30, 31, 32). Considering the behavioral needs of calves, the optimal method of colostrum intake is natural suckling (13). However, among the calves left with their dams after birth, delayed suckling, ingestion of inadequate quantities of colostrum, or both often result in a failure of passive transfer (2, 4). The disease resistance acquired from colostral Ig is only temporary, and the newborn must become immunocompetent before passive maternal immunity wanes. After absorption of Ig in the calf intestine ceases, the concentration of maternal Ig in the calf serum starts to decline. The rate of decline differs between Ig classes (34). The time period for the Ig to decline to an unprotective concentration depends on the initial concentration and
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on the beginning of endogenous production of Ig. Behavioral interactions between the dam and the newborn calf immediately after parturition (6, 8, 20, 21) and the association between Ig concentration in serum and calf morbidity (14, 25) have been studied intensively. However, the Ig concentrations in calf serum often have not been monitored systematically after the first days of life, especially for calves raised in different management systems. We compared the effects of two early management systems on the serum Ig concentrations and health of neonatal dairy calves. In one system, weaned calves were raised individually and fed from an open pail. In the other system, nursed calves were kept with their dams for 5 d and then nipple fed. The Ig concentrations in calf serum were monitored from birth to 12 wk of age. MATERIALS AND METHODS
Cows and Calves
Thirty Finnish-Ayrshire dairy cows and their calves from the experimental farm of Helsinki University were studied. The cows had previously been tethered in a stall, but, approximately 1 d before the estimated calving, each cow was moved into an individual calving pen (3.4 x 3.0 m) with straw bedding. The newborn calves were assigned to one of two experimental groups with 9 bull calves and 6 heifer calves in each group. The first experimental group consisted of 15 calves from 11 heifers, 3 second lactation cows, and 1 third lactation cow. Calves stayed with their dams in the calving pen for the first 5 d and were referred to as the nursed calves. During this time, calves could suckle freely; the cows were also milked twice daily. These pairs were continuously observed for 6 h after birth. If the calves did not suckle within this period, they were assisted in doing so after the observation period ended. There was no estimate of the amount of colostrum ingested by the nursed calves. After the first 5 d, each calf was separated from its dam and placed in an individual pen (1.0 x 1.18 m) with straw bedding in a separate room with other calves on the farm. Calves were fed 3 L of whole milk twice daily from a nipple pail. Journal of Dairy Science Vol. 78, No. 12, 1995
CASTRBN The other group consisted of 15 calves from 9 heifers, 5 second lactation cows, and 1 fourth lactation cow. Calves were separated from their dams at 15 to 30 min after birth and were referred to as the weaned calves. One heifer had a difficult calving and needed assistance. The cows were allowed to lick the calf, but the calves could not suckle the cow. These calves were each placed in pens similar to those used by the nursed calves. The weaned calves were first offered 2 L of colostrum from the dam at the age of 4 h from a nipple pail. The next two feedings each consisted of 3 L of colostrum. Thereafter, calves were fed twice daily from an open pail; each feeding consisted of 3 L of whole milk. Depending on the time of birth, some calves were fed twice and some three times during the 1st d of life. All calves were fed milk twice daily at approximately 0800 and 1500 h until 12 wk of age. Calves had free access to hay and concentrates after the first 5 d of life. Water was available for ad libitum access. At 8 to 10 wk of age, all calves were moved to stalls in the same room with the cows. Methods
Within 30 min after birth, a 10-ml blood sample was collected from the jugular vein of each calf. Subsequent samples were taken at the age of 24 & 6 h, 48 k 6 h, 4 d. 7 d, and then at 2, 4, 6, 8, 10, and 12 wk. The serum was separated and frozen at -20°C for later analysis. Colostrum samples were collected from the cows immediately after calving and frozen at -20°C for later determination of the Ig content. Of the 30 cows, only 28 colostrum samples were analyzed because 2 cows had mastitis at calving, and their weaned calves received colostrum from another cow in the experiment that had calved just before these cows. The Ig concentrations in the serum and colostrum were determined by radial immunodiffusion using commercial kits for IgG1, IgM, and IgA according to the instructions of the manufacturer (Binding Site Ltd., Birmingham, England). The Ig concentrations (IgG1, IgM. and IgA) in colostrum were measured from whole colostrum (12) using dilutions required by the commercial kit. The nursed calves and their behavioral interactions with their dams were observed
CALF MANAGEMENT, IMMUNOGLOBULINS, AND HEALTH
directly for 6 h after birth. Observations began immediately after the first blood sampling. The moment at which the calf suckled for the first time was registered as the age of the calf at first colostrum intake. The calf was considered to have suckled when it had a teat in its mouth and was seen to make the appropriate swallowing motion. All clinical signs of diseases were registered daily by the caretakers of the calves. Calves were considered to have diarrhea when the consistency of their feces was clearly soft or watery. Milk was withheld from the diarrhetic calves for 1 or 2 d. During this time, the calves received electrolyte solutions (Nutrisal Plus*; Orion-Fannos, Turku, Finland). Coughing, nasal discharge, and labored breathing were reported as symptoms of respiratory disease. Calves with severe clinical signs (e.g., fever and dullness) were treated by a veterinarian. Diarrhea was usually mild and did not require veterinary treatment. Therefore, fecal samples were not examined systematically for detemination of infectious agents. Data Analysis
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an IgGl concentration of 8 to 16 mg/ml at the age of 48 h (1). The relative risk of prolonged diarrhea for the calves in the different feeding systems was calculated (10). RESULTS Age at First Colostrum Intake and Serum lg Concentration at 24 h
All weaned calves received their first colostrum at 240 min. The 9 nursed calves that successfully suckled without help within 6 h after birth first suckled at a mean age of 136 min (SE = 22 min; range, 55 to 225 rnin). Of the 6 nursed calves that failed to suckle within the first 6 h, 3 were from heifers, and 3 were from older cows, One calf was unsuccessful because of the poor udder conformation of a dam at third calving, and 1 calf was weak after prolonged calving of a heifer, probably because of hypoxia. In other cases, the reason for delayed suckling was not evident. For the nursed calves, the age at first colostrum intake was negatively correlated with T24 (P e .Ol). Individual variation in serum Ig concentrations at 24 h of age was great, especially among nursed calves. Multiple linear regression was performed using T24 as a dependent variable and age at first colostrum intake, total colostrum Ig concentration, birth weight, and calf group as predictor variables. The calf group (weaned vs. nursed) did not have a significant effect on T24. The model presented in Table 1 explains 58.6% of the variation in T24 among the 30 calves (F value = 12.2; P c .001). The model indicated that
The serum IgGl, IgM, and IgA concentrations and the total Ig concentrations at each sampling time for both groups were compared using the general linear models technique of SAS (27) (repeated measures analysis). The calf group (nursed vs. weaned) was a betweensubjects factor, and time (age at each sampling time) was a repeated measures factor. A multiple linear regression model was used to explain the variation in the total Ig concentration in the serum at the age of 24 h n24) (27). The Pearson correlation coefficients were calculated between colostrum Ig concentrations and serum Ig concentrations at different ages TABLE 1. Multiple linear regression model' of Ig concentrations in serum (I&], IgM, and IgA) for the 30 calves at for both groups. The T24 of the calves that were healthy 24 h of age. throughout the study were compared with that Partial regression of the calves that had clinical signs of diseases Predictor P variable coefficient SE using a two-sample f test (27). To describe the differences in the serum Ig Constant 7.08 13.24 597 .01 .o001 -.07 concentrations during the first 12 wk of life, Age.z min Ig in colost1urn.3 m g / d 17 .06 ,007 the 6 calves with the lowest Ig concentrations Birth 66 .34 .06 weight, kg and the 6 calves with the highest Ig concentra'R2 = ,586. tions were compared. The calves with the 2Age of calf at the intake of first colostrum. lowest Ig concentrations were those considered to have partial failure of passive transfer with 3Concenuation of IgG1. IgM, and IgA in colostrum. ~~~
Journal of Dairy Science Vol. 78. No. 12, 1995
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every 30-min delay in the intake of first colostrum decreased Ig concentration in serum by about 2 mg/ml. Using only the data from the nursed calves, the coefficient of the age of a calf in minutes at the intake of first colostrum remained the same and was statistically significant when the regression was performed. For the nursed calves model, the same predictor variables explained 65.2% of the variation in T24, indicating an even greater effect of the age at first colostrum intake in explaining the variation in T24. The colostrum Ig concentration did not have a significant effect on T24 in that model. The mean total Ig concentration (IgG1, IgM, and IgA) of the 28 first milking colostrum samples was 76.2 mglml (SE = 3.7 mglml; range, 25.9 to 109.9 mglml). For the nursed calves, neither the total colostrum Ig concentration nor the colostral IgG1, IgM, and IgA concentrations correlated significantly with T24. However, for the weaned calves, the correlations were significant (total Ig: P c .01, IgG1: P < .05, IgM: P c .01, and IgA: P < .001). Serum ig Concentrations at Different Calf Ages
According to the repeated measures analysis, the serum Ig concentrations in any Ig class showed no significant differences at any age between the two calf groups. No interactions existed between the management system and the age at each sampling time. The age at each sampling time significantly affected the serum Ig concentrations (IgG1, IgM, and IgA; P c .OOOl). The mean serum concentrations of IgGl, IgM, and IgA and standard errors at different ages in the 30 calves are presented in Figure 1. Because of lack of significant differences between groups, the data for calves were pooled. The minimum value of the total Ig concentration in the serum (18.6 mglml) of the 30 calves appeared at 10 wk of age (Figure 1). Variation was large within the groups, especially at 24 and 48 h of age. Concentrations of IgM and IgA started to increase from 4 wk of age, but concentration of IgGl declined until the age of 12 wk. The total serum Ig concentrations of the 6 calves with the highest Ig concentrations and Journal of Dairy Science Vol. 78, No. 12, 1995
the 6 calves with the lowest Ig concentrations are presented in Figure 2. The Ig concentration of the calves with the lowest Ig began to rise at about 2 wk of age, but the Ig concentration of the calves with the highest Ig decreased until 12 wk of age. However, the serum Ig concentration of the calves with the lowest Ig was still only about half of the value of the calves with the highest Ig at 12 wk of age. According to the definition of Gay (14) for failure of passive transfer of immunity (i.e., IgGl concentration in serum
The number of calves that were healthy, unhealthy (showed symptoms of diseases), or died during the study are presented in Table 2. Records for 1 weaned calf were excluded from
TABLE 2. Health and mortality of calves that were kept with dam for 5 d and then nipple fed (nursed calves) or immediately weaned and fed from open pail (weaned calves). Nursed calves (n = 15) Healthy Unhealthy Diarrhea Symptoms of respiratory disease Mortality'
Weaned calves (n = 14)
7
3
7
10
1 1
1 1
'Calves with symptoms of respiratory disease died.
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CALF MANAGEMENT, IMMUNOGLOBULINS. AND HEALTH
the disease data because the calf was thought to be lactose intolerant and was diarrhetic whenever milk was offered. The most common disease during the study was diarrhea, which was usually mild and lasted only 2 to 3 d. Most diarrhea occurred when the calves were 4 to 8 wk old. The calves that died during the study were those with symptoms of respiratory disease. The mean T24 of the healthy calves was 28.7 mg/ml (SD = 13.8 mg/ml), and the mean T24 of the calves with symptoms of diseases was 24.9 mg/ml (SD = 10.5 mg/ml). These T24 did not differ (P > .05). However, the weaned
calves had almost three times as many days of diarrhea (1 11 d) as the nursed calves had during the study (40 d). The risk of prolonged diarrhea was almost three times as high for weaned calves as for nursed calves (relative risk = 2.88; 95% confidence limits = 2.02 < relative risk < 4.09). DISCUSSION
Passive immunity developed in the same way for all calves in both management systems. All calves absorbed some Ig. However, the sooner the nursed calves received colostrum, the higher was the T24. This result
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agrees with previous reports of the effect of early intake of first colostrum on the efficiency of Ig absorption (9, 19, 22, 30). Our results indicated that every 30-min delay in the intake of first colostrum decreased Ig concentration in serum by about 2 mg/ml. Of 30 calves, 6 showed a partial failure of passive transfer at the age of 48 h (1). Three of these failed to suckle during the first 6 h. Other reports (6, 7, 17, 23, 28, 29, 35) also show that a high percentage of calves fail to suckle within 4 to 8 h after birth, mostly because of poor udder conformation but also because of abnormal maternal behavior and poor calf vigor, especially after difficult calvings. Our results also agree with previous reports regarding the failure of passive transfer of immunity. Studies reported a failure of passive transfer of immunity for 61% (2) and 42% (4) of calves nursed by their dams because the calves failed to suckle or absorb colostral Ig when left with their dams for 1 d. The risk of failure of passive transfer of immunity seems to be greatest among calves left with their dams but not assisted to suckle early enough. An inadequate quantity of ingested colostrum might partially explain the low serum Ig concentrations among the nursed calves. ConJournal of Dairy Science Vol. 78, No. 12, 1995
versely, 3 calves that did not suckle within 6 h had relatively high Ig concentrations in their serum. As the amount of suckled colostrum was not determined in this study, we cannot explain these differences. High Ig concentrations in colostrum alone do not guarantee a high concentration of serum Ig. Presumably, individual differences exist in the efficiency of Ig absorption. Colostrum Ig concentrations did not correlate significantly with serum Ig concentrations at any age for the nursed calves. However, for the weaned calves, the correlation was significant, especially at 24 h of age, perhaps because all weaned calves received an equivalent amount of colostrum, but the amount of colostrum suckled by nursed calves was unknown. For all calves, both IgM and IgA concentrations started to increase at 4 wk of age, but IgGl declined up to 12 wk of age. This result agrees with previous results (18). In another study (15), the lowest serum IgGl concentration occurred at 16 d of age (15). This discrepancy with our results can be explained by the fact that the reported IgGl concentrations in that study were much lower than those of our study, and maternal antibodies acquired through colostrum influence the immunologi-
CALF MANAGEMENT, IMMUNOGLOBULINS, AND HEALTH
cal response of a newborn calf. For calves deprived of colostrum, endogenous Ig production O C C U K ~ much earlier than for calves that received a high level of passive immunity through colostrum (16). The onset of an increase in IgM and IgA concentrations at 4 wk of age probably indicates the start of their endogenous production. The total Ig concentration for the 30 calves continued to decline up to 10 wk of age, in agreement with the previous suggestion that endogenous production of Ig does not significantly begin to contribute to the total Ig in plasma during the first weeks of life (15) because the endogenous production is still minor to the catabolism of maternal antibodies. The most common disease among the calves was diarrhea. The number of days of diarrhea and the risk of prolonged diarrhea were three times as great for the weaned calves as for the nursed calves. However, the number of affected calves and the T24 did not differ between calf groups. Our observations agree with a previous study (23) of diarrhea morbidity of calves, which reported that morbidity was twofold lower for calves kept with their dams for 10 d after birth than for calves kept alone (23). In our study, diarrhea was most common at 4 to 8 wk of age, a time when IgM and IgA concentrations were lowest in calf serum. Feeding systems may affect the incidence of diarrhea. Zaremba et al. (37) reported that calves fed milk from an open pail four times daily had significantly higher incidence of diarrhea than calves fed for ad libitum intake from a nipple pail. Rapid ingestion of large amounts of milk or milk substitutes from an open pail can result in incomplete closure of the esophageal groove, formation of defective curd in abomasum, high pH in abomasum for several hours after feeding, excessively fast abomasal emptying, and overloading of the intestine, leading to bacterial overproliferation and diarrhea (3, 5, 26, 36). In our study, the amount of milk (3 L) consumed at one time may have been too large and may have caused the diarrhea. The presence of enteropathogens in feces was not determined, however, and the final reason for diarrhea remains unclear. CONCLUSIONS
In both management systems, the passive transfer of immunity of the newborn calves
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developed in the same way; however, individual differences in serum Ig concentrations were great. Delayed intake of first colostrum after birth decreased serum Ig concentration by about 2 mg/ml for each 30-min delay. High colostral Ig concentrations did not ensure high serum Ig concentrations among nursed calves. When calves are left with their dams after birth, they should be assisted so that they suckle dams as soon as possible to ensure the acquisition of high serum Ig concentrations. Weaned calves had about three times as many days of diarrhea as nursed calves, despite equal serum Ig concentrations. The reason for this difference remains unclear even though the diarrhea may have been caused by the feeding method. Therefore, nipple feeding is recommended. ACKNOWLEDGMENTS
This study was supported by The Finnish Society for Animal Welfare and The Academy of Finland. The authors thank the staff at the experimental farm of Helsinki University and also appreciate the help of Sole Rajala, Anou Londesborough, and Kati Leinonen. REFERENCES 1 Banks, K. L., and T. C. McGuire. 1989. Neonatal
immunology. Page 193 in Veterinary Clinical Immunology. R.E.W. Halliwell and N. T. Gorman, ed. W. B. Saunders Co., Philadelphia. PA. 2 Besser, T. E.. C. C. Gay. and L. Pritchett. 1991. Comparison of three methods of feeding colostrum to dairy calves. J. Am. Vet. Med. Assoc. 198:419. 3 Blowey, R. W. 1992. Digestive disorders of calves. Page 194 in Bovine Medicine. Diseases and Husbandry of Cattle. A. H. Andres, R. W. Blowey, H. Boyd, and R. G. Eddy. ed. Blackwell Sci. Pub]., Oxford. England. 4 Brignole, T. J.. and G. H. Stoa. 1980. Effect of suckling followed by bottle feeding colostrum on immunoglobulin absorption and calf survival. J . Dairy Sci. 63:451. 5Dirr, L., and G. Dirksen. 1989. Dysfunktion der Schlundrinne (“Pansenmnken”) als Komplikation der Neugeborenendimho beim Kalb. Tieraerztl. Prax. 17: 353. 6 Edwards, S. A. 1982. Factors affecting the time to first suckling in dairy calves. Anim. Prod. 34:339. 7 Edwards, S . A., and D. M. Broom. 1979. The period between birth and first suckling in dairy calves. Res. Vet. Sci. 26:255. 8 Edwards, S. A., and D.M. Broom. 1982. Behavioral interactions of dairy cows with their newborn calves and effects of parity. Anim. Behav. 30525. Journal of Dairy Science Vol. 78. No. 12, 1995
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9 Edwards, S. A.. D. M. Broom, and S. C. Collis. 1982. Factors affecting levels of passive immunity in dairy calves. Br. Vet. J. 138:233. 10Epi-info. Version 5. User's Guide. 1990. Cu. Dis. Control and World Health Organ. USD Inc., Stone Mountain, GA. 1 I Fallon, R. J. 1979. The effect of different methods of feeding colostrum on calf blood serum immunoglobulin levels. Page 507 in Calving Problems and Early Viability of the Calf. B. Hoffman, 1. L. Mason, and J. Schmidt, ed. Curr. Topics Vet. Med. Anim. Sci. Vol. 4. Martinus Niijhof Publ., The Hague, The Netherlands. 12 Fleenor. W. A., and H. Stott. 1983. Single radial immunodiffusion analysis for quantitation of colostral immunoglobulin concentration. J. Dairy Sci. 64:740. 13 Frazer. A. F., and D. M. Broom. 1990. Neonatal behaviour. Page 227 in Farm Animal Behaviour and Welfare. 3rd ed. Bailliere Tindall, London, England. 14 Gay, C. C. 1983. Failure of passive transfer of colostral immunoglobulins and neonatal disease in calves: a review. Page 346 in Proc. 4th Int. Symp. Neonatal Diarrhea. Vet. Infect. Dis. Organ., Saskatoon, SK, Canada. 15 Husband, A. J., M. R. Brandon, and A. K. Lascelles. 1972. Absorption and endogenous production of immunoglobulins in calves. Aust. J. Exp. Biol. Med. Sci. 50:491. 16 Husband, A. J., and A. K. Lascelles. 1975. Antibody responses to neonatal immunization in calves. Res Vet. Sci. 18:201. 17 Illmann, G.. and M. Spinka. 1993. Maternal behaviour of dairy heifers and sucking of their newborn calves in group housing. Appl. Anim. Behav. Sci. 36:91. 18 Kim, J. W., and F. W. Schmidt. 1983. Zur Frage der Absorption von kolostralen lmmunoglobulinen durch das Kalb. Dtsch. Tieraerztl. Wochenschr. 90:283. 19 Kruse, V. 1970. Absorption of immunoglobulin from colostrum in newborn calves. Anim. Prod. 12:627. 20 le Neindre. P. 1982. Cow-calf relationships: the effect of management systems. Page 24 in Welfare and Husbandry of Calves. J. P. Signoret, ed. Martinus Nijhoff Publ., The Hague, The Netherlands. 21 Lidfors, L., and P. Jensen. 1988. Behaviour of freeranging beef cows and calves. Appl. Anim. Behav. Sci. 20237. 22 Matte, J. J., C. L. Girard, J. R. Seoane, and G. J. Brisson. 1982. Absorption of colostral immunoglobulin G in the newborn dairy calf. J. Dairy Sci. 65:1765. 23 Metz, J. 1984. Behaviour and state of health of cows and calves kept together or separately in the post partum period. Page 358 in Proc. Int. Congr. Appl.
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CASTRBN Uhol. Farm Anim. J. Unshelm, G. van Putten, and K. Zeeb, ed. Kuratorium Technik Bauwesen Landwirtschaft, Kiel, Germany. 24 Petrie, L. 1984. Maximising the absorption of colostral immunoglobulins in the newborn dairy calf. Vet. Rec. 114:157. 25 Roy, J.H.B. 1990. The Calf. Volume 1. Management of Health. 5th ed. Butterworths, London, England. 26 Ruckebusch. Y. 1988. Motility of the gastro-intestinal tract. Page 64 in The Ruminant Animal: Digestive Physiology and Nutrition. D. C. Church, ed. Reston Book Publ., Englewood Cliffs. NJ. 27 SAS@ User's Guide: Statistics, Version 6 Edition. 1988. SAS Inst., Inc., Cary, NC. 28 Selman, I. E., A. D. McEwan, and E. W. Fisher. 1970. Studies on natural suckling in cattle during the first eight hours post partum 1. Behavioural studies (calves). Anim. Behav. 18:284. 29 Selman, I. E., A. D. McEwan, and E. W. Fisher. 1971. Studies on dairy calves allowed to suckle their dams at fixed times post partum. Res. Vet. Sci. 12:l. 30Stott. G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. I. Period of absorption. J. Dairy Sci. 62: 1632. 31 Stott, G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. 11. The rate of absorption. J. Dairy Sci. 62: 1677. 32 Stott, G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. 111. Amount of absorption. J. Dairy Sci. 62: 1902. 33 Ston, G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. IV. Effect of suckling. J. Dairy Sci. 62: 1908. 34Tizard. I. 1992. Immunity in the fetus and newborn. Page 248 in Veterinary Immunology, An Introduction. 4th ed. W. B. Saunders Co., Philadelphia, PA. 35 Ventorp, M., and P. Michanek. 1992. The importance of udder and teat conformation for teat seeking by the newborn calf. J. Dairy Sci. 75:262. 36Zaremba. W. 1983. Futterungstechnik und Ihre Bedeutung fur den gesundheitszustand neugeborener Kdber unter Besondere Berucksichtung der Diarrhoea. Prakt. Tieraerztl. 11:977. 37Zaremba. W., E. Grunert, and A. Binder. 1982. Der Einfluss verschiedener Trhkeverfahren auf die Gesundheit neugeborener Kiilber. Tieraerztl. Umsch. 71469.
ABSTRACT
Fifteen dairy calves were kept with their dams for 5 d after birth and thereafter were fed milk from a nipple pail in individual pens (nursed calves). Another 15 calves were separated from their dams immediately after birth, placed in individual pens, and fed from an open pail (weaned calves). These calves received colostrum for the first three feedings. Serum Ig concentrations and the health of the calves were monitored from birth to 12 wk of age. The serum Ig concentrations developed identically for calves in both groups. A 30-min delay in intake of first colostrum decreased total Ig concentrations in serum by about 2 mg/ml. Occurrence of diarrhea was three times greater for the weaned calves than for the nursed calves. Serum Ig concentrations did not explain the differences in the diarrhea Occurrence between the groups. In conclusion, the newborn calves in both management systems acquired equal passive immunity, although the time of first colostrum consumption played an important role. Open pail feeding may increase the incidence of prolonged diarrhea compared with that from nipple feeding. (Key words: calf, immunoglobulins, management, health)
Abbreviation key: T24 = total serum Ig concentration at 24 h of age. INTRODUCTION
Bovine calves are born practically agammaglobulinemic; therefore, the acquisition of
Received June 6, 1994. Accepted June 23, 1995 1995 J Dairy Sci 78:2737-2744
h RAJALA and HELl CASTREN College of Veterinary Medicine Department of Animal Hygiene PO Box 6 00581 Helsinki, Finland
passive immunity by colostrum ingestion is crucial in protecting the newborn from neonatal infections. Calves that fail to attain adequate passive immunity are more susceptible to diseases and mortality than are those with high concentrations of Ig in serum (14, 25). Dairy calves in Finland are usually raised in individual pens and fed milk or milk replacer from an open pail from birth to weaning. However, research shows that suckling and the presence of the dam can have a positive effect on the extent of passive immunity in a newborn calf (11, 29, 33). Feeding methods can significantly influence the incidence of diarrhea in neonatal calves (37). Loose housing systems are becoming more common in Finland, and dairy producers tend to leave the newborn calf unattended with its ,dam in the calving pen. The amount of Ig absorbed from the intestine of the calf depends on the amount of ingested colostrum, the concentration of Ig in colostrum, and the absorption efficiency of the gut. The age of the calf at first feeding and the method of colostrum feeding affect the efficiency of absorption and, therefore, the extent of passive immunity (2, 24, 29, 30, 31, 32). Considering the behavioral needs of calves, the optimal method of colostrum intake is natural suckling (13). However, among the calves left with their dams after birth, delayed suckling, ingestion of inadequate quantities of colostrum, or both often result in a failure of passive transfer (2, 4). The disease resistance acquired from colostral Ig is only temporary, and the newborn must become immunocompetent before passive maternal immunity wanes. After absorption of Ig in the calf intestine ceases, the concentration of maternal Ig in the calf serum starts to decline. The rate of decline differs between Ig classes (34). The time period for the Ig to decline to an unprotective concentration depends on the initial concentration and
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on the beginning of endogenous production of Ig. Behavioral interactions between the dam and the newborn calf immediately after parturition (6, 8, 20, 21) and the association between Ig concentration in serum and calf morbidity (14, 25) have been studied intensively. However, the Ig concentrations in calf serum often have not been monitored systematically after the first days of life, especially for calves raised in different management systems. We compared the effects of two early management systems on the serum Ig concentrations and health of neonatal dairy calves. In one system, weaned calves were raised individually and fed from an open pail. In the other system, nursed calves were kept with their dams for 5 d and then nipple fed. The Ig concentrations in calf serum were monitored from birth to 12 wk of age. MATERIALS AND METHODS
Cows and Calves
Thirty Finnish-Ayrshire dairy cows and their calves from the experimental farm of Helsinki University were studied. The cows had previously been tethered in a stall, but, approximately 1 d before the estimated calving, each cow was moved into an individual calving pen (3.4 x 3.0 m) with straw bedding. The newborn calves were assigned to one of two experimental groups with 9 bull calves and 6 heifer calves in each group. The first experimental group consisted of 15 calves from 11 heifers, 3 second lactation cows, and 1 third lactation cow. Calves stayed with their dams in the calving pen for the first 5 d and were referred to as the nursed calves. During this time, calves could suckle freely; the cows were also milked twice daily. These pairs were continuously observed for 6 h after birth. If the calves did not suckle within this period, they were assisted in doing so after the observation period ended. There was no estimate of the amount of colostrum ingested by the nursed calves. After the first 5 d, each calf was separated from its dam and placed in an individual pen (1.0 x 1.18 m) with straw bedding in a separate room with other calves on the farm. Calves were fed 3 L of whole milk twice daily from a nipple pail. Journal of Dairy Science Vol. 78, No. 12, 1995
CASTRBN The other group consisted of 15 calves from 9 heifers, 5 second lactation cows, and 1 fourth lactation cow. Calves were separated from their dams at 15 to 30 min after birth and were referred to as the weaned calves. One heifer had a difficult calving and needed assistance. The cows were allowed to lick the calf, but the calves could not suckle the cow. These calves were each placed in pens similar to those used by the nursed calves. The weaned calves were first offered 2 L of colostrum from the dam at the age of 4 h from a nipple pail. The next two feedings each consisted of 3 L of colostrum. Thereafter, calves were fed twice daily from an open pail; each feeding consisted of 3 L of whole milk. Depending on the time of birth, some calves were fed twice and some three times during the 1st d of life. All calves were fed milk twice daily at approximately 0800 and 1500 h until 12 wk of age. Calves had free access to hay and concentrates after the first 5 d of life. Water was available for ad libitum access. At 8 to 10 wk of age, all calves were moved to stalls in the same room with the cows. Methods
Within 30 min after birth, a 10-ml blood sample was collected from the jugular vein of each calf. Subsequent samples were taken at the age of 24 & 6 h, 48 k 6 h, 4 d. 7 d, and then at 2, 4, 6, 8, 10, and 12 wk. The serum was separated and frozen at -20°C for later analysis. Colostrum samples were collected from the cows immediately after calving and frozen at -20°C for later determination of the Ig content. Of the 30 cows, only 28 colostrum samples were analyzed because 2 cows had mastitis at calving, and their weaned calves received colostrum from another cow in the experiment that had calved just before these cows. The Ig concentrations in the serum and colostrum were determined by radial immunodiffusion using commercial kits for IgG1, IgM, and IgA according to the instructions of the manufacturer (Binding Site Ltd., Birmingham, England). The Ig concentrations (IgG1, IgM. and IgA) in colostrum were measured from whole colostrum (12) using dilutions required by the commercial kit. The nursed calves and their behavioral interactions with their dams were observed
CALF MANAGEMENT, IMMUNOGLOBULINS, AND HEALTH
directly for 6 h after birth. Observations began immediately after the first blood sampling. The moment at which the calf suckled for the first time was registered as the age of the calf at first colostrum intake. The calf was considered to have suckled when it had a teat in its mouth and was seen to make the appropriate swallowing motion. All clinical signs of diseases were registered daily by the caretakers of the calves. Calves were considered to have diarrhea when the consistency of their feces was clearly soft or watery. Milk was withheld from the diarrhetic calves for 1 or 2 d. During this time, the calves received electrolyte solutions (Nutrisal Plus*; Orion-Fannos, Turku, Finland). Coughing, nasal discharge, and labored breathing were reported as symptoms of respiratory disease. Calves with severe clinical signs (e.g., fever and dullness) were treated by a veterinarian. Diarrhea was usually mild and did not require veterinary treatment. Therefore, fecal samples were not examined systematically for detemination of infectious agents. Data Analysis
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an IgGl concentration of 8 to 16 mg/ml at the age of 48 h (1). The relative risk of prolonged diarrhea for the calves in the different feeding systems was calculated (10). RESULTS Age at First Colostrum Intake and Serum lg Concentration at 24 h
All weaned calves received their first colostrum at 240 min. The 9 nursed calves that successfully suckled without help within 6 h after birth first suckled at a mean age of 136 min (SE = 22 min; range, 55 to 225 rnin). Of the 6 nursed calves that failed to suckle within the first 6 h, 3 were from heifers, and 3 were from older cows, One calf was unsuccessful because of the poor udder conformation of a dam at third calving, and 1 calf was weak after prolonged calving of a heifer, probably because of hypoxia. In other cases, the reason for delayed suckling was not evident. For the nursed calves, the age at first colostrum intake was negatively correlated with T24 (P e .Ol). Individual variation in serum Ig concentrations at 24 h of age was great, especially among nursed calves. Multiple linear regression was performed using T24 as a dependent variable and age at first colostrum intake, total colostrum Ig concentration, birth weight, and calf group as predictor variables. The calf group (weaned vs. nursed) did not have a significant effect on T24. The model presented in Table 1 explains 58.6% of the variation in T24 among the 30 calves (F value = 12.2; P c .001). The model indicated that
The serum IgGl, IgM, and IgA concentrations and the total Ig concentrations at each sampling time for both groups were compared using the general linear models technique of SAS (27) (repeated measures analysis). The calf group (nursed vs. weaned) was a betweensubjects factor, and time (age at each sampling time) was a repeated measures factor. A multiple linear regression model was used to explain the variation in the total Ig concentration in the serum at the age of 24 h n24) (27). The Pearson correlation coefficients were calculated between colostrum Ig concentrations and serum Ig concentrations at different ages TABLE 1. Multiple linear regression model' of Ig concentrations in serum (I&], IgM, and IgA) for the 30 calves at for both groups. The T24 of the calves that were healthy 24 h of age. throughout the study were compared with that Partial regression of the calves that had clinical signs of diseases Predictor P variable coefficient SE using a two-sample f test (27). To describe the differences in the serum Ig Constant 7.08 13.24 597 .01 .o001 -.07 concentrations during the first 12 wk of life, Age.z min Ig in colost1urn.3 m g / d 17 .06 ,007 the 6 calves with the lowest Ig concentrations Birth 66 .34 .06 weight, kg and the 6 calves with the highest Ig concentra'R2 = ,586. tions were compared. The calves with the 2Age of calf at the intake of first colostrum. lowest Ig concentrations were those considered to have partial failure of passive transfer with 3Concenuation of IgG1. IgM, and IgA in colostrum. ~~~
Journal of Dairy Science Vol. 78. No. 12, 1995
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every 30-min delay in the intake of first colostrum decreased Ig concentration in serum by about 2 mg/ml. Using only the data from the nursed calves, the coefficient of the age of a calf in minutes at the intake of first colostrum remained the same and was statistically significant when the regression was performed. For the nursed calves model, the same predictor variables explained 65.2% of the variation in T24, indicating an even greater effect of the age at first colostrum intake in explaining the variation in T24. The colostrum Ig concentration did not have a significant effect on T24 in that model. The mean total Ig concentration (IgG1, IgM, and IgA) of the 28 first milking colostrum samples was 76.2 mglml (SE = 3.7 mglml; range, 25.9 to 109.9 mglml). For the nursed calves, neither the total colostrum Ig concentration nor the colostral IgG1, IgM, and IgA concentrations correlated significantly with T24. However, for the weaned calves, the correlations were significant (total Ig: P c .01, IgG1: P < .05, IgM: P c .01, and IgA: P < .001). Serum ig Concentrations at Different Calf Ages
According to the repeated measures analysis, the serum Ig concentrations in any Ig class showed no significant differences at any age between the two calf groups. No interactions existed between the management system and the age at each sampling time. The age at each sampling time significantly affected the serum Ig concentrations (IgG1, IgM, and IgA; P c .OOOl). The mean serum concentrations of IgGl, IgM, and IgA and standard errors at different ages in the 30 calves are presented in Figure 1. Because of lack of significant differences between groups, the data for calves were pooled. The minimum value of the total Ig concentration in the serum (18.6 mglml) of the 30 calves appeared at 10 wk of age (Figure 1). Variation was large within the groups, especially at 24 and 48 h of age. Concentrations of IgM and IgA started to increase from 4 wk of age, but concentration of IgGl declined until the age of 12 wk. The total serum Ig concentrations of the 6 calves with the highest Ig concentrations and Journal of Dairy Science Vol. 78, No. 12, 1995
the 6 calves with the lowest Ig concentrations are presented in Figure 2. The Ig concentration of the calves with the lowest Ig began to rise at about 2 wk of age, but the Ig concentration of the calves with the highest Ig decreased until 12 wk of age. However, the serum Ig concentration of the calves with the lowest Ig was still only about half of the value of the calves with the highest Ig at 12 wk of age. According to the definition of Gay (14) for failure of passive transfer of immunity (i.e., IgGl concentration in serum
The number of calves that were healthy, unhealthy (showed symptoms of diseases), or died during the study are presented in Table 2. Records for 1 weaned calf were excluded from
TABLE 2. Health and mortality of calves that were kept with dam for 5 d and then nipple fed (nursed calves) or immediately weaned and fed from open pail (weaned calves). Nursed calves (n = 15) Healthy Unhealthy Diarrhea Symptoms of respiratory disease Mortality'
Weaned calves (n = 14)
7
3
7
10
1 1
1 1
'Calves with symptoms of respiratory disease died.
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CALF MANAGEMENT, IMMUNOGLOBULINS. AND HEALTH
the disease data because the calf was thought to be lactose intolerant and was diarrhetic whenever milk was offered. The most common disease during the study was diarrhea, which was usually mild and lasted only 2 to 3 d. Most diarrhea occurred when the calves were 4 to 8 wk old. The calves that died during the study were those with symptoms of respiratory disease. The mean T24 of the healthy calves was 28.7 mg/ml (SD = 13.8 mg/ml), and the mean T24 of the calves with symptoms of diseases was 24.9 mg/ml (SD = 10.5 mg/ml). These T24 did not differ (P > .05). However, the weaned
calves had almost three times as many days of diarrhea (1 11 d) as the nursed calves had during the study (40 d). The risk of prolonged diarrhea was almost three times as high for weaned calves as for nursed calves (relative risk = 2.88; 95% confidence limits = 2.02 < relative risk < 4.09). DISCUSSION
Passive immunity developed in the same way for all calves in both management systems. All calves absorbed some Ig. However, the sooner the nursed calves received colostrum, the higher was the T24. This result
30
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Figure I . Mean serum concentrations (rt SE) of total Ig, IgGI, IgM, and IgA at different ages for the 30 calves. Journal of Dairy Science Vol. 78, No. 12, 1995
2742
RAJALA AND
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agrees with previous reports of the effect of early intake of first colostrum on the efficiency of Ig absorption (9, 19, 22, 30). Our results indicated that every 30-min delay in the intake of first colostrum decreased Ig concentration in serum by about 2 mg/ml. Of 30 calves, 6 showed a partial failure of passive transfer at the age of 48 h (1). Three of these failed to suckle during the first 6 h. Other reports (6, 7, 17, 23, 28, 29, 35) also show that a high percentage of calves fail to suckle within 4 to 8 h after birth, mostly because of poor udder conformation but also because of abnormal maternal behavior and poor calf vigor, especially after difficult calvings. Our results also agree with previous reports regarding the failure of passive transfer of immunity. Studies reported a failure of passive transfer of immunity for 61% (2) and 42% (4) of calves nursed by their dams because the calves failed to suckle or absorb colostral Ig when left with their dams for 1 d. The risk of failure of passive transfer of immunity seems to be greatest among calves left with their dams but not assisted to suckle early enough. An inadequate quantity of ingested colostrum might partially explain the low serum Ig concentrations among the nursed calves. ConJournal of Dairy Science Vol. 78, No. 12, 1995
versely, 3 calves that did not suckle within 6 h had relatively high Ig concentrations in their serum. As the amount of suckled colostrum was not determined in this study, we cannot explain these differences. High Ig concentrations in colostrum alone do not guarantee a high concentration of serum Ig. Presumably, individual differences exist in the efficiency of Ig absorption. Colostrum Ig concentrations did not correlate significantly with serum Ig concentrations at any age for the nursed calves. However, for the weaned calves, the correlation was significant, especially at 24 h of age, perhaps because all weaned calves received an equivalent amount of colostrum, but the amount of colostrum suckled by nursed calves was unknown. For all calves, both IgM and IgA concentrations started to increase at 4 wk of age, but IgGl declined up to 12 wk of age. This result agrees with previous results (18). In another study (15), the lowest serum IgGl concentration occurred at 16 d of age (15). This discrepancy with our results can be explained by the fact that the reported IgGl concentrations in that study were much lower than those of our study, and maternal antibodies acquired through colostrum influence the immunologi-
CALF MANAGEMENT, IMMUNOGLOBULINS, AND HEALTH
cal response of a newborn calf. For calves deprived of colostrum, endogenous Ig production O C C U K ~ much earlier than for calves that received a high level of passive immunity through colostrum (16). The onset of an increase in IgM and IgA concentrations at 4 wk of age probably indicates the start of their endogenous production. The total Ig concentration for the 30 calves continued to decline up to 10 wk of age, in agreement with the previous suggestion that endogenous production of Ig does not significantly begin to contribute to the total Ig in plasma during the first weeks of life (15) because the endogenous production is still minor to the catabolism of maternal antibodies. The most common disease among the calves was diarrhea. The number of days of diarrhea and the risk of prolonged diarrhea were three times as great for the weaned calves as for the nursed calves. However, the number of affected calves and the T24 did not differ between calf groups. Our observations agree with a previous study (23) of diarrhea morbidity of calves, which reported that morbidity was twofold lower for calves kept with their dams for 10 d after birth than for calves kept alone (23). In our study, diarrhea was most common at 4 to 8 wk of age, a time when IgM and IgA concentrations were lowest in calf serum. Feeding systems may affect the incidence of diarrhea. Zaremba et al. (37) reported that calves fed milk from an open pail four times daily had significantly higher incidence of diarrhea than calves fed for ad libitum intake from a nipple pail. Rapid ingestion of large amounts of milk or milk substitutes from an open pail can result in incomplete closure of the esophageal groove, formation of defective curd in abomasum, high pH in abomasum for several hours after feeding, excessively fast abomasal emptying, and overloading of the intestine, leading to bacterial overproliferation and diarrhea (3, 5, 26, 36). In our study, the amount of milk (3 L) consumed at one time may have been too large and may have caused the diarrhea. The presence of enteropathogens in feces was not determined, however, and the final reason for diarrhea remains unclear. CONCLUSIONS
In both management systems, the passive transfer of immunity of the newborn calves
2743
developed in the same way; however, individual differences in serum Ig concentrations were great. Delayed intake of first colostrum after birth decreased serum Ig concentration by about 2 mg/ml for each 30-min delay. High colostral Ig concentrations did not ensure high serum Ig concentrations among nursed calves. When calves are left with their dams after birth, they should be assisted so that they suckle dams as soon as possible to ensure the acquisition of high serum Ig concentrations. Weaned calves had about three times as many days of diarrhea as nursed calves, despite equal serum Ig concentrations. The reason for this difference remains unclear even though the diarrhea may have been caused by the feeding method. Therefore, nipple feeding is recommended. ACKNOWLEDGMENTS
This study was supported by The Finnish Society for Animal Welfare and The Academy of Finland. The authors thank the staff at the experimental farm of Helsinki University and also appreciate the help of Sole Rajala, Anou Londesborough, and Kati Leinonen. REFERENCES 1 Banks, K. L., and T. C. McGuire. 1989. Neonatal
immunology. Page 193 in Veterinary Clinical Immunology. R.E.W. Halliwell and N. T. Gorman, ed. W. B. Saunders Co., Philadelphia. PA. 2 Besser, T. E.. C. C. Gay. and L. Pritchett. 1991. Comparison of three methods of feeding colostrum to dairy calves. J. Am. Vet. Med. Assoc. 198:419. 3 Blowey, R. W. 1992. Digestive disorders of calves. Page 194 in Bovine Medicine. Diseases and Husbandry of Cattle. A. H. Andres, R. W. Blowey, H. Boyd, and R. G. Eddy. ed. Blackwell Sci. Pub]., Oxford. England. 4 Brignole, T. J.. and G. H. Stoa. 1980. Effect of suckling followed by bottle feeding colostrum on immunoglobulin absorption and calf survival. J . Dairy Sci. 63:451. 5Dirr, L., and G. Dirksen. 1989. Dysfunktion der Schlundrinne (“Pansenmnken”) als Komplikation der Neugeborenendimho beim Kalb. Tieraerztl. Prax. 17: 353. 6 Edwards, S. A. 1982. Factors affecting the time to first suckling in dairy calves. Anim. Prod. 34:339. 7 Edwards, S . A., and D. M. Broom. 1979. The period between birth and first suckling in dairy calves. Res. Vet. Sci. 26:255. 8 Edwards, S. A., and D.M. Broom. 1982. Behavioral interactions of dairy cows with their newborn calves and effects of parity. Anim. Behav. 30525. Journal of Dairy Science Vol. 78. No. 12, 1995
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9 Edwards, S. A.. D. M. Broom, and S. C. Collis. 1982. Factors affecting levels of passive immunity in dairy calves. Br. Vet. J. 138:233. 10Epi-info. Version 5. User's Guide. 1990. Cu. Dis. Control and World Health Organ. USD Inc., Stone Mountain, GA. 1 I Fallon, R. J. 1979. The effect of different methods of feeding colostrum on calf blood serum immunoglobulin levels. Page 507 in Calving Problems and Early Viability of the Calf. B. Hoffman, 1. L. Mason, and J. Schmidt, ed. Curr. Topics Vet. Med. Anim. Sci. Vol. 4. Martinus Niijhof Publ., The Hague, The Netherlands. 12 Fleenor. W. A., and H. Stott. 1983. Single radial immunodiffusion analysis for quantitation of colostral immunoglobulin concentration. J. Dairy Sci. 64:740. 13 Frazer. A. F., and D. M. Broom. 1990. Neonatal behaviour. Page 227 in Farm Animal Behaviour and Welfare. 3rd ed. Bailliere Tindall, London, England. 14 Gay, C. C. 1983. Failure of passive transfer of colostral immunoglobulins and neonatal disease in calves: a review. Page 346 in Proc. 4th Int. Symp. Neonatal Diarrhea. Vet. Infect. Dis. Organ., Saskatoon, SK, Canada. 15 Husband, A. J., M. R. Brandon, and A. K. Lascelles. 1972. Absorption and endogenous production of immunoglobulins in calves. Aust. J. Exp. Biol. Med. Sci. 50:491. 16 Husband, A. J., and A. K. Lascelles. 1975. Antibody responses to neonatal immunization in calves. Res Vet. Sci. 18:201. 17 Illmann, G.. and M. Spinka. 1993. Maternal behaviour of dairy heifers and sucking of their newborn calves in group housing. Appl. Anim. Behav. Sci. 36:91. 18 Kim, J. W., and F. W. Schmidt. 1983. Zur Frage der Absorption von kolostralen lmmunoglobulinen durch das Kalb. Dtsch. Tieraerztl. Wochenschr. 90:283. 19 Kruse, V. 1970. Absorption of immunoglobulin from colostrum in newborn calves. Anim. Prod. 12:627. 20 le Neindre. P. 1982. Cow-calf relationships: the effect of management systems. Page 24 in Welfare and Husbandry of Calves. J. P. Signoret, ed. Martinus Nijhoff Publ., The Hague, The Netherlands. 21 Lidfors, L., and P. Jensen. 1988. Behaviour of freeranging beef cows and calves. Appl. Anim. Behav. Sci. 20237. 22 Matte, J. J., C. L. Girard, J. R. Seoane, and G. J. Brisson. 1982. Absorption of colostral immunoglobulin G in the newborn dairy calf. J. Dairy Sci. 65:1765. 23 Metz, J. 1984. Behaviour and state of health of cows and calves kept together or separately in the post partum period. Page 358 in Proc. Int. Congr. Appl.
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CASTRBN Uhol. Farm Anim. J. Unshelm, G. van Putten, and K. Zeeb, ed. Kuratorium Technik Bauwesen Landwirtschaft, Kiel, Germany. 24 Petrie, L. 1984. Maximising the absorption of colostral immunoglobulins in the newborn dairy calf. Vet. Rec. 114:157. 25 Roy, J.H.B. 1990. The Calf. Volume 1. Management of Health. 5th ed. Butterworths, London, England. 26 Ruckebusch. Y. 1988. Motility of the gastro-intestinal tract. Page 64 in The Ruminant Animal: Digestive Physiology and Nutrition. D. C. Church, ed. Reston Book Publ., Englewood Cliffs. NJ. 27 SAS@ User's Guide: Statistics, Version 6 Edition. 1988. SAS Inst., Inc., Cary, NC. 28 Selman, I. E., A. D. McEwan, and E. W. Fisher. 1970. Studies on natural suckling in cattle during the first eight hours post partum 1. Behavioural studies (calves). Anim. Behav. 18:284. 29 Selman, I. E., A. D. McEwan, and E. W. Fisher. 1971. Studies on dairy calves allowed to suckle their dams at fixed times post partum. Res. Vet. Sci. 12:l. 30Stott. G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. I. Period of absorption. J. Dairy Sci. 62: 1632. 31 Stott, G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. 11. The rate of absorption. J. Dairy Sci. 62: 1677. 32 Stott, G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. 111. Amount of absorption. J. Dairy Sci. 62: 1902. 33 Ston, G. H., D. B. Marx, B. E. Menefee, and G. T. Nightengale. 1979. Colostral immunoglobulin transfer in calves. IV. Effect of suckling. J. Dairy Sci. 62: 1908. 34Tizard. I. 1992. Immunity in the fetus and newborn. Page 248 in Veterinary Immunology, An Introduction. 4th ed. W. B. Saunders Co., Philadelphia, PA. 35 Ventorp, M., and P. Michanek. 1992. The importance of udder and teat conformation for teat seeking by the newborn calf. J. Dairy Sci. 75:262. 36Zaremba. W. 1983. Futterungstechnik und Ihre Bedeutung fur den gesundheitszustand neugeborener Kdber unter Besondere Berucksichtung der Diarrhoea. Prakt. Tieraerztl. 11:977. 37Zaremba. W., E. Grunert, and A. Binder. 1982. Der Einfluss verschiedener Trhkeverfahren auf die Gesundheit neugeborener Kiilber. Tieraerztl. Umsch. 71469.