Administration of Recombinant Bovine Somatotropin to Dairy Cows for Four Consecutive Lactations

Administration of Recombinant Bovine Somatotropin to Dairy Cows for Four Consecutive Lactations J. T. HUBER,*,1 Z. WU,*,2 C. FONTES, JR.,*,3 J. L. SULLIVAN,*,4 R. G. HOFFMAN,† and G. F. HARTNELL† *Department of Animal Sciences, University of Arizona, Tucson 85721 †Monsanto Company, St. Louis, MO 63167

ABSTRACT Effects of long-term administration of recombinant bovine somatotropin (bST) to dairy cows on complete lactational performance [60 ( ±3 ) to 284 ( ±3 ) d in milk (DIM)] were studied for four consecutive lactations. Beginning on d 60 ( ±3 ) postpartum, Holstein cows received biweekly injections (500 mg) of bST ( n = 39) or a placebo (control; n = 39) during the first lactation of the study. Cows either continued on the same treatment ( n = 26) or were switched to the opposite treatment ( n = 29) during the second lactation. Cows that changed treatments were injected for only 16 wk during the second lactation. Six cows per treatment completed four consecutive lactations. Treatment with bST during the first lactation did not have a residual effect on milk yields during the second lactation. Injections of bST during the second lactation increased milk yield 6.5 kg/d from 60 ( ±3 ) to 172 DIM. For the four lactations, cows receiving bST yielded 3.7 kg/d (14%) more milk and gained 52 kg (37%) more body weight than did controls. Pretreatment (from 0 to 56 DIM) milk yields in yr 2, 3, and 4 were not affected by previous bST treatment. Milk yield, efficiency of feed utilization, and body weights were enhanced in cows injected with bST for four consecutive lactations. Previous bST treatment did not diminish milk yields in subsequent lactations. ( Key words: dairy cows, bovine somatotropin, milk yield, lactation) Abbreviation key: BCS = body condition score. INTRODUCTION More than 1000 studies with over 20,000 cows have shown that recombinant bST increases milk yields

Received August 16, 1996. Accepted March 24, 1997. 1Reprint requests. 2Present address: US Dairy Forage Research Center, 1925 Linden Dr. West, Madison, WI 52706. 3Present address: Cargill, Inc., Uberlandia, Minas Gerais, Brazil. 4Present address: Dairy Nutrition Services Incorporated, 900 West Chandler Boulevard, Suite D-2, Chandler, AZ 85224. 1997 J Dairy Sci 80:2355–2360

and efficiency of feed utilization in lactating cows ( 3 ) . Regimens of administration have included daily, biweekly, or monthly injections ( 3 ) . However, there are relatively few reports on the response to bST in multilactation studies. Administration of bST for two (1, 5, 8), three, or four ( 1 6 ) lactations resulted in consistent increases in milk yield and efficiency compared with controls but had no effect on overt animal health or physiology. In contrast, Gibson et al. ( 9 ) reported reduced milk yields during the first 9 wk of the second and third lactations after treatment with bST in previous lactations, and McBride et al. ( 1 4 ) reported reduced efficiency of feed conversion during the second lactation after treatment. The objectives of this study were 1 ) to determine the effects of bST administration for four consecutive lactations on performance of cows and 2 ) to determine the influence of bST treatment during previous lactations on subsequent performance. MATERIALS AND METHODS For the first lactation, 78 Holstein cows were divided into control ( n = 39) and treatment ( n = 39) groups. Treatment cows were injected intramuscularly at 14-d intervals from 60 ( ±3 ) DIM until the end of lactation with 500 mg of Zn methionyl bST suspended in 3 ml of a prolonged-release formulation of sesame oil (Monsanto Co., St. Louis, MO). Injections were administered at four alternating sites on the right or left sides in a dorsal and ventral position of the hind thigh musculature. Control cows received the suspension agent without bST. Treatment means for milk yield, milk composition, DMI, and BW were adjusted by covariance for the 39- to 60-d pretreatment period. Even though injections were continued until the end of lactation or until cows that did not conceive were sold, data were compared for 32 wk of treatment to eliminate bias of dissimilar effects of varying lactation lengths. For the second, third, and fourth lactations, a similar treatment schedule was used, but injections were subcutaneous at four alternate locations in the heart girth region just behind the front legs. Sites of injec-

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HUBER ET AL.

TABLE 1. Scheme of bST treatment through four consecutive lactations and number of cows per treatment. Lactation Treatment

1

Control

391 ... 391 ...

bST

2

3

(no. of cows per treatment) 121 71 152 ... 141 91 142 ...

4 61 ... 61 ...

1Cows received biweekly injections of 500 mg of bST for 32 wk of each lactation starting on d 60 ( ±3). 2Cows received biweekly injections of 500 mg of bST for 16 wk starting on d 60 ( ±3).

tion were on either side in a dorsal or ventral position. Data for the first lactation were reported by Sullivan et al. (20). Twenty-seven cows on the control treatment and 28 cows that received bST during lactation 1 continued on treatment during lactation 2. Of the 27 control cows, 12 continued on placebo injections for the complete lactation, and 15 were switched to bST injections for 16 wk during lactation 2 (Table 1). Of the 28 cows that received bST during lactation 1, 14 received bST starting at 60 ( ±3 ) d postpartum until the end of lactation, and 14 were switched to placebo injections for 16 wk. All cows that switched treatments during lactation 2 were discontinued from treatment after 16 wk (eight injections) or approximately 172 d postpartum. Of the 12 control cows that received placebo injections and completed lactation 2, 7 completed lactation 3, and 6 completed lactation 4. Of the 14 cows treated with bST injections that completed lactation 2, 9 completed lactation 3, and 6 completed lactation 4. Treatment cows were culled from the herd in a normal manner, principally for failure to conceive or for low milk yields. For the first two lactations of treatment cows, three formulations of TMR were used, depending on milk yield and the body condition of cows. Ingredients, nutrient content of the TMR, and feeding schedule were as described by Sullivan et al. (20). The NEL of the three TMR were approximately 1.71, 1.68, and 1.60 Mcal/kg. Diet 1 was fed to all cows until 90 DIM. Thereafter, cows were switched to diet 2 when milk yield averaged <31.8 kg/d for 7 consecutive d and to diet 3 when milk had dropped to <22.7 kg/d. When cows were judged to be overconditioned or underconditioned for their stage of lactation, some latitude was taken to change from one TMR to another. Nutrient content of the TMR varied slightly from year to year but was the same for the two treatments. Feed intakes of individual cows were Journal of Dairy Science Vol. 80, No. 10, 1997

recorded in the first 2 yr of treatment, as described by Sullivan et al. (20), but not in the last 2 yr during which cows were fed in groups with herdmates. From the beginning of pretreatment to the end of treatment in each lactation, milk yields were recorded at each milking (0500 and 1700 h). Milk samples were taken weekly from two consecutive milkings, composited, and determined by infrared procedures (Foss 360; Foss Technology, Eden Prairie, MN) for fat, true protein, and lactose content and for SCC at the DHIA laboratory (Phoenix, AZ). Body weights were determined, and body condition scores ( BCS) were estimated at the beginning of treatment and at weekly intervals thereafter for lactations 2, 3, and 4. During lactation 1, measurements were made biweekly. Cows were weighed after the 1700-h milking, and a BCS was assigned according to a five-point scale ( 1 = thin to 5 = fat) with 0.25 increments (22). Changes in BW and BCS during treatment in each lactation and in all four lactations (final measures in yr 4 minus initial measures in yr 1 ) were computed. Statistical analyses were performed using the general linear models procedure of SAS ( 1 8 ) employing the following models: Y = m + T1 + T2 + T1T2 + Cov + e

[1]

Y = m + T + Yr + YrT + Cov + e

[2]

Y = m + T + Yr + P + TP + e

[3]

Y = m + T + Yr + e

[4]

where Y = observation, m = population mean, T1 = yr 1 treatment, T2 = yr 2 treatment, T1T2 = yr 1 treatment × yr 2 treatment, Cov = covariate using data from pretreatment, e = random error, T = treatment over 4 yr, Yr = year, YrT = interaction of Yr and T, P = period, and TP = interaction of T and P. Model [1] was for data from yr 2 (55 cows; 16-wk treatment), and Models [2], [3], and [4] were for data from cows that received the same treatments for four lactations (12 cows; 32-wk treatment in each year). Analyzed parameters using Model [1] were DMI and milk traits. Model [2] used data from individual years on milk parameters, BW changes, and BCS changes for all 4 yr and DMI and the ratio of FCM:DMI for yr 1 and 2 to test treatment effects and treatment by year interactions. Model [3] was used to analyze treatment and lactation period interactions in milk and FCM yields by dividing the 32 wk of treatment into four 8-wk periods and using data from all 4 yr. Model [4] was used to analyze effects of previous treatments on milk traits during pretreatments (from 0 to 56 DIM) in yr 2, 3, and 4. Because of a lack of significance ( P > 0.25), certain inter-

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TABLE 2. Least squares means for milk and body condition traits of cows receiving control ( C ) or bST treatments from d 60 to 284 postpartum in 4 consecutive yr of lactation ( n = 6; Model [2]). 1 Lactation 1 Trait

C

Milk, kg/d 29.8 3.5% FCM, kg/d 29.2 Milk fat % 3.35 kg/d 1.00 Milk protein % 3.10 kg/d 0.92 Milk lactose, % 4.86 Milk SCC, log 10/ml 5.22 BW, kg × 102 Initial 5.89 Change 0.79 Final 6.68 BCS2 Initial 2.90 0.45 Changes3 Final 3.34

Lactation 2

Lactation 3

Lactation 4

All lactations

bST

P <

C

bST

P <

C

bST

P <

C

bST

P <

C

bST

P <

SE

32.9 32.9

0.19 0.07

24.3 24.7

29.7 28.6

0.02 0.06

26.8 26.0

31.6 29.2

0.05 0.13

25.0 23.7

26.5 25.5

0.5 0.4

26.5 25.9

30.2 29.1

0.01 0.01

0.8 0.7

3.43 1.11

0.60 0.21

3.62 0.92

3.23 0.98

0.01 0.53

3.61 0.95

3.28 0.99

0.03 0.63

3.47 0.83

3.24 0.86

0.12 0.70

3.51 0.93

3.29 0.99

0.01 0.17

0.05 0.03

3.09 1.01 4.89 5.30

0.93 0.22 0.85 0.47

3.15 0.78 4.68 5.30

3.07 0.32 0.91 0.07 4.62 0.57 5.33 0.71

3.20 0.85 4.61 5.25

3.08 0.18 0.95 0.20 4.61 0.96 5.21 0.72

3.05 0.76 4.54 4.54

3.05 0.98 0.82 0.39 4.38 0.18 4.32 0.05

3.13 0.83 4.67 5.08

3.07 0.23 0.92 0.01 4.63 0.40 5.04 0.52

0.03 0.03 0.04 0.04

6.10 0.88 6.98

0.57 0.62 0.38

6.41 0.76 7.17

6.86 0.93 7.82

0.25 0.21 0.07

6.36 0.79 7.26

7.07 0.90 7.96

0.07 1.0 0.05

6.82 0.50 7.31

7.38 0.15 0.66 0.16 8.04 0.04

6.37 1.42 7.11

6.85 1.94 7.70

0.57 0.04 0.04

6.10 0.14 8.04

2.83 0.27 3.10

0.79 0.43 0.31

2.52 0.76 3.28

2.56 0.72 3.29

0.86 0.87 0.98

2.71 0.50 3.21

2.79 0.43 3.21

0.75 0.75 0.98

2.85 0.33 3.18

2.81 0.49 3.29

2.75 0.27 3.25

2.75 0.46 3.21

1.0 0.47 0.75

0.17 0.16 0.17

0.86 0.49 0.62

1All

means were covariate-adjusted for the pretreatment period (39 to 60 DIM) of each lactation. condition score assigned on a five-point scale where 1 = thin to 5 = fat (22). 3For all 4 yr, values for each were obtained by subtracting initial values from final values for that year. Values for the four combined lactations were obtained by subtracting the initial values for yr 1 from final values for yr 4. 2Body

actions in Models [3] and [4] were pooled stepwise into the error terms. For all of the analyses, least squares means are presented. RESULTS AND DISCUSSION For cows that received the same treatments for 4 yr ( n = 12), yields of milk and FCM (Table 2 ) were apparently higher for cows treated with bST than for control cows in each year, but the differences in milk yield were significant only for yr 2 and 3 ( P < 0.02 and P < 0.05, respectively), and differences for FCM tended to be significant for yr 1, 2, and 3 ( P < 0.07, P < 0.06, and P < 0.13, respectively). For the combined 4-yr period, milk yield was 3.7 kg/d or 14% higher, and FCM yield was 3.2 kg/d or 12% higher ( P < 0.01), for cows treated with bST than for control cows. The increases as percentages of the control were smallest in yr 4, 6% for milk and 7% for FCM, suggesting that enhancement of bST on milk yield diminished in the 4th yr of treatment. However, because differences between the treatments were not significant in either yr 1 or 4, this observation needs to be confirmed. Gibson et al. ( 9 ) reported lower milk yields of cows receiving bST during the second or third lactation than for cows receiving bST during the first lactation, but yields of cows treated previously with bST were higher than those of controls. Conclusions pertaining to the prolonged response to bST in that study ( 9 )

are difficult because none of the cows received the placebo treatment for more than one lactation. In the present study with adequate controls, the greatest responses to bST were observed during lactations 2 and 3. Fat percentages of milk were lower for cows treated with bST than for control cows during the second ( P < 0.01) , third ( P < 0.03), and fourth lactations ( P < 0.12) as well as for the combined years ( P < 0.01; Table 2). One possible explanation is that cows receiving bST probably remained on the high nutrient density diet (lower fiber) for a longer period because of their higher milk yields. Effects of bST on milk fat content in early lactation noted by Richard et al. ( 1 7 ) were opposite those observed in this study and were associated with negative energy balances. In our study, energy balances [estimated from NEL intake, secretion of milk, and expenditure of energy for maintenance and BW gain using relationships from NRC (15)] were positive during the injection periods of all years for both treatments (data not shown). The increases in BW gains and BCS observed during all lactations confirmed a positive energy balance for both control and treatment cows. Because of higher milk yields, yields of milk fat of cows treated with bST were not lower than those of controls despite a decrease in milk fat percentages. Protein and lactose percentages of milk did not differ between the treatment groups, which was similar to the results of other Journal of Dairy Science Vol. 80, No. 10, 1997

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HUBER ET AL. TABLE 3. Least squares means for DMI and efficiency of feed utilization of cows receiving control ( C ) or bST treatments for two consecutive lactations ( n = 6; Model [2]). Lactation 1

Lactation 2

Item

C

bST

P <

C

bST

P <

SE

DMI, kg/d FCM:DMI

24.9 1.13

26.0 1.24

0.44 0.09

22.5 1.08

23.1 1.24

0.74 0.03

0.7 0.03

studies [(1, 2, 8, 10); Table 2]. Protein yield was higher ( P < 0.03) for cows treated with bST than for control cows for the combined four lactations. Milk SCC were not increased by bST in any of the years. Cows gained BW and BCS during each year; no significant differences in magnitude of gain between treatments was noted during any single year (Table 2). However, over the entire 4 yr of treatment, BW gain was 37% (52 kg) higher ( P < 0.04) for cows treated with bST than for control cows. The initial BW averaged 610 and 589 kg ( P > 0.50), and the final BW averaged 804 and 731 kg ( P < 0.04), for the treatment and control groups, respectively. Conversely, gains in BCS were similar, as were the final BCS. Studies employing injections of bST for one lactation showed lesser (6, 19, 21) or similar (1, 10, 13) gains in BW and BCS compared with controls. The greater BW gain and heavier BW at the end of the 4th yr of bST treatment was not attributable to increased fatness, because BCS were not different. Instead, the gain might reflect a larger digestive tract or muscular tissues. Soderholm et al. ( 1 9 ) observed a decrease in empty body fat weight after cows were administered bST for 32 wk, and Brown et al. ( 4 ) observed increased leanness of carcass and N retention in lactating cows treated with bST for 7 wk compared with controls. In finishing pigs, administration of recombinant porcine somatotropin increased

growth of muscle and visceral tissues but decreased adipose tissue deposition (12). Mean DMI for the first 2 yr of treatment showed no significant changes because of bST (Table 3). Only those 6 cows in each treatment that completed four lactations were used for this analysis in an effort to corroborate the results of other studies. Downer et al. ( 7 ) attributed the lack of response in DMI to bST to a positive energy balance in cows treated with bST. Accordingly, the positive energy balance observed in our study did not limit milk yield or result in higher feed intakes. Administration of bST appeared to increase milk yields by increasing efficiency of feed utilization, as was suggested from the higher ratios of FCM:DMI for cows treated with bST than that for control cows (Table 3). Increased gross feed efficiency for milk yield was also reported by others (1, 19, 21). Measuring intakes during yr 3 and 4 would have been desirable, but was not possible. Least squares means for milk and FCM yields for different periods over four lactations (Table 4 ) showed increases ( P < 0.10) for cows treated with bST over control cows for periods 2 (wk 9 to 16) and 3 (wk 17 to 24) of treatment but not for periods 1 (wk 1 to 8 ) or 4 (wk 25 to 32) of treatment. Results were similar to data from yr 1 for these same cows (20). A plot of mean milk yield from the 4 yr (Figure 1 ) shows that a milk yield response to bST was not

TABLE 4. Least squares means for milk and FCM yields for four 8-wk periods of cows receiving control ( C ) or bST treatments for four consecutive lactations ( n = 6; Model [3]). Milk1,2 (bST – C ) × 100/C

Period

DIM

C

bST

1 2 3 4

60–116 117–172 173–228 229–284

36.5 30.4 23.6 16.5

(kg/d) 38.5 5.5 33.8 11.2 27.5 16.5 18.8 13.9

1SE

(bST – C ) × 100/C

P <

C

bST

0.27 0.05 0.03 0.19

34.8 29.3 23.5 17.5

(kg/d) 37.0 6.3 32.3 10.2 26.3 11.9 18.2 4.0

= 1.3.

2Interactions 3SE

FCM2,3

between treatment and period were not significant ( P > 0.5).

= 1.2.

Journal of Dairy Science Vol. 80, No. 10, 1997

P < 0.21 0.08 0.10 0.40

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TABLE 5. Least squares means for milk, FCM, and fat and protein percentages of milk during pretreatment ( 0 to 56 DIM) in lactations 2, 3, and 4 from cows that previously received bST or control ( C ) injections during treatment (60 to 284 DIM) in lactations 1, 2, and 3 ( n = 6; Model [4]). Lactation 2

Lactation 3

Lactations 2, 3, and 4

Lactation 4

Item

C

bST

C

bST

C

bST

C

bST

SE1

Milk, kg/d FCM, kg/d Milk fat, % Milk protein, %

41.3 41.0 3.42 3.15

38.0 37.4 3.42 3.08

34.1 36.4 3.94 3.02

32.1 33.9 3.89 3.02

35.5 37.9 3.93 3.16

38.7 39.8 3.61 2.84

37.0 38.4 3.76 3.11

36.4 37.0 3.64 2.98

1.7 1.9 0.12 0.05

1Differences between C and bST treatments were not significant ( P > 0.23) for either individual or all three lactations for any of the variables except for protein percentage of milk, which was lower ( P < 0.06) for cows treated with bST than for control cows in lactation 4.

clearly established until wk 3 to 4 of treatment. Using cows in stages of lactation that were similar to those of cows used in our study, Downer et al. ( 7 ) showed that response was maximized at about wk 5 after initiation of treatment. The low milk yields for the 24- to 32-wk period might explain the lack of a significant difference between the bST and control treatments for that period. Soderholm et al. ( 1 9 ) also reported diminished milk yield responses when cows yielded <20 kg/d of milk in late lactation. Effects of previous bST treatment on subsequent lactation performance were evaluated in two ways. First, data (Table 5 ) from the 12 cows that completed 4 yr of treatment showed that injections of bST in yr 1, 2, and 3 did not change any of the milk traits during the pretreatment periods in yr 2, 3, and 4,

except for milk protein percentage in the 4th yr, which was lower ( P < 0.06) for cows treated with bST than for cows in the control group. These results agree with those of Oldenbroek et al. (16). Also, Dahl et al. ( 6 ) noted that milk yields of cows treated with bST returned to normal after cessation of treatment. The second test for residual effects of bST used data (Table 6 ) from the 55 cows in yr 2, which showed no interactions between treatments during yr 1 and 2 in any of the measured lactational parameters. Milk and FCM yields and the ratio of FCM:DMI in yr 2 were increased ( P < 0.01) by bST treatment during yr 2 but not by bST treatment during yr 1; increases with bST in yr 2 were independent of treatment in yr 1. Results were in contrast to those of Hemken et al. (11), who observed a diminished response by cows receiving bST for a se-

TABLE 6. Effect of bST injections (500 mg/14 d), received either continuously or variously, on performance of cows from 60 to 172 DIM during lactation 2 (Model [1]). Treatment1 Item

Treatment effect2

CC ( n = 12)

CB ( n = 15)

BC ( n = 14)

BB ( n = 14)

SE

Lactation 1 × Lactation 1 Lactation 2 lactation 2

33.7 31.3

40.1 37.3

32.4 30.9

39.0 37.2

0.9 1.0

0.19 0.79

0.01 0.01

0.93 0.90

P < Milk,3 kg/d 3.5% FCM, kg/d Milk fat % kg/d Milk protein % kg/d Milk lactose, % Milk SCC, log 10/ml DMI, kg/d FCM:DMI

3.13 1.05

3.11 1.24

3.22 1.04

3.23 1.25

0.09 0.04

0.28 0.94

0.97 0.01

0.89 0.78

3.07 1.04 4.82 2.30 26.6 1.19

3.09 1.23 4.90 2.38 27.3 1.40

3.05 0.99 4.80 2.37 26.4 1.16

3.11 1.20 4.83 2.21 26.8 1.35

0.03 0.03 0.06 0.60 0.6 0.03

0.97 0.23 0.47 0.74 0.55 0.29

0.31 0.01 0.35 0.76 0.31 0.01

0.57 0.73 0.72 0.28 0.84 0.75

1C = Control; B = bST injection. For each group, the first letter designates the treatment received during lactation 1, and the second letter designates the treatment received during lactation 2. During lactation 1 cows were treated from d 60 to the end of lactation. 2Effects were lactation 1 = CC and CB versus BC and BB; lactation 2 = CC and BC versus CB and BB. 3Milk yields for groups CC, CB, BC, and BB up to d 116 of treatment during lactation 1 were 33.4, 31.8, 35.3, and 37.0 kg/d, respectively.

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Figure 1. Milk yields over 32 wk averaged from four consecutive lactations of cows receiving control ( ⁄) or bST ( + ) treatments ( n = 6).

cond lactation compared with those that did not receive bST previously. Milk yields of cows that received the different treatments in yr 1 and 2 provide a clear contrast between those treated with bST and control cows. CONCLUSIONS Administration of recombinant bST to lactating Holstein dairy cows for four consecutive lactations increased milk yields. No significant changes were found in protein and lactose concentrations in milk, but milk fat concentrations were decreased. Apparently, recombinant bST increased milk yields by enhancing efficiency of feed utilization. Injections of bST for four consecutive lactations showed an overall enhancing effect on BW gain. Treatment with bST in previous lactations did not affect milk yields or milk yield responses to bST in subsequent lactations. REFERENCES 1 Annexstad, R. J., D. E. Otterby, J. G. Linn, W. P. Hansen, C. G. Soderholm, J. E. Wheaton, and R. G. Eggert. 1990. Somatotropin treatment for a second consecutive lactation. J. Dairy Sci. 73:2423. 2 Barbano, D. M., J. M. Lynch, D. E. Bauman, G. F. Hartnell, R. L. Hintz, and M. A. Nemeth. 1992. Effect of a prolongedrelease formulation of N-methionyl bovine somatotropin (sometribove) on milk composition. J. Dairy Sci. 75:1775. 3 Bauman, D. E. 1992. Bovine somatotropin: review of an emerging animal technology. J. Dairy Sci. 75:3432. 4 Brown, D. L., S. J. Taylor, E. J. DePeters, and R. L. Baldwin. 1989. Influence of sometribove, USAN (recombinant methionyl bovine somatotropin) on the body composition of lactating cattle. J. Nutr. 119:663. 5 Burton, J. L., B. W. McBride, J. H. Burton, and R. G. Eggert. 1990. Health and reproductive performance of dairy cows Journal of Dairy Science Vol. 80, No. 10, 1997

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