Effect of prepartum milking of primigravid cows on mammary gland health and lactation performance

Livestock Production Science 86 (2004) 105 – 116 www.elsevier.com/locate/livprodsci

Effect of prepartum milking of primigravid cows on mammary gland health and lactation performance J.E.P. Santos *, R.L.A. Cerri, J.H. Kirk, S.O. Juchem, M. Villasenˇor Veterinary Medicine Teaching and Research Center, University of California – Davis, 18830 Road 112, Tulare, CA 93274, USA Received 5 November 2002; received in revised form 27 May 2003; accepted 6 June 2003

Abstract The objectives were to determine the effects of prepartum milking of primigravid cows on mammary gland health, lactation performance and metabolic parameters during late gestation and early lactation. Primigravid Holstein cows, 267, were assigned to one of two treatments consisting of either three times daily milking or no milking during the last 15 days of gestation. Milk samples were collected for microbiological culture from all prepartum-milking cows at 15 days prepartum, and from all cows at 2 and 28 days postpartum. Udder edema was ‘assessed’ weekly by digital pressure of the udder and at day 2 postpartum by measuring the udder floor area immediately before and after milking. Blood was collected on days
11 and 14, and 4 and 17 days relative to calving for analyses of plasma glucose, h-OH-butyrate, and nonesterified fatty acids (NEFA). Prepartum milking reduced udder edema, proportion of cows with positive bacterial isolate in milk, somatic cell count, and incidence of mastitis during the first 135 days in milk. Primigravid cows milked prepartum produced 1.7 kg/day more milk and 1.1 kg/day more 3.5% fat-corrected milk. Plasma concentrations of glucose decreased and of h-OH-butyrate and NEFA increased around parturition, which resulted in a higher incidence of subclinical ketosis for cows milked prepartum. D 2003 Elsevier B.V. All rights reserved. Keywords: Prepartum milking; Mastitis; Udder edema; Dairy cows; Heifer

1. Introduction Primigravid cows are more likely to develop udder edema around calving and udder edema has been associated with increased incidence of mastitis during the periparturient period (Waage et al., 2001). Preliminary data from Bowers et al. (2002b) indicated that prepartum milking reduces the degree of udder edema as well as electrical conductivity of milk, the latter being an indirect indicator of decreased subclinical * Corresponding author. Tel.: +1-559-688-1731; fax: +1-559686-4231. E-mail address: [email protected] (J.E.P. Santos). 0301-6226/$ - see front matter D 2003 Elsevier B.V. All rights reserved. doi:10.1016/S0301-6226(03)00149-0

mastitis. Others have previously shown that incidence of new intramammary infections early in lactation is reduced by twice daily milking during the last 2 weeks prepartum (Greene et al., 1988). In addition to its effects on udder edema and intramammary infections, mammary secretory tissue development is increased postpartum upon removal of milk prepartum (Akers et al., 1977). The acclimation of primigravid cows to milking parlor and milking procedures might be beneficial to lactation performance. Introducing heifers to the milking barn prepartum might reduce stress at the time of calving. If removal of milk prior to calving affects secretory cell development, udder edema, and inci-

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dence of mastitis, it is expected that prepartum milking of primigravid cows should benefit udder health and subsequent lactation performance. The idea of milking prepartum multiparous cows has been investigated to reduce hepatic infiltration of triglycerides near the time of calving with little success (Grummer et al., 2000). Despite the tendency to increase prepartum DM intake in cows milked prior to calving, plasma glucose concentrations at calving were reduced and no effect was observed for plasma NEFA and hepatic triglycerides. The sharp decrease in plasma glucose around calving observed by Grummer et al. (2000) when cows were milked prepartum might have negative effects on energy metabolism and result in a higher incidence of ketosis. The objectives of this study were to determine the effects of prepartum milking of primigravid cows during the last 2 weeks of gestation on mammary gland health, lactation performance, and metabolic parameters during the first 135 days in lactation.

2. Materials and methods 2.1. Animals, housing, and feeding Two-hundred and eighty primigravid prepartum Holstein cows from a commercial dairy farm in the Central Valley of California were assigned to one of the two treatments in a randomized complete block design (Kuehl, 1994) on the basis of age and expected calving date. A total of 13 cows were excluded from the study because they remained in the prepartum treatments either less than 10 days, or more than 25 days. The remainder 267 cows (139 controls and 128 prepartum-milking) were included in the data analyses. The study period lasted 150 days and was composed of 15 days during the prepartum period and 135 days during the postpartum period. During the pre- and postpartum periods, all cows were housed in the same corrals and fed the same total mixed ration (TMR) described in Table 1. The prepartum steam-up diet was fed for the last 21 days of gestation. Diets were fed once daily, at 7:00 and 11:00 h for lactating and prepartum cows, respectively. During the postpartum period, all cows were housed in the same free-stall barn during the first 135 days in lactation.

Table 1 Dietary ingredients and nutrient composition of diets Ingredients

Corn silage Alfalfa hay Steam-flaked corn grain Steam-rolled barley grain Almond hulls Soybean meal, 47% CP solvent extracted Lignosulfonate treated soybean mealb Animal marine protein blendc Whole cottonseed Tallow Mineral and vitamin premixd Nutrient DM,% NEL,e Mcal/kg CP, % Fat, % Ash, % NDF, % ADF, % NFC,f % Ca, % P, % K, % Mg, % S, % Na, % Cl, % Zn, mg/kg Cu, mg/kg Mn, mg/kg

Dietsa Prepartum (% DM)

Postpartum

37.5 23.5 21.4 – 7.2 –

24.0 21.6 19.6 3.2 8.0 3.9

4.2

5.1

1.0 1.2 – 4.0

1.3 10.0 1.3 2.0

53.0 1.60 14.9 3.6 6.8 35.0 23.6 40.6 0.82 0.31 1.56 0.32 0.19 0.05 0.39 88 24 86

57.1 1.67 17.4 5.5 7.4 32.7 22.4 38.3 0.86 0.53 1.38 0.34 0.26 0.43 0.39 62 23 64

a Prepartum=steam-up diet fed during the last 21 days prepartum; postpartum=diet fed during the entire postpartum period. b Lignosulfonate treated soybean meal; Amino PlusR (Ag Processing, Emmetsburg, IA, USA). c Pro-LakR (blend of marine and animal by-products; H. J. Baker and Bro., Stamford, CT, USA). d Prepartum: Ca, 0.7%; P, 0.8%; K, 1.1%; Mg, 2.5%; Na, 0.1%; Cl, 0.1%; S, 0.5%; and (per kg) 1330 mg of Zn, 1100 mg of Mn, 307 mg of Cu, 15 mg of I, 2.3 mg of Co, and 6 mg of Se; postpartum: Zinpro 4-plex, 2.0%; Ca, 4.5%; P, 2.2%; K, 4.2%; Mg, 2.5%; Na, 5.6%; Cl, 2.1%; S, 0.9%; and (per kg) 890 mg of Zn, 580 mg of Mn, 200 mg of Cu, 15 mg of I, 14 mg of Co, and 8 mg of Se. e NEL=net energy for lactation according to NRC (2001) adjusted for the average DM intake during the prepartum (12.1 kg/day) and postpartum (19.4 kg/day) periods based on group data. f NFC=nonfibrous carbohydrates fNFC ¼ OM
ðCP þ NDF þFatÞg.

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Pre- and postpartum diets were sampled monthly, dried at 55 jC for 48 h and ground in a Wiley mill (Arthur H. Thomas CO., Philadelphia, PA, USA) to pass a 2-mm screen, then in a cyclone mill (Udy Co., Fort Collins, CO, USA) to pass a 1-mm screen. Samples were then composited and analyzed monthly for dry matter (DM), organic matter, and crude protein (AOAC, 1990), neutral detergent fiber (Robertson and Van Soest, 1981), acid detergent fiber (Goering and Van Soest, 1970), and minerals. The mineral content of diets was determined at the Dairyland Laboratory (Arcadia, WI, USA) using an ICP plasma emission spectrometer (Thermo Garrell Ash, Franklin, MA, USA). The experiment was conducted from February to September 2001. Diets were fed to allow for 3– 5% refusal of the total amount offered, which was estimated once daily when weigh backs were collected and weighed. Body condition of all cows was scored (Ferguson et al., 1994) on two consecutive days just prior to the beginning (days
16 and
15 relative to calving) and at the end of the study (130 and 131 days in lactation), and again at 1, 28, and 60 days postpartum.

analyzed for SCC, fat and true protein concentrations (Foss 303 Milk-O-ScanR; Foss Foods, Eden Prairie, MN, USA) at the DHIA Laboratory in Tulare, CA, USA.

2.2. Milking

2.4. Determination of udder edema

During the prepartum period, the milking group was milked three times daily, and during the postpartum period, all cows were milked three times daily starting at 5:30, 13:30, and at 20:30 h. The milking units were equipped with automatic take offs and those were set with a delay time of 90 s. An additional 1 s delay was set once the sensor noticed no milk flow. In case any milk is sensed during that second, the sensor is reset and the take offs are not activated again until no milk flow is sensed. The electric resistance for the take offs to be activated was set at 600 ohms. Therefore, every cow was milked for at least 91 s regardless of milk flow. All cows received 500 mg of exogenous bovine somatotropin (PosilacR, Monsanto Co., St. Louis, MO, USA) every 14 days, starting between 60 and 67 days postpartum. Milk yields were recorded for individual cows once monthly during the official California dairy herd improvement association (DHIA) test. Individual milk samples were also collected from consecutive milkings, composited, and

The degree of udder edema was determined in each cow once during the first 60 h after calving. Udder floor areas were measured immediately before and after the a.m. milking to objectively quantify severity of edema. Sheets of paper were pressed against wet teat ends just prior to and immediately after milking (Seykora and McDaniel, 1986). The area of the quadrilateral defined by the four spots was determined by connecting two spots with a diagonal line from which perpendicular lines were drawn to each of the remaining two spots. The sum of areas of the resulting four right triangles was then calculated. The absolute (cm2) and relative (%) decrease in udder floor area after milking relative to prior to milking was determined. It was assumed that the less edematous udder would have a greater reduction in size upon removal of milk from the mammary gland. In addition to udder floor area, assessment of udder edema was performed weekly based on digital impression on the udder skin from 3 weeks prepartum to 3 weeks postpartum. Edema was classified based on a

2.3. Bacteriological analyses of milk samples A composited aseptic fore sample of milk was collected from each cow in the prepartum-milking group at the first or second day of milking during the prepartum period. Two other aseptic fore samples of milk were collected from all cows, one during the first 60 h after calving and the second at day 28 postpartum. The prepartum samples were cultured in bovine blood agar and in brain and heart infusion medium (NMC, 1999) for determination of microbiological status at the Veterinary Medicine Teaching and Research Center, Milk Quality Laboratory in Tulare, CA, USA. The milk samples collected postpartum were analyzed for SCC and cultured as described previously. An aseptic fore sample of milk was also collected from every cow diagnosed with clinical mastitis prior to the first intramammary treatment, frozen, and then later cultured for bacterial determination.

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1– 4 scale: 1, classified as no edema when only a little depression after digital pressure on the side of the udder was observed and less than 2 s were required for the skin to return to normal; 2, classified as some edema when a depression remained for 2 – 5 s after digital pressure on the side of the udder; 3, classified as somewhat severe edema when a depression remained for more than 5 s after digital pressure on the side of the udder and little ventral edema; and 4, classified as severe edema when a noticeable depression on the side of the udder remained for more than 5 s after digital pressure in association with edema in the ventral portion of the abdomen. 2.5. Monitoring of early postpartum cows All cows were monitored daily during the first 3 weeks postpartum. Any cow displaying signs of illness was evaluated daily by the same person. Rectal temperature was taken and the presence of ketones was determined in the urine (KetostixR, Bayer Co., Pittsburgh, PA, USA). Cows with rectal temperature above 39.5 jC were considered as febrile and treated accordingly. Clinical ketosis was characterized by lack of appetite and presence of ketones in the urine using Ketostix. Diagnosis of left displacement of abomasum (LDA) was based upon clinical signs presented by the affected cow, which included reduced milk production, rumen atony, ketonuria, diarrhea, and presence of an acute ping sound at auscultation and percussion on the left side of the abdomen. All cows were rectally palpated by the same person at 23 days postpartum to determine the presence of uterine content, vaginal discharge, and involution of the uterus. Uterine involution was considered complete when the uterus had been repositioned in the pelvic canal with the two uterine horns being symmetric with similar size. 2.6. Blood sample collection and analyses Blood samples (10 ml) were collected from a subset of 44 randomly chosen blocks of cows biweekly during the prepartum period and at days 4 and 17 postpartum. For the prepartum period, samples collected at
11F1 and
4F1 days prior to each cow’s day of calving were analyzed.

Samples from 85 cows (42 controls and 43 prepartum-milking) were analyzed on days
11 and from all 88 cows on day
4 relative to each cow’s day of calving. During the prepartum period, blood was sampled between 9:00 and 10:00 h, approximately 1 h prior to the feeding time; postpartum, blood was sampled between 7:00 and 8:00 h, immediately after the morning milking and at the same time when animals were fed. Blood was sampled by puncture of the coccygeal vein or artery using heparinized VacukainerR tubes (Becton Dickinson, Franklin Lakes, NJ, USA). Samples were immediately placed on ice and arrived at the laboratory within 4 h of collection. Blood tubes were centrifuged at 1500 g for 15 min in a refrigerated centrifuge at 10 jC for plasma separation. Plasma was frozen at
25 jC and later analyzed for glucose by direct measurement using the YSI Model 2700 SELECT Biochemistry Analyzer (Yellow Springs Instrument Co., Yellow Springs, OH, USA). Measurement of plasma hOH-butyrate (BHBA) (Williamson et al., 1962) was performed by using a Sigma kit 310-A (Sigma Diagnostics, St. Louis, MO, USA). Plasma was also analyzed for its concentration of nonesterified fatty acids (NEFA) according to the method described by Johnson and Peters (1993) using a commercial kit (NEFA C, Wako Chemicals USA, Richmond, VA, USA). Subclinical ketosis was characterized based upon plasma BHBA equal to or greater than 15.0 mg/dl (Duffield, 2000). This threshold was chosen because it has been shown to affect lactation performance (Duffield, 2000).

3. Statistical analyses Lactation performance data, plasma metabolites, udder edema based on digital pressure of the skin, and BCS were analyzed by ANOVA for repeated measures by the MIXED procedure of SAS (Littell et al., 1998) with observed mean, block, treatment effect, period effect, the interaction between treatment and period effect, covariate effect, and cow nested within treatment as the random error. Period was defined as the day when the outcome variable being analyzed was measured. For the analyses of blood metabolites, day of blood sampling relative to the day

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of calving was used for covariate adjustment of data during statistical analyses. The initial udder edema score at the beginning of the study was used for covariate adjustment of the data during the analysis of udder edema. Body condition score changes, days postpartum when a disease process was diagnosed for those cows affected by the disease, and degree of udder edema were all analyzed by the GLM procedure of SAS (2001) with observed mean, block, treatment effect, covariate effect, and the residual error. The initial body condition score (BCS) was used as covariate for the analyses of BCS. Day postpartum when udder floor area was evaluated and the udder edema score based on digital pressure of the skin at the beginning of the study were used as a covariate for the analyses of udder floor area. The product limit method of the Kaplan –Meier model (Kaplan and Meier, 1958) for the survival analysis procedure of the MinitabR (MINITAB, 1996) program was utilized to assess the effect of treatment on days postpartum when a cow left the study either by culling or death. Cows that did not experience the event at the end of the study were censored at 135 days postpartum. Univariant differences in respective cumulative proportion between treatments were assessed using the logrank nonparametric method. Incidence of health disorders was analyzed by Chi-square using MINITAB (1996). Treatment differences with PV0:05 were considered significant and 0:05 < PV0:10 were considered a tendency.

4.1. Mammary gland health status Prepartum milking of primigravid cows resulted in decreased udder edema as indicated by a greater reduction in udder floor area immediately after milking (Table 2). Furthermore, udder edema as measured by digital pressure of the udder skin was also reduced during the pre- and postpartum periods by prepartum milking. These reductions indicate that prepartum milking has the potential to reduce udder edema in primigravid cows. Similar to our findings, preliminary data from Bowers et al. (2002b) also showed that prepartum milking of primigravid cows reduced udder edema scores through the first 5 weeks postpartum. Because these were primigravid cows, they had not been subjected to dry cow therapy with intramammary infusion of antibiotics. When milk samples were collected for microbiological analyses from cows milked prepartum, 81% of them had a positive bacterial isolate in milk on day 15 prior to calving. However, milking them prior to calving decreased the proportion of cows with bacterial isolation in milk compared with control cows immediately after calving (P < 0:01), but not at 28 days postpartum (P < 0:14). The predominant bacterial isolate throughout the study was coagulase-negative Staphylococcus sp. (Staph sp.). At day 15 prior to calving, Staph sp. Table 2 Effect of prepartum milking of primigravid cows on mammary gland health status Treatment Control

4. Results and discussion The average number of days in the prepartum treatments did not differ and they were 15.1 and 14.9 days for prepartum milking and controls, respectively (P < 0:87). The timing of the milking unit on the udder during the prepartum period was monitored twice weekly in 20 cows and it averaged 3.2 min. An increase in time with the milking unit on the udder was observed as the cows approached parturition, which coincided with a more copious milk flow. In the first 5 days of milking, the unit was on for an average of 2.7 min compared with 4.8 min during the last 3 days of gestation (P < 0:01).

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Udder floor area Reduction, cm2 Reduction, % Udder edema score, 1 – 4 Prepartum Postpartum Positive bacteriology, % Day 1 postpartum Day 28 postpartum SCC,a103/ml SCSb Mastitis incidence, % DIMc at first mastitis Mastitis cases per cow a

Milking

33.5 16.9

43.0 23.9

1.90 0.90

0.001 0.001

2.8 2.3

2.1 1.8

0.14 0.12

0.03 0.05

66.4 58.6 445.2 3.23 14.1 25.4 0.21

SCC=somatic cell count. SCS=somatic cell score. c DIM=days in milk. b

S.E.M. P <

50.0 49.2 197.2 2.39 6.1 70.9 0.04

– – 32.3 0.07 – 16.4 0.05

0.01 0.14 0.0001 0.0001 0.04 0.03 0.02

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represented 49.0% of the total positive isolates for cows milked prepartum. At calving, the predominant isolate was again Staph sp. representing 79.1 and 82.5% of all positive isolates for control and prepartum milking heifers, respectively. Similarly, the predominant bacterial isolate at day 28 postpartum in 78.7 and 74.1% of the control and prepartum milking heifers with positive bacterial cultures, respectively, was environmental Staph sp. In addition to reducing the degree of udder edema and the proportion of cows with positive bacterial isolate in milk, prepartum milking of primigravid cows decreased somatic cell linear score (SCS) throughout the experimental period (Fig. 1). Interestingly, cows with a greater degree of udder edema had also a higher SCS immediately after calving (P < 0:01), as well as throughout the 135-day experimental period (P < 0:02). After grouping cows into quartiles according to their degree of reduction in udder floor area immediately after milking (Q1V13:37%; Q2 ¼ 13:38
20:36%; Q3 ¼ 20:37
26:39%; and Q4z26:40%), those with greater reduction (less udder edema) had reduced SCS immediately after calving (P < 0:01) and throughout the 135-day experimental period (P < 0:02). In fact, primigravid cows milked prepartum had lower udder edema scores and lower milk electrical conductivity readings during the first weeks postpartum (Bowers et al., 2002b), which is indicative of less intramammary infections suggesting better udder health. Waage et al. (2001)

conducted a case-control study to evaluate risk factors for clinical mastitis in primigravid cows during the first 2 weeks of lactation. They observed that the presence of udder edema increased the risk for mastitis, and primigravid cows with udder edema at calving were 2.61 times more likely to develop mastitis early postpartum. The positive effects of prepartum milking on udder edema, SCC, and proportion of cows with positive bacterial isolate in milk was also accompanied by a lower incidence of clinical mastitis during the first 135 days postpartum. Milking primigravid cows prior to calving not only reduced the incidence of mastitis by less than half of that observed for control cows (P < 0:04 ), but it also extended the interval between calving and the diagnosis of the first postpartum clinical case (P < 0:03). The combination of a lower incidence of mastitis and a longer interval for the diagnosis of the first clinical case resulted in a lower mean number of clinical cases per cow when primigravid cows were milked prior to calving (P < 0:02). Reducing the proportion of cows affected by mastitis and extending the interval between parturition and the occurrence of the first clinical case is expected to minimize the economic impact of mastitis on dairy farms. Previously, Greene et al. (1988) conducted a field study to determine the effects of prepartum milking of dairy cows on postpartum performance and health. They observed that milking cows prepartum had no effect on SCC, but it reduced the incidence of new intramammary infections during the early postpartum period. Collectively, these results indicate that prepartum milking reduces udder edema, SCC, and incidence of mastitis in dairy cows. 4.2. Lactation performance

Fig. 1. Least square means of linear somatic cell count score (SCS) during the first 135 days in milk (DIM) for control (E) and prepartum milking cows (n). Pooled S.E.M.=0.07. Effect of treatment (P < 0:0001 ), period (P < 0:0001 ), and interaction between treatment and period (P < 0:02).

Yields of milk and 3.5% FCM during the first 135 days in lactation were positively affected by prepartum milking (Table 3). Primigravid cows that were milked prior to calving produced an additional 1.7 and 1.1 kg/day of milk (P < 0:001 ) and 3.5% FCM (P < 0:004 ), respectively, compared with control cows. The increase in milk yield for cows milked prepartum tended to be similar throughout the 135 days postpartum based on the observed tendency for interaction between treatment and period (P < 0:10;

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Table 3 Effect of prepartum milking of primigravid cows on lactation performance during the first 135 days postpartum

Control

Milking

P
34.9 35.9

36.6 37.0

0.27 0.28

3.73 1282

3.61 1308

2.86 994

2.85 1041

Treatment

Milk, kg/d 3.5% FCM,b kg/day Milk fat % g/day Milk true protein % g/d a b

TRT

Period

0.001 0.004

0.001 0.001

0.10 0.60

0.03 12

0.001 0.12

0.001 0.001

0.007 0.83

0.01 7.6

0.16 0.001

0.001 0.001

0.001 0.68

TRT  Period

TRT=Effect of treatment. FCM=fat-corrected milk.

Fig. 2), which indicates that the positive effects of prepartum milking on lactation performance were extended for the entire study period. Grummer et al. (2000) utilized 20 multiparous Holstein cows to determine the effects of prepartum milking during the last 10 days of gestation on milk production during the first 7 weeks postpartum. Although mean milk yields throughout the experimental period were greater for cows milked prepartum, the increase did not differ statistically. Similarly, Greene et al. (1988) observed no positive effect of twice daily milking during the last 2 weeks prepartum on postpartum yields of milk in primigravid and multiparous cows. When cows had one udder half milked twice daily starting 10 days prior to the expected calving date and the other udder half milked only postpartum, quarters milked prepartum were more developed as they contained more mature and total epithelium and less stroma than quarters not milked prepartum (Akers et al., 1977). Subsequently, the same group observed similar improvements in mammary development upon removal of milk prepartum (Akers and Heald, 1978). The authors indicated that prepartum removal of milk stimulate secretory cell development, and suggested that it could potentially increase subsequent milk production (Akers et al., 1977). It is possible that milking primigravid prepartum improved secretory cell development, which resulted in greater yields of milk during the first 135 days postpartum. Furthermore, primigravid cows milked prepartum had lower SCC and lower incidence of clinical mastitis, both known for causing decreases in yields of milk and milk components (Fetrow et al., 1988; Rajala-Schultz et al., 1999; Santos et al., 2003).

Concentration of fat in milk was higher for control than prepartum milking cows, but most of this effect was detected for the early postpartum period as indicated by the interaction between treatment and period (P < 0:007). The concentration of fat in milk during the first month postpartum was 4.23 and 3.87% for control and prepartum-milking cows, respectively. After that, milk fat content was similar between the two treatment groups and it averaged 3.60%. Although concentration of true protein in milk was similar between the two treatments (P < 0:16), yields of milk protein was higher for cows milked prepartum. Prepartum milking reduced SCC, the incidence of mastitis, and extended the interval from calving to first clinical mastitis by 45 days compared with control cows, which are expected to improve lactation

Fig. 2. Least square means of milk production (kg/days) during the first 135 days in milk (DIM) for control (E) and prepartum milking cows (n). Pooled S.E.M.=0.27. Effect of treatment (P < 0:001 ), period (P < 0:001), and interaction between treatment and period (P < 0:10).

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performance (Rajala-Schultz et al., 1999; Santos et al., 2003). 4.3. Plasma metabolites Concentration of plasma glucose prepartum tended to be reduced by prepartum milking (P < 0:10; Table 4). However, immediately prior to calving the concentration of plasma glucose was lower for prepartummilking cows compared with control cows as indicated by the interaction between treatment and period (P < 0:001). Plasma concentrations of glucose on day
4 prior to calving were 66.5 and 72.6 mg/day for prepartum-milking and control cows, respectively. Similar effects of prepartum milking were observed on plasma concentrations of BHBA and NEFA. Because of the greater energy needs in cows that were milked prepartum, plasma BHBA and NEFA were increased and most of the effect was observed immediately prior to calving as indicated by the interactions between treatment and period (P < 0:01). At day
4 prepartum, plasma BHBA concentrations were 8.15 and 11.5 mg/dl for control and prepartum-milking cows, respectively. At the same time, plasma NEFA concentrations were 351 and 1035 AEq/l for control and prepartum-milking cows, respectively. Grummer et al. (2000) observed a sharp decrease in plasma glucose concentrations immediately prior to calving when multiparous cows were milked prior to calving. When primigravid cows were initially milked prepartum, milk production was negligible and the milking unit stayed on the cow, in many instances, only for the minimum 120-s delay time to detach because of

the lack of milk flow. However, as parturition approached, milk production became more copious, which probably increased the energy requirements of the cow. Bowers et al. (2002b) observed a steady increase in milk production as primigravid cows milked prepartum approached parturition. Unfortunately, milk production could not be measured during the prepartum period in the current study. The effect of increasing energy needs as parturition approaches can be evidenced by the changes in BCS during the prepartum period (Fig. 3). Cows in both treatment groups had similar BCS at the beginning of the study (BCS ¼ 4:16 ), but a greater decrease in body condition between the beginning of the study and calving was observed for those primigravid cows milked prepartum, as evidenced by the tendency for interaction between treatment and period on BCS. Collectively these results indicated that milking primigravid cows prepartum resulted in greater energy needs immediately prior to calving, which were compensated for by the greater mobilization of body reserves. Using plasma BHBA equal to or greater than 15.0 mg/dl as an indicator of subclinical ketosis (Duffield, 2000), it becomes clear that primigravid cows milked prepartum were more likely to develop subclinical ketosis immediately before and after calving than control cows (Fig. 4). These results indicate that the period immediately around calving becomes critical and the energy requirements for milk synthesis during the prepartum period need to be met by a diet more energy dense or by strategies that supply gluconeogenic precursors to minimize ketosis. The diet offered

Table 4 Effect of prepartum milking of primigravid cows on concentrations of plasma metabolites pre- and postpartum Treatment

Prepartum Glucose, mg/dl h-OH-butyrate, mg/day NEFA,b AEq/l Postpartum Glucose, mg/dl h-OH-butyrate, mg/day NEFA, AEq/l a b

P
TRT

Week

TRTWeek

Control

Milking

72.1 7.71 363.5

70.0 9.36 846.4

0.88 0.49 43.0

0.10 0.02 0.001

0.18 0.001 0.05

0.001 0.01 0.001

67.0 14.6 683.2

63.8 17.8 644.9

2.54 1.66 38.6

0.37 0.17 0.48

0.44 0.001 0.79

0.21 0.01 0.25

TRT=effect of treatment; TRTWeek=interaction between TRT and week. NEFA=nonesterified fatty acids.

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Fig. 3. Least square means of body condition score (BCS) during the first 130 days in milk (DIM) in primigravid dairy cows subjected or not to prepartum milking. Control cows: dashed line with squares (—n—); prepartum milking cows: solid line with triangles (—E—). Pooled S.E.M.=0.02. Effects: treatment (P < 0:01); period (P < 0:001); and interaction between treatment and period (P < 0:12).

to cows during the prepartum period was already high in energy content with a substantial amount of nonfibrous carbohydrates, especially starch, from corn silage and steam-flaked corn. It would be difficult to

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increment the energy density of the ration by adding additional fermentable carbohydrates without compromising rumen health and risk for digestive disorders and displacement of abomasum. Additional strategies to minimize the energy deficit and improve the metabolic status of cows milked prepartum warrants further investigation and ionophores (Duffield, 2000) and gluconeogenic precursors such as propylene glycol might be beneficial. Interestingly, no primigravid cow had plasma BHBA equal to or greater than 15.0 mg/dl at day
11 relative to the day of calving, but immediately after calving 32.8 and 62.8% of the control and prepartum-milking cows developed subclinical ketosis, respectively. At 17 days postpartum, the incidence was similar between the two treatment groups and the numbers had decreased to 19.5%. Using the same threshold of plasma BHBA concentration as an indicator of subclinical ketosis, Duffield (2000) observed wide variations in the incidence of this metabolic disturbance in different dairy herds in Canada. When 507 primigravid and multiparous cows that had not

Fig. 4. Incidence of subclinical ketosis as determined by plasma h-OH-butyrate concentration equal to or greater than 15.0 mg/dl (Duffield, 2000) in primigravid dairy cows subjected or not to prepartum milking. Control cows: black solid bars; milking cows: white bars with vertical dashing. Effect of treatment (*, P < 0:01) on days
4 and 4 relative to calving.

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received the ionophore Monensin in a large study involving 25 dairy herds were considered, the cumulative incidence of subclinical ketosis over the first 9 weeks postpartum was 43.0%. Similar to our findings, they observed that the peak incidence occurred in the first week postpartum, but only 28% of the cows were affected. Nevertheless, cows with plasma BHBA concentration equal to or greater than 15.0 mg/dl produced less milk than herdmates without subclinical ketosis (Duffield, 2000). Therefore, if prepartum milking of primigravid cows is to be implemented, strategies to minimize the incidence of subclinical ketosis also need to be considered. During the postpartum period, treatment had no effect on plasma concentrations of glucose, BHBA, and NEFA. However, an interaction between treatment and period was observed for plasma BHBA (P < 0:01), which indicates that plasma ketone concentrations were higher for prepartum milking cows immediately after calving. In fact, plasma BHBA concentrations on day 4 postpartum were 23.5 and 15.7 mg/dl for prepartum-milking and control cows, respectively.

Table 5 Effect of prepartum milking of primigravid cows on incidence of health disorders Treatment

Postpartum fever Incidence, % DIMa up to diagnosis Ketosisb Incidence, % DIM up to diagnosis LDAc Incidence, % DIM up to diagnosis Lameness Incidence, % DIM up to diagnosis Culling Incidence, % DIM when sold Mortality Incidence, % DIM when dead

P<

Control

Milking

37.5 5.6 (F0.9)

39.1 4.7 (F0.9)

0.79 0.56

10.2 4.4 (F5.2)

17.4 11.4 (F5.2)

0.10 0.61

3.9 15.8 (F2.1)

3.5 7.5 (F2.1)

0.86 0.03

3.9 82.8 (F15.1)

7.0 53.8 (F15.1)

0.29 0.26

10.1 38.4 (F8.14)

10.9 41.8 (F8.14)

0.82 0.77

3.6 21.0 (F8.78)

3.1 13.5 (F9.19)

0.83 0.59

a

DIM=days in milk. Determined by the presence of ketonuria (KetostixR, Bayer Co., Pittsburgh, USA). c LDA=left displacement of abomasum. b

4.4. Incidence of health disorders Only two primigravid cows developed retained fetal membranes during the study. Generally, incidence of diseases and days postpartum when a disease was first diagnosed did not differ between the two treatment groups (Table 5). Approximately 38.3% of the primigravid cows developed postpartum fever and had to be treated accordingly. The day of diagnosis of the first fever was similar between the two treatment groups (P < 0:56) and it averaged at approximately 5 days postpartum. Similar to subclinical ketosis, the incidence of clinical ketosis tended to be higher for cows milked prepartum suggesting that these animals mobilized more body reserves to support lactation as indicated by the higher plasma BHBA and NEFA around parturition. Incidence of LDA was similar between the two treatment groups, but cows milked prepartum developed LDA sooner in lactation than control cows (P < 0:03). Because ketosis is a risk factor for LDA Geishauser et al., 2000, it is possible that prepartum milking of primigravid cows, which resulted in more subclinical and clinical ketosis around parturition,

might have predisposed them to develop LDA sooner after calving. Nevertheless, prepartum milking did not increase the number of cows affected by LDA. The proportion of cows leaving the study prematurely was 13.9% for both groups (P < 0:93 ). This may be reflective of the similar incidence of periparturient disorders. Of the 13.9% of the cows that left the study prematurely, approximately 10.5 and 3.4% left because they were sold and died during the first 135 days postpartum, respectively (Table 5). The average number of days in lactation when the affected cows were either sold or died was similar between the two treatments. In fact, when survival analyses examined the number of days in lactation when a cow left the study with censoring at 135 days in lactation, treatment had no effect on the proportion of animals remaining in the study (P < 0:92), which reinforces the observation that prepartum milking had no effect on survivability of cows. Contrasting our results, Greene et al. (1988) indicated that cows milked prepartum were less likely to be culled for nondairy reasons compared with control cows. They suggested that the major effect of prepartum milking on culling

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was due to the lower incidences of mastitis and milk fever in prepartum milking cows. Since primigravid cows rarely develop milk fever, prepartum milking of primigravid cows should not reduce culling because of a possible benefit in calcium metabolism. When cows were palpated at approximately 23 days postpartum, the proportion of animals that had complete uterine involution (78.3 vs. 85.1; P < 0:16 ), presented vaginal discharge (36.5 vs. 35.5%; P < 0:87) or had palpable fluid in the uterus (28.8 vs. 26.5%; P < 0:68) did not differ between control and prepartum milked cows. When primigravid Holstein and Jersey primigravid cows were milked twice daily during the last 3 weeks prepartum, postpartum uterine involution as measured by uterine tone and position of the uterus in the pelvic canal throughout the first weeks after calving did not differ between milking and control cows (Bowers et al., 2002a). These data indicate that milking primigravid cows during the last 15 days of gestation did not affect uterine involution.

5. Conclusions Prepartum milking of primigravid cows reduced the degree of udder edema as indicated by the greater reduction in udder floor area immediately after milking and by the decreased udder edema score based on digital pressure pre- and postpartum. The positive effects of prepartum milking were extended to improved udder health with a marked reduction in somatic cell counts and incidence of clinical mastitis, resulting in improved lactation performance during the first 135 days postpartum. Milking prepartum primigravid cows while maintaining them in the same plane of nutrition of control cows resulted in negative effects on their energy status at calving as measured by plasma concentrations of glucose, h-OH-butyrate, and nonesterified fatty acids, which resulted in a tendency to increase clinical ketosis. Therefore, strategies that minimize the incidence of ketosis such as ionophores and gluconeogenic precursors might be indicated during the prepartum period when primigravid cows are milked prior to calving. In conclusion, prepartum milking of primigravid cows has the potential to reduce udder edema, which improves udder health and lactation performance.

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Acknowledgements The authors thank Jack DeJong and the staff of River Ranch Dairy. Our thanks are extended to Michael Ballou for helping with data collection, and to Kathy Glen and Lisa Ruiz of the Milk Quality Laboratory at the VMTRC for microbiological culture of milk samples.

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