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Department of Dairy Science, University of Wisconsin, Madison 53706
Corresponding author: Milo C. Wiltbank; e-mail: wiltbank{at}calshp.cals.wisc.edu.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Key Words: reproduction • first postpartum ovulation • dry period • nutrition
Abbreviation key: CL = corpus luteum, DP = dry period, EB = energy balance, HE = high energy, LE = low energy, ME = moderate energy, N = no planned DP, S = shortened 28-d DP, T = traditional 56-d DP management scheme.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Most of the literature indicates that a dry period (DP) of 40 to 60 d is needed to achieve maximum milk yield during the following lactation (Coppock et al., 1974; Sorensen and Enevoldsen, 1991; reviewed by Bachman and Schairer, 2003). Other research indicates that a DP of 30 d is sufficient to maintain milk (Lotan and Adler, 1976; Bachman, 2002; Gulay et al., 2003). Nevertheless, a shortened DP seemed to reduce milk production in primiparous, but not multiparous, cows in a recent study (Annen et al., 2004) and our recent study found somewhat of a reduction in milk production per day, but not in FCM production (Rastani et al., 2005). Information relating the effects of DP to subsequent reproductive performance of lactating cows is sparse. Lotan and Adler (1976) reported that days open, number of inseminations, and pregnancy rates for 18 pairs of dairy cows having DP of 30 and 60 d were numerically similar.
Remond et al. (1997) reported that BW of cows with no planned DP increased 24 kg in the first 60 DIM, whereas BW of cows with a 60-d DP lost 28 kg during same time period. We speculated that cows with a DP of 56 d would be in more negative EB than cows with no planned DP due to reduced milk production in cows with no planned DP. Thus, cows with no planned DP were expected to ovulate earlier than cows with a 56-d DP; whereas cows with a 28-d DP were expected to be intermediate in days to first ovulation based on an expected intermediate level of negative EB.
The objective of our study was to determine the effects of reducing duration of DP and simplifying feeding of transition cows on interval to first postpartum ovulation and other reproductive measures of periparturient dairy cows. It should be clearly noted that the small number of cows in this intensive study did not allow definitive evaluation of binomial reproductive measures (e.g., conception rate), but data were collected to provide a rationale for future large studies related to the effect of DP on reproductive performance.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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). If a cow on N dropped below 2 kg/d, milking was discontinued for the remainder of the prepartum period. All cows were fed a postpartum HE diet (NEL = 1.71 Mcal/kg) from parturition through 70 DIM. The only difference between the prepartum HE diet and the postpartum HE diet was the addition of sodium bicarbonate and a reduction in level of vitamins in the postpartum HE diet. The experimental timeline is summarized in Figure 1. Cows were fed a TMR for ad libitum intake throughout the entire experimental period. Ingredient and nutrient composition of the diets, selection criteria for the cows, and energy calculations were reported previously (Rastani et al., 2005).
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Blood Sampling
Blood samples for progesterone, estradiol, and FSH analyses were collected from the coccygeal vein or artery into Vacutainer tubes (Becton Dickinson Co., Franklin Lakes, NJ) at 76, 30, 21, 14, and 7 d before expected calving date, 1 d after calving, and beginning on d 6 or 7 postpartum, 3 times weekly (i.e., Monday, Wednesday, and Friday) until 7 d after second ovulation or until 70 d postpartum. Blood was allowed to clot at 4°C for 24 h and centrifuged at 1500 x g for 15 min. Serum was collected and stored at –20°C until further analysis.
Hormone Assays
Serum concentration of FSH was determined using a radioimmunoassay validated for use in cattle (Bolt and Rollins, 1983; Bolt et al., 1990). The FSH assay incorporated bFSH (USDA-bFSH-I-2) for iodination and reference standards and NIDDK-anti-o-FSH-I-2 as the primary antiserum. Hormone sensitivity, calculated as 2 standard deviations less than the mean cpm at maximum binding, was 0.08 ng/mL. Coefficients of variation for within and between assays for FSH were 3.2, 3.8% (cows in diestrus) and 6.8, 8.7% (cows near estrus), respectively.
Serum concentration of progesterone was determined by solid-phase radioimmunoassay kits containing antibody-coated tubes and 125I-labeled progesterone (Coat-A-Count, Diagnostic Products Corp., Los Angeles, CA) as previously described by Gümen and Wiltbank (2005). Hormone sensitivity, calculated as 2 standard deviations less than the mean cpm at maximum binding, was 0.03 ng/mL (mean of 10 assays). Coefficients of variation for within and between the assays for progesterone were 5.4 and 7.4%, respectively, using a quality control sample with 2.0 ng/mL, and 5.3 and 5.6%, respectively, using a quality control sample with 10 ng/mL of progesterone.
Prepartum and d 1 postpartum serum concentration of estradiol were determined by a competitive ELISA as described previously (Rasmussen et al., 1996). A quality control sample was prepared from charcoal-stripped serum containing a known concentration of estradiol (250 pg/mL). The quality control sample was evaluated multiple times in each estradiol assay and the within- and between-assay coefficients of variation were 3.2 and 8.6%, respectively.
Serum concentrations of estradiol were measured in samples collected between d 6 and 14 postpartum by using modifications to a commercially available estradiol radioimmunoassay kit (Third Generation Estradiol Assay Kit, Diagnostics Systems Laboratories Inc., Webster, TX) previously validated for use in cattle (Kulick et al., 1999). The quality control sample (5 pg/mL) was evaluated multiple times in each estradiol assay and the within- and between-assay coefficients of variation were 4.8 and 6.2%, respectively.
Postpartum Ultrasound Evaluation and Reproductive Management
Ovarian ultrasonography examinations were performed using a real-time, B-mode scanner equipped with a 7.5-MHz linear-array intrarectal transducer (Aloka 500V, Corometrics Medical Systems Inc., Wallingford, CT). Measurements were made on a single frozen image of the apparent maximal area of each follicle, using the average diameter in 2 directions at right angles. Transrectal ultrasound scanning to monitor follicles was performed thrice weekly (i.e., Monday, Wednesday, and Friday) beginning on d 6 or 7 postpartum until 7 d after second ovulation or until 70 d postpartum in anovulatory cows. Ovulation was determined by ultrasound scanning based on disappearance of a large follicle followed by appearance of a resulting corpus luteum (CL) and confirmed by an increase in serum progesterone concentration.
A persistent CL was defined as a luteal structure that remained detectable in the ovary for >30 d and maintained serum progesterone concentrations >1 ng/mL (Bulman and Lamming, 1977). A short luteal phase was defined as an interval between first and second postpartum ovulation of <12 d. Anovulation was defined as no ovulation for the entire 70-d postpartum period.
Pregnancy status was determined using ultrasound at 25 to 31 and 60 to 66 d after AI. Visualization of a fluid-filled uterine horn with embryonic vesicles and a large CL (d 25 to 31) or the presence of a fetus (d 60 to 66) were used as positive indications of pregnancy. All fertility data described in the text were based on the later pregnancy diagnosis; the earlier pregnancy diagnosis was only used to determine rate of embryonic loss. First-service conception rate was calculated as the number of cows diagnosed pregnant divided by the number of cows previously inseminated. Overall conception rate was calculated as the number of cows diagnosed pregnant divided by total number of inseminations for all cows per treatment. Herd personnel were responsible for reproductive management including detection of estrus and AI. The voluntary waiting period was 50 d. For first service, cows that were detected in estrus (7 of 20 in N, 8 of 23 in S, and 3 of 20 in T cows) were inseminated by herd personnel. In the remaining cows, ovulation was synchronized by using the Ovsynch protocol (GnRH –7d – PGF2
– 56 h – GnRH – 16 to 18 h – timed AI) in which AI occurred at 70 to 76 DIM. Cows that were diagnosed not pregnant between 25 and 31 d after AI were retreated with the Ovsynch protocol for AI (98 of 117 second or later breedings). Cows that were detected in estrus were inseminated by herd personnel based on the a.m.-p.m. rule (19 of 117 second or later breedings). Fertility data was collected until 250 DIM.
Statistical Analyses
Analyses of hormonal data were conducted using the mixed models procedure of SAS with repeated measures in time as a subplot (SAS Inst. Inc., Cary, NC). The model was:
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where Yijkl = dependent observations (serum progesterone, estradiol, and FSH); µ = overall mean; trti = effect of treatments [i = N, S, T (fixed effect)]; cowj = cows [j = 1, 2, 3,......20 (random effect)]; timek = effect of time [k = days (fixed effect)]; trti x timek = interaction of treatments and time (fixed effect); and 
ijkl = random error. To account for auto-correlated errors due to repeated measures and unequal time intervals for the same experimental unit cowj(trti), the spatial power structure was used (Littell et al., 1998). Prepartum and postpartum periods were analyzed separately.
Single mean comparisons, including days to first ultrasonography, days to first ovulation, days to 10-mm follicle size, days to first AI, and days open in pregnant cows were analyzed using the mixed models procedure. The model was:
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whereYijkl = dependent observations (mean comparisons); µ= overall mean; Bi = effect of blocks [i = 1, 2, 3, ......23 (random effect)]; Pj = effect of parity [j = primiparous or multiparous (fixed effect)]; trtk = effect of treatments [k = N, S, T (fixed effect)]; Pj x trtk = interaction of parity and treatments (fixed effect); and ijkl = random error.
When treatment was significant in the model, differences between treatments were determined using the PDIFF option (SAS Inst. Inc.). Significance was declared when P < 0.05, and trends were discussed when P < 0.15. Services per conception were analyzed by the nonparametric Kruskal-Wallis test (SAS Inst. Inc.). One-way ANOVA was used to compare EB, milk production, BCS (average value for the 3 evaluators), and BW among treatments (N, S, and T). Outliers were determined by the Univariate procedure (SAS Inst. Inc.). Cows were considered outliers when data were outside of 1.5 interquartile ranges. Correlation coefficients were calculated using PROC CORR (SAS Inst. Inc.). Binomial response data were analyzed by Fisher’s Exact test, using all possible 2 x 2 comparisons from the 3 x 2 table.
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RESULTS AND DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Regardless of treatments, prepartum serum progesterone and FSH concentration decreased (P < 0.001) as calving approached (Figure 2). Serum estradiol concentration increased (P < 0.001) in all cows as calving approached regardless of treatment (Figure 2). Serum estradiol concentration was not different among treatments until 14 d before expected day of calving (Figure 2). At 14 and 7 d before expected day of calving serum estradiol was greater (P < 0.05) in T than N cows, with S cows being intermediate (Figure 2). To our knowledge, no previous studies have evaluated the changes in prepartum hormonal concentrations during manipulation of DP. Nevertheless, hormonal concentrations during a traditional DP are similar to a previous report (Rasmussen et al., 1996). Before analysis of these samples, we hypothesized that circulating estradiol and progesterone would be decreased in cows with shortened DP due to the greater feed consumption and milk production in these cows. This hypothesis was based on a previous study (Sangsritavong et al., 2002) in which elevated DMI increased metabolism of steroids in lactating cows. Although circulating progesterone was not altered, the decrease in circulating estradiol was consistent with this hypothesis and could be due to the greater DMI in N than T cows (Rastani et al., 2005). The physiological implications of reduced circulating estradiol concentrations during the final prepartum days are intriguing. Circulating estradiol dramatically increases as parturition approaches and this increase may be important for changes in the reproductive tract that are important for normal parturition. Despite the reduced concentrations of estradiol, no problems with parturition were detected in the N cows (Rastani et al., 2005). In addition, increased circulating estradiol near parturition may be important for changes in the mammary gland that are essential for maximal milk production after parturition. Milk production was less in the N cows compared with S and T cows (Rastani et al., 2005). Based on our results, we propose that a reduced prepartum circulating estradiol should be included among the numerous possible explanations for reduced milk production in cows with no DP or shortened DP.
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). It seems likely that the postpartum FSH surge was earlier in N cows (based on follicle data described below) and therefore, the lack of blood samples between d 1 and 6 might have not allowed detection of the peak of the FSH surge in this treatment.
Average days from calving to first ultrasonography were similar among groups (between 6.3 and 6.6 d postpartum; Table 1). Average diameter of follicles at first ultrasonography was greater (P < 0.05) in N than T cows, with S cows being intermediate. Average days from calving until first detection of a 10-mm follicle were less (P < 0.05) in N and S than T cows. Beam and Butler (1997) reported that average days from calving until the first 10-mm follicle ranged from 8.5 ± 0.6 to 10.5 ± 0.5 d in cows with varying EB (–2.8 ± –6.7 Mcal/d). In another report, postpartum interval to detection of the first dominant follicle was 11.6 ± 8.9 d (Savio et al., 1990). In our experiment, follicles of cows in N reached 10 mm in diameter 2.5 d earlier than in T cows. In addition, although days to first ultrasonography were not different among treatment, follicular diameter was greater in N (9.5 ± 0.7 mm) than T (6.3 ± 0.6 mm) cows at first ultrasonography. Larger follicular diameter in N at 7 d postpartum supports the idea that emergence of the first postpartum follicular wave occurred earlier in N than in T cows.
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). One cow each from S and T did not ovulate during the experimental period (70 d postpartum). Day of ovulation for these 2 cows was assigned to be 70 d. Even without these cows, the range for ovulation was more variable in S (9 to 51 d) and T (9 to 63 d) than N (7 to 27 d) cows (Figure 3). The results for the T and S cows were similar to those in previous studies in which cows had a traditional DP. Savio et al. (1990) reported that days from calving to first postpartum ovulation were 27.4 ± 5.3 d (range 9 to 85 d) including the cows that developed cysts. Based on plasma progesterone, the interval from calving to first postpartum ovulation was 24.1 ± 1.5 d without including 4 anovulatory cows (n = 17; Zurek et al., 1995) and 24.4 ± 2.3 d (n = 11; Spicer et al., 1990). In a recent study, Sakaguchi et al. (2004) reported that days to first ovulation were 30.9 ± 2.4 d in 50 high milk-producing dairy cows based on thrice-weekly ultrasound evaluations. Thus, N cows ovulated earlier than cows in the other 2 treatments and apparently earlier than cows in previously reported research studies.
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). The other 2 cows in N ovulated a follicle from the second follicular wave. However, incidence of ovulation was distributed between first, second, and third follicular wave in S (62, 28, and 10%, respectively) and T (42, 21, and 37%, respectively) cows (Table 2). Savio et al. (1990) reported that most cows (74%) ovulated the first dominant follicle. However, Beam and Butler (1999) found that 46% of cows ovulated the first dominant follicle postpartum, whereas 31% developed at least 2 waves of dominant follicles before the first ovulation. Sakaguchi et al. (2004) reported first postpartum ovulations of 46% from first wave, 22% from second waves, and 12% from third or fourth waves. These ovulation results are similar to T cows in the present study.
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shows EB differences among treatments during the first few weeks after parturition. Cows with no planned DP had, on average, a 1.7 ± 1.2 Mcal/d positive EB during the first 3 wk postpartum in which 12 of 18 cows were in positive EB during the early postpartum period (Figure 4). Positive EB seemed to be primarily due to greater DMI, and consequently, a greater net energy intake during this period in N cows, combined with somewhat less energy output in milk production (Rastani et al., 2005).
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shows the association between mean EB during the first 21 d after calving and days to first ovulation for each individual cow in the 3 treatments. Although the correlation is significant (r = –0.42; P < 0.01), it would not be possible to accurately predict the time to first ovulation for an individual cow based on the mean EB during the first 21 d. Interval to first ovulation after calving has been reported to increase with increasing negative EB in some studies (Butler et al., 1981; Ducker et al., 1985; Butler and Smith, 1989; Lucy et al., 1991; Senatore et al., 1996; Beam and Butler, 1998), but not in others (Villa-Godoy et al., 1988; Spicer et al., 1990; Lucy et al., 1992). Similarly, we found that the EB nadir was inversely correlated with days to first ovulation (r = –0.45; P < 0.001). In contrast, unlike other studies (Canfield and Butler, 1990; Canfield et al., 1990; Beam and Butler, 1997; Beam and Butler, 1998; Senatore et al., 1996), days from calving to negative EB nadir was not related to days to first ovulation in our study, with N having the longest time to EB nadir (Table 3). This discrepancy between studies is probably due to the irrelevant nature of this value in cows that experience almost no negative EB such as N cows in our study. Loss in BW also was not significantly correlated to days to first ovulation, as reported in previous reports (Stevenson and Britt, 1979; Butler et al., 1981; Villa-Godoy et al., 1988; Lucy et al., 1992), but not by Senatore et al. (1996). Similarly, using all cows from the 3 treatments, no significant association was detected between BCS loss and days to first ovulation, which is in contrast to a previous report that used only a traditional DP (Beam and Butler, 1999). Thus, it seems very likely that the very consistent early ovulation in cows with no planned DP was due to the maintenance of a positive EB during the postpartum period in these cows.
Double Ovulation Rate
Incidence of double ovulation at first postpartum ovulation was greater (P < 0.05) in T (61%) than N (17%) cows, with S (35%) cows being intermediate. No difference in double ovulation rate, however, occurred at second ovulation (13/56; Table 2). First follicular wave double ovulation rate was greater (P < 0.01) in T (6/8; 75%) than N (3/16; 19%) cows, with S (5/13; 39%) cows being intermediate. Two of 6 cows in S and 1 of 4 cows in T ovulated 2 follicles originating from the second follicular wave and 4 of 7 cows in T ovulated 2 follicles originating from the third follicular wave. In our study, average milk yield during the first 70 DIM was greater in T (42.4 kg/d) than N (33.9 kg/d) cows (Rastani et al., 2005). In addition, the later DIM at first ovulation led to an even greater discrepancy in milk production at the time of first ovulation (43.1 ± 0.9 kg/d for T vs. 28.8 ± 1.9 kg/d for N) between T and N treatments. In previous studies, the incidence of double ovulation was nearly 3-fold greater for cows with high (50.7 ± 0.7 kg; 20.2%) vs. low (31.1 ± 0.7 kg; 6.9%) milk production (Fricke and Wiltbank, 1999; Lopez et al., 2005), although this milk production effect was not detectable at first postpartum ovulation (Lopez et al., 2005). Therefore, greater double ovulation in T cows could be due to greater postpartum milk production than in N cows or other factors such as later DIM at first ovulation.
Luteal Phase Length and Progesterone Concentrations
Prolonged luteal phase, short luteal phase, and anovulation have been reported to be important ovarian dysfunctions (Royal et al., 2000). Number of cows (27%; 15/56) with persistent CL (>30 d based on criteria of Bulman and Lamming, 1977) was not different among treatments. In contrast to the present study, a low incidence (1.5 to 12.5%) of persistent CL was reported after the first postpartum ovulation in previous studies (Bulman and Lamming, 1977; Bulman and Wood, 1980; Senatore et al., 1996; Lamming and Darwash, 1998). Short luteal phases were greater (P < 0.05) in N (28%; 5/18) than S (0%; 0/20) with T (11%; 2/18) cows being intermediate. In previous studies, variable rates (11 to 54%) of short luteal phases were reported after the first postpartum ovulation in lactating dairy cows (Savio et al., 1990; Senatore et al., 1996; Royal et al., 2000). Only 2 cows (1 cow from S and 1 from T) were anovulatory during the 70-d experimental period. Unlike previous studies, the incidence of anovulation was very low in our study (3%; 2 of 58 cows). Previously, we used weekly ultrasound evaluations combined with circulating progesterone concentration to analyze and classify anovulation at the start of the breeding period in a commercial dairy herd and found that 20% of cows were anovulatory (Gümen et al., 2003).
Serum progesterone concentrations were similar among treatments after calving (Figure 2). Progesterone concentration was low (<0.6 ng/mL) in all cows from d 6 to 13 (Figure 2). Postpartum serum estradiol concentration increased (P < 0.001) in all cows from d 6 to 13 (Figure 2), but no differences were detected among treatments.
Other Reproductive Data
Our study was not designed to evaluate fertility data, and the number of cows in each treatment was limited. Reproductive performance results, however, were interesting and may stimulate further studies. Although our experiment ended at 70 d postpartum, fertility data of cows were monitored until 250 d after calving. The first 5 cows in the study were not evaluated in terms of first postpartum ovulation. However, these 5 cows (2 in N, 2 in S, and 1 in T) were evaluated for a total of 63 cows. Days to first AI were less (P < 0.06) in N (69 d) and S (68 d) than T (75 d) cows (Table 4). First-service conception rate was greater (P < 0.05) in N (55%) than T (20%), with S (30%) cows being intermediate (Table 4). Overall conception rate, however, was similar (26 to 31%) among treatments (Table 4). Embryonic loss was limited to only 3 pregnancies lost between d 25 to 31 and d 60 to 66 (2 cows in S and 1 cow in T). In a recent study, cows with shortened or no planned DP had similar conception rates, but an insufficient number of cows were studied to make valid conception rate comparisons (Annen et al., 2004). Services per conception in pregnant cows were less (P < 0.05) in N (1.75) than T (3.0), with S (2.44) cows being intermediate (Table 4). Days open in pregnant cows were less (P < 0.05) in N than T, with S cows being intermediate (Table 4). These reproductive improvements in N cows could be due to differences in EB or milk yield. Cows with no planned DP had greater EB and produced less milk than cows in the other 2 treatments during the 70-d experimental period (Rastani et al., 2005). Nevertheless, it seems that conception rate after the first AI may have been reduced (P = 0.055) for N cows (5 pregnancies in 15 breedings) compared with T cows (14 pregnancies in 39 breedings). Future studies should not neglect a careful analysis of this potential reduction in conception rate in second and later AI due to reduction in DP.
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Practical Implications
Poor reproductive performance in lactating dairy cows is a substantial concern for commercial dairy producers. Results of our study demonstrated that eliminating the dry period resulted in a consistent and shorter postpartum interval to first ovulation and possibly improved reproductive performance. These changes may have been due to the maintenance of a positive energy balance during the early postpartum period when cows did not have a planned dry period. Further studies are warranted to evaluate if these encouraging results can be repeated in studies having sufficient numbers of cows to provide sufficient power to test potential differences in conception rate. Reducing the DP to 28 d while maintaining a high-energy diet seemed to cause some of the same effects, although less dramatically, when compared with a traditional dry period protocol. Our results emphasize the pressing need for further research to produce a dry period protocol that optimizes milk production, reproduction, and health for high-producing dairy herds.
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ACKNOWLEDGEMENTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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Received for publication December 10, 2004. Accepted for publication February 15, 2005.
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTS AND DISCUSSIONACKNOWLEDGEMENTSREFERENCES |
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), S (
), and N (•). Average days from calving to first ovulation also are shown for each treatment (mean ± SEM).