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Influence of negative energy balance and body condition on luteal function and estrous behavior in dairy cattle /

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Influence of negative energy balance and body condition on luteal function and estrous behavior in dairy cattle /
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  Association Between Energy Balance and Luteal Function in Lactating Dairy Cows A. VILLA-GODOY, 2 T. L. HUGHES, l R. S. EMERY, 1 L.T. CHAPIN, 1 and R. L. FOGWELL 1 3 Michigan State University East Lansing 48824 ABSTRACT Our objective was to determine the relationship between energy balance and secretion of progesterone in lactating dairy cows. Eight primiparous and 24 muhiparous lactating Holstein cows were studied from parturition to 100 d post- partum or conception. Cows calved normally and remained healthy through- out the study. All cows were fed ad libitum a total mixed diet formulated to satisfy requirements for maintenance and lactation. Intake of feed and production of milk per cow were measured twice daily. Body weight was determined weekly. Daily energy balance was de- termined by subtracting energy required for maintenance and lactation from intake of energy. Concentrations of progesterone were determined in milk sampled every 3rd d. For at least 4 successive d postpartum, 81 of cows were in negative energy balance. Varia- tion in energy balance was explained largely by intake of energy. Duration of luteal phases was not associated with energy balance. Energy balance within 9 d postpartum was correlated positively with concentration of progesterone with- in second and third postpartum luteal phase. Postpartum interval to nadir and magnitude of nadir of energy balance interacted to reduce progesterone within second and third postpartum estrous cycles. Thus, in lactating cows, secretion of progesterone is reduced by spon- Received August 27, 1987. Accepted November 16, 1987. 1Animal Reproduction Labolatory, Department of Animal Science, Michigan Agricultural Experi- ment Station Journal Article Number 12395. National Institution for Forestry, Crop and Livestock Research. Department of Physiology. Apdo. Postal 29-A; Queretaro, Qro 76020, Mexico. 3 Requests for reprints. taneous caloric deficit and is modulated by timing and magnitude of maximal caloric deficit. Spontaneous caloric de- ficit is a potential source of infertility in lactating dairy cows. INTRODUCTION Yield of milk and amounts of dietary energy have been implicated as causes of infertility in lactating dairy cows. Effects of milk yield on fertility of cows are equivocal. Some researchers observed that reproductive efficiency declines as yield of milk increases (3, 22, 29), but other workers did not confirm this association (7, 12, 16). Similarly, effects of low dietary energy on reproductive performance are in- consistent. Ducker et al. (8) and King (20) observed that low dietary energy was detri- mental to fertility of dairy cows. In contrast, other workers did not find a relationship between diet and reproductive performance (5, 9, 13). Energy balance (EB) is the net result of associations among yield of milk, diet, intake, and use of nutrients by cows. Thus, EB should integrate homeorhetic changes that occur during lactation (2). At least 92 of dairy cows experience negative EB (NEB) during early lactation (6, 26), but magnitude and duration of NEB are variable among cows (4). In dairy cattle, luteal function is associated with three events that determine fertility: 1) detection of estrus (21), 2) conception (11, 12), and 3) embryonic survival (17). Therefore, identification of factors that affect luteal func- tion in dairy cows is important. The objective of this study was to determine the relationship between energy balance and luteal function in lactating dairy cows. MATERIALS AND METHODS General Eight primiparous and 24 muhiparous lactating Holstein cows were studied from 1988 J Dairy Sci 71:1063-1072 1063  1 64 VILLA GODOY ET AL. parturition to 100 d postpartum or conception, whichever occurred first. Prepartum diets were not identical but were managed to maintain or achieve moderate prepartum body condition. Cows calved normally and remained healthy throughout the study. Cows were housed in stanchion stalls and received water and feed ad libitum. A total mixed diet (50 roughage: 50 grain on DM basis) was fed at 0200 and 1400 h (Table 1). Ingredients of diet were sampled and DM of ingredients determined weekly. Amount of ingredients in diet was adjusted according to variation in DM to maintain a 50:50 ratio of roughage to grain. On alternate weeks during the experiment, diet was sampled for chemical analysis (Table 1). Milk Yield Body Weight and Energy Balance Cows were milked twice daily (0400 and 1500 h) and yields of milk were recorded. Concentrations of fat in milk were determined monthly by Michigan Dairy Herd Improvement Association using an infrared analyzer. Monthly TABLE 1. Composition of total mixed diet. Concen- Item tration value for fat in milk was used to calculate daily 4 FCM for 15 d before and after the date of actual test. Milk was adjusted to 4 fat (4 FCM) by formula derived from Tyrrell and Reid (30): 4 FCM = yield of milk [136 + 5 (actual percent of fat)/340]. From d 4 to 7 postpartum until the end of the study, body weight of cows was measured (6 to 7 h after 0200 h feeding) on 2 successive d/wk. Weekly changes in body weight were extrapolated to estimate daily body weight. Energy balance of cows was estimated daily by subtracting net energy (NE) required for maintenance and lactation from daily intake of NE for individual cows. Requirements of NE for maintenance were based on estimated daily body weight and calculated as suggested by NRC (23): NE (Mcal) = 80 (kcal NE/kg'75). Due to requirements for growth, cows in first and second lactation were fed 20 and 10 , respectively, above requirements of NE for maintenance indicatedfor mature cows (23). To determine NE for lactation, daily yield (kg) of 4 FCM was multiplied by .74 Mcal (23). Daily intake of NE (DM basis) was calculated by multiplying NE (Mcal) per kilogram of diet (Table 1) by kilograms of diet ingested by COWS. Ingredient, Alfalfa hay 12.5 Corn silage 37.5 High moisture ear corn 30.0 Protein supplement (44 ) 17.0 Dicalcium phosphate and vitamin 3.0 premix Chemical analyses ~,~ Dry matter, 52.9 Energy, Mcal/kg 4 1.6 Crude protein. 17.8 Acid detergent fiber, 21.0 1Dry matter basis. Means are from 10 samples of total mixed diet taken in alternate weeks during the study. 2 Methods for chemical analyses in Pritchard and Staubus (24). 3Concentrations of minerals in total mixed diet were Ca (.6 ), P (.4 ), K (1 ), Mg (.2 ), S (.2 ), Na (.15 ), Mn (32 ppm), Fe (217 ppm), Cu (10 ppm), and Zn (4-5 ppm). 4As NE 1. Luteal Function and Other Reproductive Measures Concentrations of progesterone in fat-free milk parallel concentrations of progesterone in serum of cows [(25) Appendix]; therefore, luteal function can be monitored by pro- gesterone determined in milk or serum. To quantify progesterone in milk, samples of milk were obtained every 3rd d from d 5, 6, or 7 postpartum until the end of the experiment. Collection and processing of samples of milk and radioimmunoassay techniques used to quantify progesterone are described in the appendix. Basal progesterone (.18 -+ .01 ng/ml) was the mean of progesterone in milk when all cows were anovulatory (d 1 to 9 postpartum). At weekly intervals from 5, 6, or 7 d post- partum to first insemination, reproductive organs of cows were examined rectally to determine presence of corpora lutea and uterine involution. Uterine involution for a cow was indicated when diameter of previously gravid uterine horn was similar to the contralateral uterine horn and diameter of neither horn ournal of Dairy Science Vol. 71, No. 4, 1988  ENERGY BALANCE ON LUTEAL FUNCTION 1065 declined further. Data regarding presence of corpora lutea were used to confirm stages of estrous cycles. Data on uterine involution was used to confirm that cows were reproductively healthy. Thus, no data from rectal examina- tion of reproductive organs was examined statistically or will be reported. To detect estrus, cows were observed daily for three periods of 30 min (0600, 1800, and 2400 h). Estrus was when a cow stood to be mounted (/>2 s) during intervals when pro- gesterone in milk was <1 ng/ml. Ovulations were assumed to occur 24 h after first detection of estrus. If estrus was not detected, ovulation was assumed to occur 3 d before progesterone in milk exceeded 2 SD above basal proges- terone. Progesterone in milk was used to verify all diagnoses of estrus (< 1 ng/ml) and detection of corpora lutea (>1 ng/ml). Estrous cycles were the interval between two consecutive ovulations or periods of estrus as defined. ssimilation of Data and Statistical nalysis To characterize changes in EB of cows throughout the study, EB was expressed as megacalories of NE per day and could be positive (PEB) or NEB. To explain variation in EB, daily EB was the dependent variable in multiple linear regression using backward elimination procedures (14). Independent vari- ables were daily yield of 4 FCM, estimated daily body weight, daily intake of DM, and parity (1, 2, or/> 3 parturitions). Concentrations of progesterone in milk were plotted over time within an estrous cycle per cow and area under the curve was calculated. Area included values that exceeded .18 ng/ml by 2 SD and that were sustained for >/ three consecutive samples of milk. Maximal con- centration of progesterone within an estrous cycle (peak) and duration of luteal phase (interval that progesterone exceeded basal concentrations by two standard deviations) were calculated for first to third postpartum estrous cycles. Area, peak, and duration of progesterone profiles were used as measures of luteal function. In preliminary examination of variation in luteal function, area, peak, or duration of progesterone were used as dependent variables in multiple linear regression analyses, including backward elimination procedures (14). Inde- pendent variables were mean EB per estrous cycle, mean intake of DM per estrous cycle, mean yield of 4 FCM during the first 100 d postpartum, mean body weight per estrous cycle, parity (1, 2 or >3 parturitions), and con- secutive estrous cycles (first, second, or third). Duration of postpartum anovulation, number of consecutive postpartum estrous cycles, and EB exerted significant and confounded effects on progesterone. To reduce confounding, EB was limited to the interval when all cows were anovulatory (1 to 9 d postpartum), and unless stated differently, will be referred to as mean EB. Mean EB was used as a basis to group cows or was used as an independent variable. Two types of analysis were conducted to examine association between mean EB and progesterone with reduced influence of con- founding factors. First, area of progesterone profiles was partitioned within luteat phase according to four mean EB; />0 Mcal (con- trol), --.1 to -3.0, --3.1 to --6.0, or <--6 Mcal. Specific contrasts within luteal phase between mean EB were by Dunnett's t test (14). In addition, area of progesterone profiles within luteal phase was regressed against mean EB. Second, to determine association between mean EB and luteal function over time post- partum, we examined progesterone among luteal phases within mean EB. Specifically, we examined regression of progesterone (area, peak, and duration) among estrous cycles. Then we contrasted regressions of zero slope against regressions of progesterone (14) among estrous cycles with mean EB. Positive slopes indicated greater secretion of progesterone with succes- sive postpartum luteal phase. In addition, slopes of regression lines of progesterone within mean NEB (--.1 to --3.0, --3.1 to --6.0, or <-6 Meal) were contrasted with corresponding slopes of cows with positive mean EB (>0 Meal). Lack of parallelism between slopes indicated different effects of mean EB on luteal function among successive postpartum estrous cycles. To examine further the association between EB and luteal function, cows were grouped by mean EB (>0, --.1 to --3.0, --3.1 to --6.0, or <--6 Meal) and then actual duration and magnitude of EB were determined. We defined onset of NEB as the first 3 consecutive d postpartum when cows were in NEB. End of NEB was when cows were in PEB for at least 8 d of 2 consecutive wk. Duration of NEB was Journal of Dairy Science Vol. 71, No. 4, 1988  1066 VILLA-GODOY ET AL. the interval between the first and last day of NEB. Magnitude of NEB was indicated by nadir of EB. To determine the relationship between these aspects of EB and luteal function, area of progesterone within first, second, or third estrous cycles was the dependent variable in a regression analysis by backward elimination in which the independent variables were day and magnitude of nadir of EB and duration of NEB. To determine sources of variation on dura- tion of postpartum anovulation, we used interval from parturition to first ovulation postpartum as the dependent variable and used the same analysis and independent variables described in the previous paragraph. Using chi-square (14), proportions of ovula- tions associated with estrous behavior were contrasted among mean EB, mean intake of DM per estrous cycle, mean body weight per estrous cycle, mean yield of 4 FCM during first 100 d postpartum, or parity (1, 2, or ~3 parturitions). RESULTS AND DISCUSSION Yield of Milk Body Weight and Energy Balance Mean yield of 4 FCM during the experi- ment was 32.4 -+ .9 kg/d (range 20.8 to 40.7 kg). Peak yield of milk (40.2 + 3.4 kg) was at 44.8 + 3.5 d postpartum. Initial body weight of cows averaged 601 + 30 kg. Four cows main- tained or gained body weight throughout the study. All other cows lost 29 + 4 kg (range 9 to 106 kg) from 1st wk to 43 -+ 4 d postpartum when nadir for body weight occurred. From nadir, body weight increased, and by the end of the study all cows averaged 591 -+ 3i kg. Mean intake of DM increased from 19 + I kg in 1st wk to 27 -+ 2 kg by d 100 postpartum. When EB was averaged by day postpartum for all cows (Figure 1, top panel), EB was positive during first 2 d postpartum, became negative on d 3, reached nadir by d 10 post- partum, and was zero or positive by 80 d postpartum. From 1 to 9 d postpartum, 81 of cows were in NEB for at least 1 d. Among these 26 cows that experienced NEB, nadir of EB (--16.3 + 1.2; range --4 to --35 Meal) and duration of NEB (69.6 -+ 5.9; range 4 to 98 d) were similar to values reported previously (4, 19). From i to 9 d postpartum, 19 cows (59 ) experienced mean NEB. By the end of the study, 69 of cows did not recover energy lost at earlier stages of lactation and had net energy loss. Overall, daily EB was highly variable among cows and among days within cow. Although numbers of cows were limited, we detected no effect of parity on EB. Cows experienced NEB even when calories offered were not limiting thus EB and variation in EB were spontaneous. Consequently, we examined the relationship between luteal function and different EB without dietary manipulation. This is consistent with examining effects of homeorhetic control of lactation on luteal function. 20~ All Cows (n=32) YIELD 0 - -- - 32.4 - o4 0 'i~ne;,,~/~ -F: -~-- ~ 32.3 llO i 1 I 1 I i I I I I I I I I I I I [ l LU 20- (_> - I to-3Mcal (n:6) z IO- -J O- 31.8 <I m -i0 o 71t a~ -3.11 o-6 Mcol (n=5) IJJ z 0 1/ . ~ ~ .~A 34.8 -I0 I I I ~ I T I I I I I I I I I ~ I i I I 20~ <-6 Mcol (n=8) °tl ~ --v--v-J ~r 31.3 -lOl~, ,, ,,,, , , 0 20 40 60 80 I00 DAY POSTPARTUM Figure 1. Energy balance and yield of milk during the first 100 d postpartum. Daily mean of energy balance (Meal of net energy) was calculated for all cows (top panel) or for cows grouped according to mean energy balance during postpartum anovulation (1 to 9 d). Yield of 4 FCM (kg) is the daily mean during first 100 d postpartum. Numbers of cows are in parenthesis. Pooled SE is 1.3 for energy balance and .9 for yield of milk. Journal of Dairy Science Vol. 71, No. 4, 1988  ENERGY BALANCE ON LUTEAL FUNCTION 1067 TABLE 2. Effect of mean energy balance during anovulation on interval to nadir and actual nadir of energy balance in lactating cows. Mean energy balance Energy balance Postpartum interval to nadir Actual nadir (Mcal) ~ (d)~ ~ (Mcal) .X SE X SE >0 38.6 12.2 a --8.7 1.6 a --.1 to --3.0 40.0 10.5 a --19.1 1.3 b --3.1 to --6.1 30.2 8.5 a --22.2 1.5 b <--6 12.0 4.4 b --23.5 1.6 b a'bMeans within columns without common superscripts differ (P<.01). Factors ssociated with Variation in Energy Balance Daily EB was regressed on parity (1, 2, or ~3 parturitions) and was not correlated (r = .10). In addition, daily EB was not correlated with estimated daily body weight, either actual or percent change in body weight (r = .13). Variation in EB was explained largely by intake of energy (r = .73, P<.01) and to a lesser extent by yield of milk (r = -.25 P<.05). Throughout the study, only 19 (n = 6) of cows never experienced NEB. Yield of 4 FCM (32.8 -+ 1.9 kg) of cows always in PEB did not differ from mean yield of 4 FCM (32.3 - 1.0 kg) for the 26 cows that experienced NEB at least transiently. That yield of milk did not differ among cows with distinctly different EB (Figure 1) illustrates that some cows ingest sufficient nutrients to satisfy requirements for high yield of milk and to sustain PEB but other cows fail to do so and convert nutrients to milk less efficiently. Yield of milk, although as- sociated negatively, has a minor effect on variation in EB of cows. Thus, yield of milk would not be highly predictive of EB, intake of feed, or metabolic status of lactating cows. But interval to nadir and actual nadir of EB differed among mean EB (Table 2). Specifically, cows with lowest mean EB had shortest postpartum interval to nadir of EB. Factors ssociated with Luteal Function All cows formed at least two corpora lutea during the study. Duration of postpartum anovulation averaged 23.9 -+ 2.2 d (range 10 to 52 d). Behavioral signs of estrus were detected in association with 64.9 of ovulations. Estrus was detected with a lower proportion (P<.01) of first postpartum ovulations (34.4 ) than with second (71.9 ) or third (83.3 ) post- partum ovulations. Duration of postpartum anovulation and detection of estrus were not correlated significantly with parity, body weight, yield of 4 FCM, intake of DM, or mean EB. Our observation that all cows ovu- lated and resumed estrous cycles by 23.9 -+ 2.2 d postpartum is consistent with previous reports (4, 5, 27). Thus, postpartum anovula- tion is not a source of extended intervals not pregnant in most dairy cows. Together, peak and duration of progesterone profiles accounted for most variation in area under profiles of progesterone (r 2 = .84; P<.001). Thus, results for area will be pre- sented most frequently, but peak and duration were always examined. Yield of 4 FCM, mean body weight per cycle, and parity were not correlated with area and peak of progesterone in milk or with duration of luteal phases (Table 3). In addition, changes in body weight from parturition to nadir of body weight were not associated with progesterone in milk (data not shown). We found no evidence that duration of postpartum anovulation, detection of estrus, or luteal function were influenced by yield of milk or body weight. Thus, as independent factors, yield of milk or body weight may not influence reproductive performance in lactating dairy cows. Yield of milk and body weight may ournal of Dairy Science Vol. 71, No. 4, 1988
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