The most critical period for a dairy cow is called the transition period and lasts 21 days before and 21 after parturition. During the transition period, dairy cows adapt to numerous hormonal and metabolic changes related to the end of pregnancy and the beginning of lactation (7, 14). Approximately 50% of cows suffer from various metabolic, nutritional, and infectious disorders (23, 27).
Cows may experience reduced dry matter intake during the close-up period, which generally results in negative energy balance. A pre- or post-partum negative energy balance directly alters the metabolic status of dairy cows (35). An energy requirement due to energy deficiency in the transition period causes fat mobilisation and a consequent increase in non-esterified fatty acids (NEFA) in the blood (30). Excessive concentrations of NEFA in the blood might be toxic (1) because the ruminant liver has insufficient ability to metabolise all NEFA into triacylglycerol. Therefore, ketone bodies are seen in the blood, urine, or in milk when the metabolic efficiency of the liver is overmatched (1, 13). The predominant form of ketone bodies in the blood is β-hydroxybutyric acid (BHBA) which reflects the fatty acid oxidation and energy status of the dairy cow (10, 40). Besides illuminating energy status, excessive concentrations of NEFA and BHBA have a negative effect on immune cell functions, such as impairing respiratory burst activity (37) and chemotaxis (39). Not only the energy problem but also ion deficiencies are important detriments seen during the transition period and as postpartum effects on dairy cow health (24, 31). Calcium is an important ion used in metabolic processes during the transition period to produce good quality colostrum and subsequently milk (31). Most cows suffer from clinical or subclinical hypocalcaemia during the first days of lactation, and total plasma calcium levels reach their physiological level 2 to 3 days after parturition (17, 32). Clinical or subclinical hypocalcaemia negatively affects energy metabolism and the immune status of cows and a variable degree of Ca insufficiency impairs leukocyte activity (24).
The body condition score (BCS) is a useful and simple method to assess an animal’s energy reserves (16) as an indirect measurement of fat metabolism and its correlation with energy metabolism (12). The incidence of metabolic disorders and their relationship with BCS has been studied since BCS relates to the fertility status of dairy cows (4, 16, 38).
It is known that serum metabolites, calcium concentrations and BCS alter during early lactation. The relationship of blood metabolites and ions to the degree of BCS loss during the dry period may provide important information for herd management and reproduction (21). Prepartum BCS loss has been investigated in a few papers, however its consequences on pre- and postpartum period are still not known perfectly (21, 35). We hypothesised that pre-calving BCS loss alters calcium and serum metabolites as well as fertility in Brown Swiss dairy cows. The objective of this study was to determine the role of pre-calving BCS loss level in postpartum metabolic status and reproductive outcomes.
Constituents of diets fed during far-off (−50 to −31 days relative to expected calving), close-up (−30 days to calving), and early lactation
Component | Far-off | Close-up | Early lactation |
---|---|---|---|
Ingredient, % of DM | |||
Vetch hay | 11.58 | - | - |
Alfalfa silage | - | - | 9.67 |
Alfalfa hay | 7.89 | 6.97 | 10.29 |
Corn silage | 52.60 | 43.51 | 44.16 |
Wheat straw | 10.52 | 22.25 | - |
Soybean meal, 48% CP | - | - | 1.61 |
Concentrated feed | 15.78 | 20.94 | 30.31 |
Limestone | 0.82 | 2.25 | 1.57 |
Salt | 0.30 | - | 0.26 |
Ammonium chloride | - | 1.15 | - |
Dicalcium phosphate | 0.14 | 0.30 | 0.44 |
Magnesium oxide | - | 0.12 | 0.44 |
Magnesium sulphate | 0.16 | 1.35 | 0.25 |
Sodium bicarbonate | - | - | 0.70 |
Calcium sulphate | - | - | 0.10 |
Mineral-vitamin mix1 | 0.21 | 0.17 | 0.20 |
Diet contained a minimum 4.3% of Mg, 8% of S, 6.1% of K, 2.0% of Fe, 3.0% of Zn, 3.0% of Mn, 5,000 mg/kg of Cu, 250 mg/kg of I, 40 mg/kg of Co, 150 mg/kg of Se, 2,200 kIU/kg of vitamin A, 660 kIU/ kg of vitamin D3, and 7,700 IU/kg of vitamin E
The following model was used for evaluating the effect of the group, day of sampling and their interaction with BCS, BIT, BID, AST, ALP, ALT, GGT, CK, cholesterol, glucose, urea, LDH, albumin, total protein, triglyceride, NEFA, BHBA, P, and Ca:
(
Animals within groups were assessed as a random effect, while group, period, or day of sampling and their interaction were assessed as fixed effects. When a significant difference was revealed, any significant terms were compared by simple effect analysis with Bonferroni adjustment. P < 0.05 was considered significant in all analyses. All data were analysed using the mixed procedure of SPSS (V22.0; IBM SPSS, USA).
The number of parities was not statistically significantly different between groups. The mean age of production was 2.2 lactations.
Body condition scores changed over time in all groups (P < 0.05). The changes during the study period are shown in Fig. 1. The mean BCS was significantly higher in BCS-C cows compared to BCS-L and BCS-H animals after parturition (P < 0.05).
The concentrations of AST, ALP, cholesterol, BIT, BID, glucose, urea, total protein, Ca, triglyceride, and NEFA changed over time in all groups (P < 0.05). However, regardless of the group, no significant difference was observed in BHBA, albumin, LDH, P, ALT, CK, or GGT as the study advanced (P > 0.05).
Prepartum blood sampling showed that the mean Ca levels of BCS-H cows were in the subclinical hypocalcaemia range (8.4 ± 0.2 mg/dl). On the third day postpartum, Ca concentration was greater in BCS-C than BCS-H (P < 0.05) cows, but the BCS-H and BCS-L groups had similar Ca concentrations (P > 0.05).
Mean blood Ca concentrations were at subclinical hypocalcaemia levels in BCS-L and BCS-H cows (Fig. 2).
Whereas BHBA levels were different during the postpartum period, NEFA concentration was similar among groups during the study period (not shown in table). None of the cows included in the study had a severe negative energy balance effect as indicated by NEFA values. On the other hand, the BCS-L and BCS-C groups showed similar blood BHBA concentrations during the study period, but the BCS-H group showed greater BHBA levels on days 3 (1,378 ± 317 μmol/L) and 30 ± 4 (1,216 ± 273 μmol/L) postpartum (Fig. 3). The concentrations of BHBA on these days were at subclinical ketosis level. For BCS-H cows, NEFA concentration and BHBA levels showed moderate correlation on day 3 (r = 0.365; P < 0.05) and strong correlation on days 14 (r = 0.755; P < 0.05) and 30 ± 4 (r = 0.776; P < 0.05), and these parameters were also negatively correlated with Ca content (r = −0.591; P < 0.05) in prepartum.
Glucose, urea, LDH, ALT, albumin, total protein, cholesterol, triglyceride, and P levels were similar among the groups (not shown in table).
Aspartate aminotransferase, an enzyme for liver damage detection, was higher in the BCS-H group than in other groups at 14 days postpartum (P < 0.05). This group also had greater CK concentration on the third day postpartum, and AST concentration showed a positive strong correlation with CK levels (r = 0.641; P < 0.05). On day 3 postpartum in the BCS-L group, BID and BIT values were greater than in BCS-C cows. The high level of BIT concentration was also sustained at 14 days postpartum (P < 0.05; Table 2).
Effect of different body condition score (BCS) changes on concentrations of AST, CK, GGT, cholesterol, BID, and BIT (mean ± SEM) among groups
Days | P-value | ||||||
---|---|---|---|---|---|---|---|
Parameters | −14 ± 3 |
3 |
14 |
30 ± 4 |
Group | Time | Group*Time |
AST | |||||||
BCS-H | 76.76 ± 4.09b | 146.09 ± 18.46a | 146.26 ± 17.36a,A | 88.90 ± 5.03b | |||
BCS-L | 82.49 ± 5.51b | 127.04 ± 12.01a | 112.70 ± 11.97ab,C | 92.21 ± 5.22b | 0.034 | 0.000 | 0.050 |
BCS-C | 79.75 ± 3.18 | 107.23 ± 4.03 | 102.03 ± 4.98B | 85.51 ± 4.85 | |||
ALP | |||||||
BCS-H | 45.63 ± 3.26 | 34.94 ± 5.07 | 34.25 ± 4.74 | 35.69 ± 5.75 | |||
BCS-L | 40.85 ± 4.87ab | 51.90 ± 6.27a | 33.75 ± 3.92b | 30 ± 3.74b | 0.624 | 0.000 | 0.052 |
BCS-C | 45.81 ± 6.27ab | 50.48 ± 6.23a | 37.76 ± 5.87b | 40.62 ± 7.12ab | |||
CK | |||||||
BCS-H | 464.18 ± 183.58b | 1675.20 ± 621.04a,A | 536.60 ± 130.88b | 404.19 ± 139.10b | |||
BCS-L | 452.46 ± 228.74 | 433.14 ± 104.29B | 376.79 ± 114.27 | 414.46 ± 132.60 | 0.010 | 0.047 | 0.048 |
BCS-C | 458.78 ± 118.61 | 219.90 ± 29.43B | 286.23 ± 51.44 | 329.82 ± 91.09 | |||
GGT | |||||||
BCS-H | 15.01 ± 1.27 | 13.20 ± 2.45 | 16.10 ± 1.78 | 18.54 ± 1.49 | |||
BCS-L BCS-C | 19.02 ± 2.85 15.75 ± 1.63 | 23.21 ± 3.02 18.90 ± 2.82 | 22.76 ± 1.95 17.50 ± 2.17 | 16.03 ± 1.78 14.31 ± 1.26 | 0.041 | 0.322 | 0.112 |
Cholesterol | |||||||
BCS-H | 93.88 ± 3.43b | 68 ± 4.14c | 79.94 ± 4.48bc | 115.19 ± 5.91a | |||
BCS-L | 88.70 ± 2.90b | 67.25 ± 2.77c | 76.55 ± 8.45bc | 110.30 ± 7.29a | 0.164 | 0.000 | 0.940 |
BCS-C | 92.38 ± 2.99b | 76.86 ± 3.05c | 87.48 ± 6.09bc | 117 ±6.01a | |||
BID | |||||||
BCS-H | 0.11 ± 0.02ab | 0.18 ± 0.03a,AB | 0.13 ± 0.03ab | 0.08 ± 0.02b | |||
BCS-L | 0.10 ± 0.01bc | 0.27 ± 0.03a,A | 0.16 ± 0.02b | 0.08 ± 0.01c | 0.008 | 0.000 | 0.016 |
BCS-C | 0.11± 0.01a | 0.14 ± 0.02a,B | 0.10 ± 0.02ab | 0.05 ± 0.01b | |||
BIT | |||||||
BCS-H | 0.09 ± 0.01b | 0.31 ± 0.06a,AB | 0.20 ± 0.05ab,AB | 0.11 ± 0.01b | |||
BCS-L | 0.11 ± 0.01b | 0.45 ± 0.07a,A | 0.32 ± 0.05a,A | 0.15 ± 0.02b | 0.001 | 0.000 | 0.014 |
BCS-C | 0.09 ± 0.01 | 0.20 ± 0.02B | 0.16 ± 0.03B | 0.13 ± 0.02 |
Means within a row (a–c) and column (A–B) with different superscript letters differ significantly (P < 0.05)
Postpartum genital tract examination, clinical endometritis rate, and fertility parameters are shown in Table 3. BCS-C cows had a high proportion of ovarian resumption at 30 ± 4 days postpartum and fewer days open (89.2 days). Also, BCS-C cows had a significantly lower clinical endometritis rate (9.5%), and higher overall pregnancy rate (80.95%) than the BCS-H and BCS-L groups (P = 0.032 and P = 0.035, respectively).
Effect of different body condition score (BCS) changes on rate of the corpus luteum activity, clinical endometritis, calving to conception interval (median (min–max)), and pregnancy rate
Group | ||||
---|---|---|---|---|
Parameter | BCS-C | BCS-L | BCS-H | P-value |
Corpus luteum activity < 30 ± 4d (%) | 61.90 | 40 | 50 | 0.187 |
Clinical endometritis (%) | 9.50 b | 35 a | 37.50 a | 0.032 |
Interval from calving to conception (day) | 82 (47–119) | 122(50–168) | 106 (47–150) | 0.561 |
Pregnancy rate (%) | ||||
1st service | 61.90 | 50 | 50 | 0.473 |
Overall | 80.95a | 65 b | 56.25 b | 0.035 |
Means within a row (a, b) with different superscript letters differ significantly (P < 0.05)
Body condition score loss depends on many factors starting with the genotype of the cow and ending with farm management. BCS loss during the last weeks of the dry period may depend on mistakes made during transition period management which may include inadequate nutrition or controlled energy feeding strategies (6, 35). Pre-partum BCS loss has been investigated in a few papers; however, its consequences for the pre- and postpartum periods are still not perfectly known (21, 35).
Prepartum BCS loss has no role in prepartum blood concentrations; however, it does have one in determining metabolic and ion status in the postpartum period (35). High NEFA concentration has a negative effect on reproduction (22) and health status in dairy cows (12). The results of energy-controlled feeding studies do not refer to the exact consequences on prepartum serum NEFA concentrations (3, 20). Although in our study we did not observe any significant difference between groups in NEFA concentrations in prepartum and postpartum examinations, NEFA concentration increased similarly on three days post-calving. All cows were on the same farm and fed the same TMR during the study period. It was clearly shown that the energy in the feed ration had no role in prepartum BCS loss.
Concentrations of NEFA increased after parturition and then started to decline dramatically until 30 ± 4 days postpartum; however, there was no difference between groups. It is known that increased NEFA concentration is followed by a decrease in dry matter intake. Combined with that, energy demands for milk production increase. Whereas the liver has limited capacity for fatty acid oxidation and at the end of the limit, ketone bodies accumulate. As a result of that process, clinical or subclinical ketosis might be seen during early lactation (33). This information is supported by the present study. BCS-H cows suffered from subclinical ketosis at one week (1,378.34 ± 317.29 μmol/L) and four weeks (1,216.04 ± 273.86 μmol/L) postpartum. McCarthy
Postpartal metabolic tests showed that cows in the BCS-H group suffered from high mean BHBA levels at 3 and 30 ± 4 days after parturition. A high concentration of BHBA is related to weaker immune response (23) and lower reproductive parameters (22). Roche
The present study suggested that a BCS loss of 0.5 points or greater during the close-up period had a negative influence on calcium balance in the prepartum and early postpartum period. The mean calcium concentrations at −14 ± 3 and 3 days were at subclinical hypocalcaemia level in the BCS-H group (8.40 ± 0.20 mg/dl and 7.81 ± 0.33 mg/dl, respectively). Sheehy
The blood AST levels in the BCS-H group were significantly higher on days 3 and 14 postpartum and correlated with CK at 3 days postpartum (r = 0.641; P < 0.05). The high level of AST could be associated with higher fat mobilisation and negative energy balance due to increased metabolic demands (5). AST is not a liver-specific enzyme, and muscle damage could also result in an increase in AST levels (11, 15, 19). CK activity in cows betrays the source releasing AST (liver-related or muscle-related). The increase in AST levels together with CK reflected that BCS-H cows had muscle loss. The present study also indicated higher total and direct bilirubin concentrations in BCS-L cows than in the BCS-H and BCS-C groups at 3 days postpartum, and significantly higher total bilirubin concentrations at 14 days. When these results were combined with AST concentrations, the related groups were seen not to have suffered any crucial hepatic damage during the study period.
The prepartum high BCS and low Ca levels and postpartum high BHBA concentration might be responsible for reduced dry matter intake (34), suppressed bacterial clearance ability in the early puerperal period, subsequent clinical endometritis occurrence (33), and predisposition to periparturient metabolic disorders such as ketosis, milk fever, displacement of abomasum, retained fetal membranes,
In BCS-H and BCS-L cows, although the resumption of ovarian activity at 30 ± 4 days postpartum was delayed and resulted in more days open compared to the BCS-C group, the differences were not statistically significant (Table 3). But these groups had a significantly higher rate of clinical endometritis and lower overall pregnancy rate (56.25% and 65%, respectively) than the BCS-C group (overall pregnancy rate 80.9%). These results agree with Hoedemaker
Prepartum BCS loss of 0.5 points or more could negatively affect blood serum Ca level at pre- and postpartum and postpartum BHBA concentrations in Brown Swiss cows. The subclinical ketosis and subclinical hypocalcaemia in the periparturient period would increase the risk of clinical endometritis on the 30th ± 4 days postpartum, and furthermore would decrease the overall pregnancy rate at 150 days postpartum. Otherwise, the screening of blood Ca and the monitoring of BCS loss during the last 14 ± 3 days of pregnancy and early postpartum period could be useful to identify cows susceptible to metabolic and reproductive problems in the postpartum period.