IMMUNE FUNCTION AND METABOLIC STRESS DUE TO PRECALVING ENERGY LEVEL AND POSTCALVING MASTITIS CHALLENGE IN DAIRY COWS

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1 IMMUNE FUNCTION AND METABOLIC STRESS DUE TO PRECALVING ENERGY LEVEL AND POSTCALVING MASTITIS CHALLENGE IN DAIRY COWS Daniel Graugnard, Massimo Bionaz, Erminio Trevisi, Manishi Mukesh, Mario Ordonez, Kasey M. Moyes, Janeen L. Salak-Johnson, Richard L. Wallace, James K. Drackley, Giuseppe Bertoni, and Juan. J. Loor TAKE HOME MESSAGES Inclusion of straw in far-off and close up diets designed to meet requirements of dry cows improved energy balance and dry matter intake (DMI) after calving compared with liberal access to a moderate energy diet. Milk yield during the first 41 days after calving did not differ in cows fed highstraw/controlled energy diet compared to liberal access to a moderate energy diet. Blood neutrophil phagocytosis, a measure of immune function, was greater after a mastitis challenge postcalving in cows fed high-straw/controlled energy diets during the dry period. The mastitis challenge postcalving induced greater metabolic stress in cows that were fed moderate energy precalving. A high-straw/controlled-energy diet precalving was more beneficial in reducing postcalving severity of negative energy balance, DMI, while also enhancing immune function and reducing metabolic stress during a mastitis challenge. INTRODUCTION Frequently, high-producing dairy cows experience a significant number of metabolic (fatty liver, ketosis) and infectious diseases (mastitis) that may impair reproductive performance and survival during early lactation, thus, resulting in financial losses to farmers. The majority of diseases occurring after calving are caused by a multitude of factors including a level of production inconsistent with nutrient intake, provision of an inadequate diet pre- and post-partum, an unsuitable environment, or various combinations of these factors. Although the periparturient period (3 wk pre-calving through 3 wk post-calving) is associated with peak incidence of production and infectious diseases, their effects on dairy cow health and productivity extend far into the following lactation. Primary objectives of this study were to evaluate 1) how different levels of dietary energy prepartum affect energy balance, DMI, and milk production in early lactation; and 2) how a mastitis challenge after calving affects immune function as well as production parameters. 20

2 MATERIALS AND METHODS During the entire dry period (~45 d), 40 Holstein cows entering their second or greater lactation were assigned (n = 20/diet) to a controlled-energy (high-straw) diet, which was fed for ad libitum intake to provide at least 100% of calculated net energy for lactation (NE L = 1.34 Mcal/kg dry matter), or were assigned to moderate-energy diet to provide ~150% of calculated NE L (1.62 Mcal/kg dry matter). Cows were fed using an individual Calan (American Calan, Northwood, NH) gate feeding system during the dry period and were housed in a ventilated enclosed barn. After calving, cows were moved to a tie-stall barn and were fed a common lactation diet (NE L = 1.69 Mcal/kg dry matter) and milked twice daily (0400 and 1600 h). During the first 10 days after calving, cows (n = 10/precalving diet) were assigned to receive an intramammary mastitis challenge (Escherichia coli lipopolychacharide (LPS), 200 μg) or served as controls (no LPS infusion). Cows used were bacteriologically-negative in all mammary quarters before the LPS challenge. Parameters of interest included milk yield, DMI, and energy balance. Blood samples for determination of non-esterified fatty acids (NEFA), hydroxybutyrate (BHBA), glucose, insulin, urea, ceruloplasmin, haptoglobin, albumin, GOT, bilirubin, reactive oxygen metabolites (ROM), cholesterol, vitamin A, vitamin E, -carotene and creatinine concentration were collected at 2, 7, 10, 14 and 21 days relative to calving. Blood neutrophils were isolated on -14, 7 (prior to LPS), 14, 30, 60, and 120 days relative to calving for the in vitro determination of their ability to engulf a pathogen (also known as phagocytosis). The PROC MIXED procedure of SAS (SAS Institute, Cary, NC) was used to analyze data according to pre-determined periods of interest including 1) the effect of LPS challenge vs. control in cows fed moderate energy precalving only; and 2) postcalving temporal effect due to prepartum dietary energy (controlled-energy vs. moderate energy) in cows receiving intramammary LPS. RESULTS AND DISCUSSION Effect of mastitis challenge postcalving in cows fed moderate energy during the dry period (Table 1): During the period of time evaluated we observed greater DMI (3.38 vs % of BW) in the unchallenged control group compared with the LPS-challenged group. Milk yield was similar for both treatments (43.9 vs kg/d). Energy balance calculations indicated that cows in the unchallenged control group were able to cover ~5% more of their energy requirements over the first six weeks after calving when compared with the LPS-challenged group. Blood concentrations of NEFA and BHBA increased (data not shown) to a greater extent (interaction effect) in cows receiving the mastitis challenge. Overall, most of the parameters evaluated followed the typical postcalving pattern in both groups, but it was evident that those cows receiving the mastitis challenge soon after parturition were affected to a greater extent. Despite the lack of difference in milk yield, the mastitis challenge and likely the ensuing alterations in metabolism, e.g. inflammation, appeared to have long-lasting effects on the animal including reduced DMI. That response was reflected in the more negative energy balance through week 6 of the study. Long-term post-calving effect of feeding controlled-energy (high-straw) or moderate energy diets during the dry period in cows receiving a mastitis challenge (Table 2): We observed greater DMI (2.90 vs %BW) starting the first week after calving in cows fed 21

3 high-straw/controlled-energy in the dry period, a response that remained consistent until 41 DIM. Milk yield was similar for both treatments. Energy balance calculations indicated that cows fed high-straw/controlled energy vs. moderate energy were able to cover ~10-12% more of their energy requirements during the first 2 weeks after calving. Thereafter, cows fed highstraw/controlled-energy pre-calving tended to cover more of their energy requirements. NEFA and BHBA were consistently greater in cows fed the moderate energy diet pre-calving, indicating a higher degree of mobilization of fat reserves from adipose tissue (Table 2). In contrast, cows fed the moderate energy diet had greater concentrations of ceruloplasmin as well as reactive oxygen metabolites indicating both a marked positive inflammatory response and more pronounced oxidative stress response (Figure 1). Neutrophils from cows fed highstraw/controlled-energy had a greater phagocytic capacity compared with animals fed moderate energy. This effect was more evident at 14 days post-calving (Figure 2), i.e. the first sampling after the mastitis challenge on day 7. The post-calving DMI and energy balance data suggest that the high-straw/controlled energy group was able to cover their nutrient requirements to a greater extent compared to the moderate energy group. NEFA and BHBA are good predictors of lipid mobilization, liver fatty acid oxidation, and ketogenesis. In this study, the NEFA data indicated that the group fed the moderate energy diet precalving likely accumulated more body fat, hence, the greater NEFA concentrations postcalving. Although we do not currently have data on liver tissue lipid composition, it is likely that the moderate energy precalving would have led to higher uptake of NEFA by the liver leading to increased triglyceride accumulation. The extent of fatty liver will be determined based on those data. Ceruloplasmin is a positive acute phase protein which increases in concentration during the acute phase response of inflammation or infection. In this study, the higher ceruloplasmin levels in the group fed moderate energy precalving might suggest more pronounced inflammation during the mastitis challenge. In addition, when there is overt inflammation a proinflammatory cascade leads to activation of immune cells (i.e., neutrophils) that produce both reactive oxygen species and reactive nitrogen species as a mechanism of killing pathogens; the use of these highly reactive compounds in the cytotoxic (i.e., cell killing) response by the immune cells can at some point also damage the host tissue. The imbalance in the amount of reactive oxygen species used to kill pathogens is known as oxidative stress. Reactive oxygen metabolites are a marker of oxidative stress which along with ceruloplasmin were suggestive of cows fed moderate energy precalving being under a more pronounced metabolic stress. Neutrophils are immune cells of key importance in the containment of infection. Their function is to engulf and destroy bacteria to protect the host s tissues, including mammary gland and liver. In this study, the neutrophils from the animals fed high-straw/controlled energy seemed to be more active because after the mastitis challenge they were able to engulf bacteria (a measure of killing potential) to a higher extent when compared to animals fed moderate energy. PRELIMINARY CONCLUSIONS Data from this study provides evidence that feeding high-straw/controlled energy diets that meet the calculated requirements of dietary energy precalving can improve the transition into lactation 22

4 potentially by preventing excessive fat deposition, which in turn may affect liver and immune cell function as well as oxidative stress of the cow after calving. Table 1. Effect of mastitis challenge (LPS) early postcalving in cows fed moderate energy precalving. Treatment P value Item Control LPS SEM 1 Trt Time Trt time DMI 2 (%BW ) 7 to Milk 2 (kg/d) 7 to Energy balance 2 wk 1 % requirements wk 1 to 6 % requirements Blood Metabolites 3 NEFA, meq/l BHBA, mmol/l Largest SEM is shown. 2 Day or wk relative to parturition. 3 Data from 7, 14, and 30 DIM. Table 2. Effect of a mastitis challenge (LPS) early postcalving in cows fed highstraw/controlled energy or a moderate energy diet precalving. Prepartum diet P value Item Moderate Controlled SEM 1 Diet Time Diet time DMI 2 (% BW) 7 to to Milk 2 (kg/d) 7 to Energy balance 2 wk 1 % requirements wk 1 and 2 % requirements wk 1 to 6 % requirements Blood Metabolites 3 NEFA, meq/l BHBA, mmol/l Largest SEM is shown. 2 Day or wk relative to parturition. 3 Data from 7, 14, and 30 DIM. 23

5 Figure 1. Blood Reactive Oxygen Metabolites and Ceruloplasmin during lactation in cows fed a high-straw/controlled energy or moderate energy diet during the entire dry period and receiving an intramammary mastitis challenge with LPS at 7 d postcalving. Concentration ROM (mg H 2 O 2 /100 ml) Diet and time P < 0.05 Controlled Energy Moderate Energy Ceruloplasmin (mol/l) Diet P = 0.08 Time P < 0.05 Day relative to calving Figure 2. Total blood neutrophil (PMN) phagocytosis during lactation in cows fed a highstraw/controlled energy diet or moderate energy diet during the entire dry period and receiving an intramammary mastitis challenge with LPS at 7 d postcalving. a,b = diet x time effect; *diet x time effect in cows fed moderate energy precalving. Phagocytosis (%) * Diet x time P = 0.15 Diet P = 0.01 a b * ** * *** Moderate Energy Controlled Energy F Day relative to calving a b 24