Influence of a marine algae supplementation on the oxidative status of plasma in dairy cows during the periparturient period

Preventive Veterinary Medicine 103 (2012) 298–303

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Influence of a marine algae supplementation on the oxidative status of plasma in dairy cows during the periparturient period N. Wullepit a,b , M. Hostens c , C. Ginneberge a,b , V. Fievez a , G. Opsomer c , D. Fremaut b , S. De Smet a,∗ a b c

Laboratory for Animal Nutrition and Animal Product Quality, Department of Animal Production, Ghent University, Proefhoevestraat 10, 9090 Melle, Belgium Faculty of Biosciences and Landscape Architecture, University College Ghent, Schoonmeersstraat 52, 9000 Ghent, Belgium Department of Reproduction, Obstetrics, and Herd Health, Faculty of Veterinary Medicine, Ghent University, Salisburylaan 133, 9820 Merelbeke, Belgium

a r t i c l e Keywords: Micro algae Transition period Milk fat depression Oxidative status NEB Dairy cow

i n f o

a b s t r a c t This study was part of a larger study that addressed the effects of marine algae (ALG) supplementation in the ration of high yielding periparturient dairy cows. The objectives were to induce milk fat depression (MFD) in early lactation by feeding docosahexaenoic acid (DHA) from ALG and to determine the effects on milk production, milk components and metabolic status early post partum. This study focuses on the oxidative status in the plasma during the ALG supplementation. Plasma samples were collected from 16 Holstein Friesian cows at the day of parturition and at −1, 2, 4 and 6 weeks relative to calving with half of the cows receiving the ALG supplement (44 g DHA/d) from 3 weeks pre partum on. The following parameters were measured in plasma: ferric reducing ability of plasma (FRAP), ␣-tocopherol level, glutathione peroxidase activity (GSH-Px) and thiobarbituric acid reactive substances (TBARS) concentration. There was a significant effect of time for FRAP and ␣-tocopherol indicating changes in the plasma oxidative status around parturition. The ALG supplementation was successful in creating a milk fat depression (MFD) but could not improve the energy balance. Feeding of ALG significantly increased lipid peroxidation as measured by TBARS, probably through their high content of n-3 polyunsaturated fatty acids. © 2011 Elsevier B.V. All rights reserved.

1. Introduction The peripartum and early lactation periods are especially critical for health and subsequent performance of dairy cows which are exposed to drastic physiological adaptations and concomitant metabolic stress (Goff and Horst, 1997; Drackley et al., 2005). During the transition period, cows are also more susceptible to oxidative stress (Miller and Madsen, 1994; Bernabucci et al., 2002), which may contribute to an impaired immune function and an

∗ Corresponding author. E-mail address: [email protected] (S. De Smet). 0167-5877/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.prevetmed.2011.09.007

enhanced susceptibility to periparturient diseases (Miller et al., 1993; LeBlanc et al., 2004). The primary challenge faced by periparturient dairy cows is a sudden and marked increase of nutrient requirements for milk production, at a time when dry matter intake (DMI), and thus nutrient supply, lags behind. The cow therefore enters a period of negative energy balance (NEB), which leads to the mobilization of body reserves (Drackley, 1999; Collard et al., 2000) and a pronounced alteration of the oxidative status (Bernabucci et al., 2005). Possible efforts to enhance the energy status in the transition period include the manipulation of the dry period length and the optimization of pre partum nutritional level, by increasing the energy density of the diets, and increasing the DMI and/or decreasing the early post partum energy

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output (Son et al., 1996; Dann et al., 2006; Grummer, 2007). The energy density of a diet can be increased by replacing grain or forage with fats, like n-3 polyunsaturated fatty acids (PUFA), and may increase energy intake if DMI is not depressed (Staples et al., 1998). A dietary supply of PUFA can also alter the milk fatty acid composition and result in a milk fat depression (MFD) (Chilliard et al., 2007), which possibly can diminish the energy output post partum (Jensen, 2002). Dietary supply of PUFA can be achieved through addition of specific marine algae (ALG) rich in DHA (e.g. Schizochytrium spp.). As described by Boeckaert et al. (2008) a micro algae supplementation level of about 10 g/kg of DMI can result in a MFD of more than 50%. Hence, a supplementation of ALG during the transition period could result in a better post partum energy status and help the high yielding dairy cow to cope with the metabolic challenges during early lactation (Bernabucci et al., 2005). However, PUFA-rich diets may at the same time increase the risk of lipid peroxidation in plasma of dairy cows (Gobert et al., 2009). This could induce oxidative stress and compromise animal health (Miller et al., 1993). The objectives of the present study were therefore to evaluate the effects of ALG supplementation in the ration of high yielding dairy cows during the transition period on some plasma oxidative status parameters. 2. Materials and methods 2.1. Experimental design and diets Sixteen healthy Holstein Friesian cows were randomly assigned to either a control (CON) or micro algae (ALG) supplemented diet, with treatment groups being balanced for parity (3 primiparous and 5 multiparous cows), expected calving date, expected milk production and milk fat content, and genetic origin. The study was conducted at the experimental research farm of the Ghent University (Biocentrum Agrivet, Melle, Belgium). On this farm the average 305 d – milk yield per cow was 9934 kg milk (3.86% fat and 3.47% protein). During the experimental period (August 2007 until March 2008), all cows were housed in a loose stable with cubicles. Cows were milked 2.2 (±0.66 SD) times a day by means of an automated voluntary milking system (VMS, Delaval, Sweden). The multiparous cows were dried off in their previous lactation to achieve an average dry period of 55 d, during which they were offered wheat straw (ad libitum), 7 kg DM of corn silage, 1.4 kg DM of soybean meal, 25 g of magnesium oxide (Nutreco, Ghent, Belgium) and 200 g of dry period mineral mixture (Runergreen, P5, Nutreco, Ghent, Belgium) per day until 20 d (±3.5 SD) before the calving date. For the last 20 d the animals were transferred to the lactating group in order to adapt to the ration offered to the cows after calving. Similarly, the primiparous cows were transferred to the lactating group 19 d (±3 SD) before their actual calving date. Cows received a partially mixed ration ad libitum balanced for net energy and digestible protein with 2 (CON) or 3 (ALG) types of concentrates (Table 1). The CON group was offered 2 kg/d of balanced concentrate (Glucolac 21® , AVEVE Group, Merksem, Belgium) from 14 d prior to parturition. After parturition, the amount of

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Table 1 Ingredient composition of the post partum ration. Partially mixed ration (g/kg DM) Corn silage Grass silage Soybean meal Sugar beet Corn cob mix Hay Minerals Balanced concentrate

Ad libitum 532 242 100 45 57 20 4 Up to 3 and 6 kg/d for primiparous and multiparous cows respectively 2 kg/d

Protein corrector concentrate

balanced concentrate increased over 20 d leading to a maximum of 3 kg/d for primiparous and 6 kg/d for multiparous cows. Next to the balanced concentrate, after parturition, a protein corrector (Aminolac 38 Extra® , AVEVE Group, Merksem, Belgium) was offered at a constant amount of 2 kg/d to all animals. The ALG group was fed according to the same protocol as the CON. The algae concentrate contained 110 g/kg DHA-Gold (Martek DHA gold® , Martek Biosciences Corp., Colombia, MD) (Table 2). Supplementation of the ALG concentrate started 3 weeks before expected calving date at a rate of 1.8 kg/d (202 g of DHAGold, corresponding to 40 g of DHA) and remained at 2 kg/d (224 g of DHA-Gold, 44 g of DHA) throughout the entire post partum period (46 d). 2.2. Plasma samples and analyses Blood samples were collected by jugular vein puncture at the day of parturition (week 0) and at −1, 2, 4 and 6 weeks relative to calving into tubes containing ethylenediaminetetraaceticacid (EDTA) as an anticoagulant. Samples were centrifuged (10 min; 1500 × g) and plasma was stored at −20 ◦ C until analysis. The following parameters related to oxidative status were measured: ferric reducing ability of plasma (FRAP), ␣-tocopherol level, glutathione Table 2 Chemical composition (g/kg DM) and fatty acid composition (%FAME) of DHA-Gold (Schizochytrium sp.). DHA-Gold (Schizochytrium sp.) ADF NDF Crude fibre Crude protein Crude fat 14:0 16:0 18:0 18:1 c9 + c11 + t10 + t11 18:2 n-6 18:3 n-3 20:5 n-3 22:6 n-3 SFA MUFA PUFA Total fatty acids (g/kg DM) a

n.d. = not detected.

250 n.d.a n.d. 102 581 10.1 26.3 0.93 1.05 0.32 0.17 0.04 37.8 38.7 1.67 40.5 523

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Table 3 Mean values of oxidative status markers in dairy cow plasma according to week and dietary treatment. Week peripartum

FRAP (nmol Fe2+ /ml) ␣-Tocopherol (␮g/ml) GSH-Px (Ua )

Treatment

P-Value

−1

0

2

4

6

CON

ALG

RMSE

Week peripartum

Treatment

263ab 3.27a 0.077

274ab 1.97b 0.089

257a 2.76b 0.109

266ab 3.21a 0.094

284b 3.61a 0.093

264 2.78 0.103

274 2.91 0.082

31.6 0.859 0.036

0.009 <0.001 0.066

0.266 0.634 0.130

b

Means within a row with different letters (a and b) differ (P < 0.01). a U = amount of enzyme needed to oxidize 1 ␮mol NADPH/min/ml. b RMSE = root mean square error.

peroxidase activity (GSH-Px) and thiobarbituric acid reactive substances (TBARS). The FRAP method is used to measure the total antioxidative capacity of plasma, results representing the non-enzymatic antioxidative systems (Benzie and Strain, 1996). The method is based on the conversion of Fe3+ tripyridyltriazine to Fe2+ -tripyridyltriazine by antioxidants present in the plasma resulting in the formation of a blue colour. The absorbance was kinetically followed at 593 nm and 37 ◦ C and the end-point was taken at 20 min. Using a calibration curve of Fe2+ , FRAP values were calculated and expressed in nmol Fe2+ formed per ml plasma. The ␣-tocopherol content, as a non-enzymatic low molecular weight antioxidant, was determined according to the method of Desai (1984). After saponification and hexane extraction, samples were analyzed by reversed phase HPLC on a Supelcosil LC 18 column (25 cm × 4.6 mm × 5 ␮m) following UV detection at 292 nm. The eluting solvent was methanol/water (97/3, v/v) at a flow rate of 2 ml/min. The results are expressed as ␮g/ml plasma. GSH-Px is an endogenous enzyme involved in the reduction of H2 O2 and hydroperoxides. It’s plasma activity was determined by kinetically measuring the oxidation of NADPH at 340 nm and 37 ◦ C in the presence of reduced glutathione and H2 O2 (Devore and Greene, 1982), and is expressed as units (U) with one unit being equivalent to the amount of enzyme needed to oxidize 1 ␮mol NADPH/min/ml plasma. The global lipid oxidation was determined by the TBARS method, in which the absorbance of a coloured complex that is formed from the reaction of malondialdehyde (MDA) with 2-thiobarbituric acid (2-TBA) in acid environment, is measured at 532 nm (De Vos and De Schrijver, 2003). It is expressed in eq nmol MDA/ml plasma. 2.3. Additional data and statistics Data on milk yield, energy balance, and measurements of metabolic and reproductive parameters are reported elsewhere (Hostens et al., 2009; Vlaeminck et al., 2009). Here, some results on production and energy parameters are reported in order to investigate the relationship with the oxidative status. Statistical analysis of the oxidative status parameters was performed using the Linear Mixed Models procedure of SPSS for windows version 15.0. The mixed model included the fixed effects of sampling week and treatment, and animal as random effect. There were no significant 2-way

interaction terms between the fixed effects. Comparison of means was performed using the Bonferonni post hoc test. The correlations between the residuals of the models were calculated with the Pearson’s correlation analysis. Significance and tendency were declared at P < 0.05 and 0.05 < P < 0.1 respectively. 3. Results 3.1. Production and energy parameters The average total roughage intake was similar for both dietary groups (19.4 ± 1.36 kg/d). As expected, the mean milk fat content in the first 6 weeks post partum was lower (P = 0.015) in the ALG group vs. the CON group (31.6 ± 2.33 g/kg vs. 40.7 ± 2.33 g/kg). On the other hand, mean daily milk yield (41.2 ± 1.08 kg/d vs. 38.2 ± 1.08 kg/d), energy corrected milk yield (ECM) (35.8 ± 1.03 kg/d vs. 37.7 ± 1.03 kg/d) and protein content (32.8 ± 0.78 g/kg vs. 34.7 ± 0.78 g/kg) of the ALG vs. the CON group in the first 6 weeks post partum were not affected (NS) by treatment. The plasma and serum metabolic parameters glucose (3.22 ± 0.09 mmol/l vs. 3.42 ± 0.09 mmol/l), non-esterified fatty acids (NEFA) (0.32 ± 0.05 mmol/l vs. 0.31 ± 0.05 mmol/l) and beta-hydroxybutyrate (BHBA) (0.88 ± 0.08 mmol/l vs. 0.73 ± 0.08 mmol/l) were not significantly affected in the ALG vs. the CON group. The body condition score (BCS) did not significantly differ between the ALG (3.02 ± 0.05) and CON group (2.98 ± 0.08, P > 0.05) during the experiment. The BCS was dependent of time relative to calving (P < 0.001). 3.2. Oxidative status indicators Table 3 and Fig. 1 show the effect of time peripartum and ALG supplementation on the mean values of the oxidative status parameters. Week peripartum. The oxidative status parameters FRAP and ␣-tocopherol were significantly affected by sampling time. The total antioxidative capacity of plasma, expressed as FRAP values, was lower at 2 weeks after calving than at 6 weeks after calving (P < 0.01). Plasma ␣-tocopherol concentrations decreased around parturition with a nadir at calving (P < 0.001), thereafter increased again and returned to pre partum levels at 4 weeks after calving. The plasma GSH-Px activity was not significantly affected by sampling time but showed a clear trend to be higher after calving with a peak at 2 weeks post partum. The TBARS level was unaffected (NS) by time in the present study.

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TBARS (eq nmol/ml plasma)

6.5 6 5.5 5 4.5 4 3.5 3 -2

-1

0

1

2

3

4

5

6

7

Week peripartum

Fig. 1. Mean values (standard error bars) of plasma TBARS of periparturient cows fed the control diet (䊉) or the marine algae diet ().

Micro algae supplementation. The mean plasma TBARS level was significantly higher (P < 0.05) in the ALG group compared to the CON group (Fig. 1). Although the overall interaction term was not significant, Fig. 1 shows that the largest difference in plasma TBARS level occurred at the partus (week 0) (P < 0.05). Differences between the two treatment groups were not significant at the other sampling times. 3.3. Relationships between production and metabolic parameters, and antioxidant status indicators Table 4 gives the Pearson correlation coefficients between the residuals of the plasma antioxidant status parameters and the production and metabolic parameters. The residual terms of the linear models were used to account for the fixed effects of the experimental factors. Overall, there were few significant correlation coefficients and all coefficients were below 0.27. The ␣-tocopherol concentration correlated negatively with NEFA and BHBA, and positively with glucose. A positive correlation was also observed between GSH-Px activity and NEFA, and between TBARS and glucose. 4. Discussion The hypothesis tested in the present study was that a supplementation of ALG, used to improve the energy status, might influence the oxidative status of high yielding dairy cows coping with the very stressful transition period. It has been previously reported (Miller and Madsen, 1994; Bernabucci et al., 2005) that the transition period is characterized by an imbalance in the antioxidant status which makes the cows more susceptible to oxidative stress Table 4 Correlation coefficients between plasma antioxidant status indicators and metabolic and production parameters.

Milk (kg/d) ECM (kg/d) Fat (g/d) Protein (g/d) Glucose (mmol/l) NEFA (mmol/l) BHBA (mmol/l) a

FRAP

␣-Tocopherol

GSH-Px

TBARS

NSa NS NS NS NS NS NS

NS NS NS NS 0.23 −0.27 −0.22

NS NS NS NS NS 0.17 NS

NS NS NS NS 0.19 NS NS

NS = not significant (P > 0.05).

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and concomitant diseases. In our study, the lowered plasma total antioxidant capacity (i.e. FRAP) and ␣-tocopherol concentration peripartum, and the higher plasma GSH-Px activity post partum compared to pre partum confirm this finding. The mean plasma ␣-tocopherol concentration was 1.97 ␮g/ml at calving and thus close to or lower than the recommended value of 2 ␮g/ml (Dobbelaar et al., 2010) or 3–3.5 ␮g/ml (Weiss et al., 1997; Weiss, 1998) respectively. Only at 6 weeks post partum, the mean plasma ␣-tocopherol concentration was higher than 3.5 ␮g/ml. The higher TBARS values at parturition further illustrate the occurrence of oxidative stress in the transition period, although this was only apparent on the ALG diet. It should be noted that only a limited number of oxidative stress parameters were assessed in the present study. In addition, the plasma ␣-tocopherol concentration was expressed per millilitre of plasma. Weiss et al. (1992) argued that the ratio of plasma ␣-tocopherol to cholesterol is a better index of the ␣-tocopherol status, since plasma ␣-tocopherol is related to plasma lipids. These authors also observed a strong decrease in plasma cholesterol in the periparturient period, resulting in a more stable ␣-tocopherol concentration over time when expressed on a cholesterol rather than on a volume basis. Depending on the effect of treatment on the plasma cholesterol concentration, treatment effects on the plasma ␣-tocopherol concentration were or were not different when expressed on a cholesterol or volume basis (Weiss et al., 1997, 2009). It is likely that in the present study, the plasma cholesterol concentration also decreased around calving, hence we cannot exclude that much of the decrease in the plasma ␣-tocopherol concentration was related to a reduced plasma lipid content. Nevertheless, the ALG treatment had no effect on the plasma ␣-tocopherol concentration, and we expect this would not change when expressed on a cholesterol basis. Bernabucci et al. (2005) hypothesized a possible relationship between body weight loss and oxidative status. In the present study the negative relationship between ␣-tocopherol and both NEFA and BHBA, and the positive relationship between ␣-tocopherol and glucose, and between GSH-Px and NEFA could support this hypothesis, although the positive relationship between TBARS and glucose does not really fit in this context. In a study on heifers varying in energy balance due to genetic and management factors, Wullepit et al. (2009) also found a weak positive relationship between plasma TBARS and glucose, and weak negative relationships between ␣-tocopherol and both NEFA and BHBA. However, the authors concluded that there were no clear indications that breeding value, milk frequency or feed energy level jeopardized the animals in a way oxidative stress became critical. Also in heifers, Dobbelaar et al. (2010) concluded that a higher BCS was not associated with more oxidative stress and that BCS loss as such did not induce oxidative stress. Whether improving the NEB of periparturient dairy cows could ameliorate their oxidative status needs thus further investigation. As described by Vlaeminck et al. (2009) the experimental conditions were successful in creating a MFD. On the other hand, there were no clear indications (NEFA, BHBA, glucose and BCS) that ALG supplementation diminished the NEB. Staples et al. (1998) and Santos et al. (2008)

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reported that when fat is fed in early lactation, cows often have a lower DMI or an increased milk production, leaving the energy balance unaltered. In the present study the unchanged DMI and lower milk fat content, but nondiminished ECM in the fat-supplemented group, indicate an unaltered EB in early lactation. The latter does not exclude an effect of ALG supplementation on the oxidative status of the transition cow. Indeed, Staples et al. (1998) stated that an effect of supplemental fat is often independent of the energy status of the cow. The present study indicates also a unaltered EB in early lactation but an effect of ALG supplementation on the plasma oxidative status. The plasma ␣-tocopherol concentration remained unchanged when ALG were added to the periparturient diet, whereas plasma FRAP and GSH-Px levels indicated a numerical improvement of the oxidative status. On the other hand, the ALG group showed a significantly higher mean TBARS level, which was most distinct at parturition. This means that ALG supplementation tends to increase lipid peroxidation, and this is especially the case when cows are more susceptible to oxidative stress, e.g. at parturition as was the case in the present study (Fig. 1). It has been reported earlier that high dietary levels of PUFA are a risk for increased susceptibility to oxidative stress, especially when no extra antioxidants are supplemented (Halliwel and Chirico, 1993; Sarkadi-Nagy et al., 2003; Gobert et al., 2009). Other studies (Kesavulu et al., 2002; Barbosa et al., 2003; Iraz et al., 2005) hypothesized a possible relationship between n-3 fatty acids and the reduction of oxidative stress. They reported that n-3 fatty acids (like DHA) might protect tissues from oxygen damage, exert antioxidant enzyme activities and even help to prevent lipid peroxidation. However, these results were obtained from studies with rats and man. It could be that these effects are different in dairy cows, e.g. due to ruminal biohydrogenation. In our study, we found indeed no clear indication that the ALG supplementation could improve the oxidative status of the cows or diminish the susceptibility to oxidative stress around parturition. Otherwise, our data indicate that periparturient dairy cows supplemented with ALG experienced increased global lipid peroxidation, admittedly leaving the other oxidative status parameters roughly unchanged. 5. Conclusion Based on the results of the present study, we can state that by supplementing ALG into the ration of periparturient dairy cows, we were able to create a significant milk fat depression, but could not significantly improve the energy balance. The ALG could not diminish the cows’ susceptibility to oxidative stress in the transition period. On the contrary, they induced, probably through their high PUFA content, more lipid peroxidation. This affirms the recommendations to add antioxidants to PUFA-rich diets of cows in early lactation. Conflict of interest The authors declare that they have no conflicts of interest.

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