1. bookVolume 66 (2022): Edizione 2 (June 2022)
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Effect of oxidative status on the occurrence of haemolactia in dairy cows after calving

Pubblicato online: 31 May 2022
Volume & Edizione: Volume 66 (2022) - Edizione 2 (June 2022)
Pagine: 251 - 255
Ricevuto: 04 Jan 2022
Accettato: 12 May 2022
Dettagli della rivista
License
Formato
Rivista
eISSN
2450-8608
Prima pubblicazione
30 Mar 2016
Frequenza di pubblicazione
4 volte all'anno
Lingue
Inglese
Abstract Introduction

Dairy cows may infrequently give milk tinged with blood after calving, which is a condition termed haemolactia. Economic losses for dairy farmers are caused by cases of haemolactia because of the condemnation of such milk, potential contamination of good bulk tank milk with haemolactic milk, and need for veterinarian intervention. This study was performed to elucidate the oxidative status of dairy cows with haemolactia during the peripartum period.

Material and Methods

Plasma glutathione peroxidase, malondialdehyde (MDA) and superoxide dismutase concentrations along with serum vitamin A, C and E concentrations were determined as indices of oxidative stress. The sampled dairy cows comprised two haemolactic (n = 11 and n = 6) and two non-haemolactic (n = 11 and n = 6) groups.

Results

On the first day when haemolactia was identified in colostrum (at mean 2.1 days after parturition), a significantly increased concentration of plasma MDA was noted in the haemolactic group. During the prepartum period, low levels of serum vitamin E were continuously observed from prepartum week 4 to the parturition day but only in the haemolactic group.

Conclusion

These results demonstrate that continuous low levels of serum vitamin E in the prepartum period may play a pivotal role as a requisite factor in the onset of haemolactia after calving.

Keywords

Introduction

After calving, dairy cows occasionally produce blood-tinged milk that is light pinkish to dark reddish in colour; haemolactia is the term for the condition these animals are diagnosed with (3, 5, 7, 11). Haemolactia causes serious economic losses because the discarding of all milk containing blood and protracted veterinary care are necessary and the elimination of risk of the mixture of this milk with acceptable bulk milk must be guaranteed. The pathophysiology of haemolactia involves local or systemic hyperaemia and/or increased blood vessel permeability due to mastitis, trauma or unknown causes (5, 11, 15). However, little information is available on the pathogenesis underlying the mechanism of haemolactia.

According to previous reports (3, 5, 15), haemolactia in dairy cows occurred within one week of parturition, and no marked changes were noted in routine haematology, coagulation, serum chemistry or urinalysis. In humans, increased oxidative stress accompanied by reduced endogenous defences has been reported to play a role in the pathogenesis of several diseases during the pre- and perinatal period (12). Based on this information, we focused on oxidative status during the peripartum period because transition cows are exposed to complicated stress leading to immune dysregulation and inflammation associated with infection and metabolic disorders (10, 17, 19, 23). As plasma or serum indices of oxidative stress, the enzymatic antioxidants glutathione peroxidase (GPx) (8) and superoxide dismutase (SOD) (4), the degradation product malondialdehyde (MDA) (9) from peroxidised lipids and the nonenzymatic antioxidant vitamins A (14), C (21), and E (16, 22) have all been measured. These have been established in dairy cows as biomarkers for evaluating oxidative stress during late pregnancy and early lactation (1, 2, 10, 18, 20).

The aim of the study was to delineate the oxidative status of dairy cows with haemolactia and to detect the sequential changes in oxidative status at the peripartum stage.

Material and Methods

Animals. Dairy cows were reared in stalls on 10 commercial farms (Miyagi, Japan), where incidences of haemolactia occurred. Cows were twice daily fed 6 to 8 kg of feed on a dry matter basis and provided tap water ad libitum.

Criterion of haemolactia. The classification of haemolactia was conducted visually based on the findings of a previous report (11). The cows with haemolactia were divided into three grades by milk appearance as follows: slightly (pale pink milk with trivial to spot-like erythrocyte sediment in centrifugation), moderately (pink milk with thin-layered erythrocyte sediment) or severely (dark red milk with thick-layered erythrocyte sediment) tinged with blood.

Experiments. This study consisted of two experiments (Table 1). In the first experiment (Exp. 1), to delineate the oxidative status of dairy cows with haemolactia, two groups of 11 dairy cows were utilised, one haemolactic and the other non-haemolactic. Examinations were conducted using blood samples collected on the day when haemolactia was first identified in the colostrum, namely between parturition day and 5 days postpartum. Only the cows showing severe haemolactia were assigned to the haemolactic group in this study, because it was expected that there would be considerable fluctuations in oxidative indices. The cows in the non-haemolactic group were selected from the animals with the same parturition day, which was an average of 2 days after parturition, and served as the control group. There were no substantial differences in body weight (haemolactic: 658 ± 12.1 kg vs. non-haemolactic: 658 ± 13.9 kg), body condition score (BCS, haemolactic: 3.36 ± 0.05 vs. non-haemolactic: 3.41 ± 0.06), or parity (haemolactic: 2.6 ± 0.3 vs. non-haemolactic: 2.5 ± 0.3) between the two groups.

Group composition and blood sampling time

Experiment Study group Haemolactia grade Prepartum week Postpartum week
n −4 −2 0 2 4
Haemolactic Severe 11 - - a) - -
Exp. 1 Non-haemolactic - 11 - - a) - -

Haemolactic Moderate 6 b)
Exp. 2 Non-haemolactic - 6 b)

Moderate grade: pinkish milk with thin-layered erythrocyte sediment

Severe grade: dark reddish milk with thick-layered erythrocyte sediment

〇 – blood collection; - – no blood collection; a) – on the day when haemolactia was found; b) – on parturition day

In the second experiment (Exp. 2), to detect the sequential changes in oxidative status at the peripartum stage, 20 pregnant dairy cows were registered in prepartum week 5. The expected delivery date was determined from the date of artificial insemination. Their milk after calving was graded as non- (n = 9), slightly (n = 3), moderately (n = 6) or severely (n = 2) haemolactic. The six cows with moderate haemolactia were selected for this study because of the limited number of cows with severe haemolactia. Six of the nine cows in the non-haemolactic group were selected randomly as the corresponding control. There were no large differences in body weight (haemolactic: 700 ± 7.3 kg vs. non-haemolactic: 708 ± 9.8 kg), BCS (haemolactic: 3.50 ± 0.06 vs. non-haemolactic: 3.46 ± 0.08) or parity (haemolactic: 2.3 ± 0.3 vs. non-haemolactic: 1.8 ± 0.4) between the two groups. The same oxidative indices as in Exp. 1 were measured five times (in prepartum weeks 4 and 2, on the parturition day and at postpartum weeks 2 and 4) during the peripartum period.

Cows showing mastitis or trauma were excluded from the study based on the results of a modified California mastitis test (PLT; ZENOAQ, Fukushima, Japan) and macroscopic examination of milk, teats and udder. Cows diagnosed with hypocalcaemia, ketosis, fatty liver or abomasal displacement were also excluded.

Blood collection and analysis of oxidative indices. Individual blood samples were collected from the caudal vein and transported to the laboratory in ice boxes shortly after collection. The plasma levels of GPx, MDA (assay wavelength: 532 nm) and SOD were determined using commercially available kits (Northwest Life Science Specialties, Vancouver, WA, USA). Retinol (vitamin A), α-tocopherol (vitamin E) and ascorbic acid (vitamin C) serum levels were quantified using reversed-phase high performance liquid chromatography and ion pair reversed phase high performance liquid chromatography methods and a Prominence chromatograph (Shimadzu, Kyoto, Japan).

Statistical analysis. Numerical data are expressed as the mean ± standard error of the mean (SEM). Statistical evaluation was performed using Student’s t-test or repeated-measures analysis of variance with Free EZR version 1.40 (Saitama Medical Centre, Jichi Medical University, Saitama, Japan). Statistical significance was set at P < 0.05.

Results

In Exp. 1, in which the experimental cows were severely haemolactic, the time identified as the first incidence of haemolactia in the colostrum was 2.1 ± 0.5 days after parturition. The average plasma MDA value on the day of onset significantly increased in the haemolactic group (4.63 ± 0.28 μmol/L) compared to that in the non-haemolactic group (3.12 ± 0.23 μmol/L) without any changes in GPx, SOD or vitamin levels (A, C and E) in plasma or serum (Fig. 1).

Fig. 1

Changes in plasma or serum indices of oxidative stress in dairy cows with haemolactia (solid grey column, n = 11) or without haemolactia (void column, n = 11) after calving

Upper bars – maxima; lower bars – minima; horizontal bars through boxes – medians; GPx – glutathione peroxidase; MDA – malondialdehyde; SOD – superoxide dismutase. ** – P < 0.01 vs. non-haemolactic group

In Exp. 2, in which the experimental cows were moderately haemolactic, low levels of serum vitamin E were observed continuously from prepartum week 4 to the parturition day in the haemolactic group (mean range: 150–200 μg/dL vs. non-haemolactic group: 290– 310 μg/dL) without any changes in plasma MDA value. Alterations in plasma GPx, SOD and vitamin A serum were noted sporadically throughout the observation period (Fig. 2).

Fig. 2

Changes in plasma or serum indices of oxidative stress in dairy cows with haemolactia (solid circles, n = 6) or without haemolactia (void circles, n = 6) during the peripartum period. Values are expressed as the mean ± standard error of the mean. * – P < 0.05 and ** – P < 0.01 vs. non-haemolactic group; GPx – glutathione peroxidase; MDA – malondialdehyde; SOD – superoxide dismutase

Discussion

The onset day of haemolactia after calving was highly consistent with the day stated in previous reports (5, 15). Differences in fluctuations of MDA and vitamin E levels were found between Exp. 1 and Exp. 2; however, these may relate to some extent to dietary provision. Vitamin E serum levels decreased only in the prepartum period of Exp. 2 but did not during the postpartum period of this experiment or Exp. 1. This may be partially explained by the reduced intake of dietary vitamin E in the prepartum period (3), followed by adaptive response of vitamin E (recovery from a deficient level to the control level with increased feed intake) to MDA overproduction immediately after calving in Exp. 1. However, further studies are required to determine this difference. The clinical importance of the sporadic changes in plasma GPx and SOD levels and serum vitamin A in Exp. 2 remains unknown.

The present data and data from previous reports (3, 9, 15, 16, 22) imply the same underlying pathophysiological process. Vitamin E is a requisite element of the nutritional regimens that meet the antioxidant requirements of dairy cows, especially in the peripartum period (3, 16, 22). Several reports suggest vitamin E at the recommended level enhances the host’s defence against metabolic diseases and confers protection against them to transition cows (1, 6, 16, 22). Considering that gestation or parturition is accompanied by the high energy demand of various bodily functions with an increased oxygen requirement (13), deteriorated levels (i.e. continuously decreased vitamin E) of antioxidant capacity during the prepartum period followed by additional oxidative stress due to parturition may contribute to the development of lipid peroxidation (increased MDA). The overproduction of MDA has been reported to increase the risk of oxidative stress (1, 3, 9), which may be a mediator of endothelial dysfunction. Retrospective surveillance of dairy cows with haemolactia in Japan (15) by microscopy found that of two indicia, namely increases in mammary epithelial cells (including their cell debris) and neutrophils and blood clots in the milk sediment, the former was more extensive in severe cases, presumably because of epithelial damage to the mammary gland. Therefore, continuously low levels of serum vitamin E in the prepartum period appear to play a key role in the onset of haemolactia.

Recently, it was reported that the calculation of the relative ratio of blood oxidants (MDA) to antioxidants can provide a more accurate representation of the redox status (balance) in the transition period of dairy cows (1, 2). Among the ratios calculated in this study, only the MDA/vitamin E ratio (×100) significantly increased from the prepartum period (Exp. 2 haemolactic group: mean range 3.21–3.88 vs. non-haemolactic group: 1.88–1.95, P < 0.05) to the day when haemolactia was identified (Exp. 1 haemolactic group: 1.18 ± 0.10 vs. non-haemolactic group: 0.74 ± 0.07, P < 0.01). Observable high MDA/vitamin E ratios during the peripartum period may be useful in the profiling of the pathophysiological process (such as continual redox imbalance) in haemolactia after calving.

In conclusion, it is suggested that continuously low levels of serum vitamin E in the prepartum period may play a pivotal role as a requisite factor in the onset of haemolactia, and that high MDA levels in plasma after calving may reflect at least in part the degraded physiological status of the mammary gland. Further studies are necessary to determine whether an appropriate vitamin E-supplemented diet during the prepartum period would prevent the onset of haemolactia after calving.

Fig. 1

Changes in plasma or serum indices of oxidative stress in dairy cows with haemolactia (solid grey column, n = 11) or without haemolactia (void column, n = 11) after calving
Upper bars – maxima; lower bars – minima; horizontal bars through boxes – medians; GPx – glutathione peroxidase; MDA – malondialdehyde; SOD – superoxide dismutase. ** – P < 0.01 vs. non-haemolactic group
Changes in plasma or serum indices of oxidative stress in dairy cows with haemolactia (solid grey column, n = 11) or without haemolactia (void column, n = 11) after calving Upper bars – maxima; lower bars – minima; horizontal bars through boxes – medians; GPx – glutathione peroxidase; MDA – malondialdehyde; SOD – superoxide dismutase. ** – P < 0.01 vs. non-haemolactic group

Fig. 2

Changes in plasma or serum indices of oxidative stress in dairy cows with haemolactia (solid circles, n = 6) or without haemolactia (void circles, n = 6) during the peripartum period. Values are expressed as the mean ± standard error of the mean. * – P < 0.05 and ** – P < 0.01 vs. non-haemolactic group; GPx – glutathione peroxidase; MDA – malondialdehyde; SOD – superoxide dismutase
Changes in plasma or serum indices of oxidative stress in dairy cows with haemolactia (solid circles, n = 6) or without haemolactia (void circles, n = 6) during the peripartum period. Values are expressed as the mean ± standard error of the mean. * – P < 0.05 and ** – P < 0.01 vs. non-haemolactic group; GPx – glutathione peroxidase; MDA – malondialdehyde; SOD – superoxide dismutase

Group composition and blood sampling time

Experiment Study group Haemolactia grade Prepartum week Postpartum week
n −4 −2 0 2 4
Haemolactic Severe 11 - - a) - -
Exp. 1 Non-haemolactic - 11 - - a) - -

Haemolactic Moderate 6 b)
Exp. 2 Non-haemolactic - 6 b)

Abuelo A., Hernández J., Benedito J.L., Castillo C.: The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation. J Anim Physiol Anim Nutr 2015, 99, 1003–1016, doi: 10.1111/jpn.12273. Abuelo A. Hernández J. Benedito J.L. Castillo C. The importance of the oxidative status of dairy cattle in the periparturient period: revisiting antioxidant supplementation J Anim Physiol Anim Nutr 2015 99 1003 1016 doi 10.1111/jpn.12273Apri DOISearch in Google Scholar

Abuelo A., Hernández J., Benedito J.L., Castillo C.: Redox biology in transition periods of dairy cattle: role in the health of periparturient and neonatal animals. Antioxidants 2019, 8, 20, doi:10.3390/antiox8010020. Abuelo A. Hernández J. Benedito J.L. Castillo C. Redox biology in transition periods of dairy cattle: role in the health of periparturient and neonatal animals Antioxidants 2019 8 20 doi10.3390/antiox8010020Apri DOISearch in Google Scholar

Bani Ismail Z., Abutarbush S.M., Al-Qudah K., Omoush F.: Serum and milk concentrations of oxidant and anti-oxidant markers in dairy cows affected with bloody milk. Pol J Vet Sci 2020, 23, 341–347, doi: 10.24425/pjvs.2020.133651. Bani Ismail Z. Abutarbush S.M. Al-Qudah K. Omoush F. Serum and milk concentrations of oxidant and anti-oxidant markers in dairy cows affected with bloody milk Pol J Vet Sci 2020 23 341 347 doi 10.24425/pjvs.2020.133651Apri DOISearch in Google Scholar

Bernabucci U., Ronchi B., Lacetera N., Nardone A.: Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows. J Dairy Sci 2005, 88, 2017–2026, doi: 10.3168/jds. S0022-0302(05)72878-2. Bernabucci U. Ronchi B. Lacetera N. Nardone A. Influence of body condition score on relationships between metabolic status and oxidative stress in periparturient dairy cows J Dairy Sci 2005 88 2017 2026 doi 10.3168/jds.S0022-0302(05)72878-2Apri DOISearch in Google Scholar

Blood D.C., Radostits O.M.: Veterinary medicine Seventh Edition, Bailliere Trindall, London, UK, 1989. Blood D.C. Radostits O.M. Veterinary medicine Seventh Edition Bailliere Trindall London, UK 1989Search in Google Scholar

Bouwstra R.J., Nielen M., Stegeman J.A., Dobbelaar P., Newbold J.R., Jansen E.H.J.M., van Werven T.: Vitamin E supplementation during the dry period in dairy cattle. Part I: Adverse effect on incidence of mastitis postpartum in a double-blind randomized field trial. J Dairy Sci 2010, 93, 5684–5695, doi: 10.3168/jds.2010-3159. Bouwstra R.J. Nielen M. Stegeman J.A. Dobbelaar P. Newbold J.R. Jansen E.H.J.M. van Werven T. Vitamin E supplementation during the dry period in dairy cattle. Part I: Adverse effect on incidence of mastitis postpartum in a double-blind randomized field trial J Dairy Sci 2010 93 5684 5695 doi 10.3168/jds.2010-315921094740Apri DOISearch in Google Scholar

Bradford P.S.: Large animal internal medicine Third Edition, Mosby, Maryland Heights, MO, 2001. Bradford P.S. Large animal internal medicine Third Edition Mosby, Maryland Heights, MO 2001Search in Google Scholar

Castillo C., Hernández J., Bravo A., López-Alonso M., Pereira V., Benedito J.L.: Oxidative status during late pregnancy and early lactation in dairy cows. Vet J 2005, 169, 286–292, doi: 10.1016/j.tvjl.2004.02.001. Castillo C. Hernández J. Bravo A. López-Alonso M. Pereira V. Benedito J.L. Oxidative status during late pregnancy and early lactation in dairy cows Vet J 2005 169 286 292 doi 10.1016/j.tvjl.2004.02.00115727923Apri DOISearch in Google Scholar

Castillo C., Hernández J., Valverde I., Pereira V., Sotillo J., López-Alonso M., Benedito J.L.: Plasma malonaldehyde (MDA) and total antioxidants status (TAS) during lactation in dairy cows. Res Vet Sci 2006, 80, 133–139, doi: 10.1016/j.rvsc.2005.06.003. Castillo C. Hernández J. Valverde I. Pereira V. Sotillo J. López-Alonso M. Benedito J.L. Plasma malonaldehyde (MDA) and total antioxidants status (TAS) during lactation in dairy cows Res Vet Sci 2006 80 133 139 doi 10.1016/j.rvsc.2005.06.00316084546Apri DOISearch in Google Scholar

Celi P.: Biomarkers of oxidative stress in ruminant medicine. Immunopharmacol Immunotoxicol 2011, 33, 233–240, doi: 10.3109/08923973.2010.514917. Celi P. Biomarkers of oxidative stress in ruminant medicine Immunopharmacol Immunotoxicol 2011 33 233 240 doi 10.3109/08923973.2010.51491720849293Apri DOISearch in Google Scholar

Fraile L., Arcas A., Jiménez L.M., Mallo J., Armengol R.: Treatment with etamsylate reduces haemolactia in lactating cows. J Dairy Res 2019, 86, 193–195, doi: 10.1017/S0022029919000219. Fraile L. Arcas A. Jiménez L.M. Mallo J. Armengol R. Treatment with etamsylate reduces haemolactia in lactating cows J Dairy Res 2019 86 193 195 doi 10.1017/S002202991900021931038091Apri DOISearch in Google Scholar

Gitto E., Reiter R.J., Karbownik M., Tan D., Gitto P., Barberi S., Barberi I.: Causes of oxidative stress in the pre- and perinatal period. Biol Neonate 2002, 81, 146–157, doi: 10.1159/000051527. Gitto E. Reiter R.J. Karbownik M. Tan D. Gitto P. Barberi S. Barberi I. Causes of oxidative stress in the pre- and perinatal period Biol Neonate 2002 81 146 157 doi 10.1159/00005152711937719Apri DOISearch in Google Scholar

Goff J.P., Horst R.L.: Physiological changes at parturition and their relationship to metabolic disorders. J Dairy Sci 1997, 80, 1260–1268, doi: 10.3168/jds. S0022-0302(97)76055-7. Goff J.P. Horst R.L. Physiological changes at parturition and their relationship to metabolic disorders J Dairy Sci 1997 80 1260 1268 doi 10.3168/jds.S0022-0302(97)76055-7Apri DOISearch in Google Scholar

Johansson B., Persson Waller K., Jensen S.K., Lindqvist H., Nadeau E.: Status of vitamins E and A and β-carotene and health in organic dairy cows fed a diet without synthetic vitamins. J Dairy Sci 2014, 97, 1682–1692, doi: 10.3168/jds.2013-7388. Johansson B. Persson Waller K. Jensen S.K. Lindqvist H. Nadeau E. Status of vitamins E and A and β-carotene and health in organic dairy cows fed a diet without synthetic vitamins J Dairy Sci 2014 97 1682 1692 doi 10.3168/jds.2013-7388Apri DOISearch in Google Scholar

Kikuchi T., Ichijo T., Yoshida Y., Kohono M., Murayama I., Takahashi C., Kimura Y., Satoh H.: Bloody milk of the dairy cow: occurrence and somatic cell profiles in Miyagi Prefecture. Jpn J Large Anim Clin 2013, 4, 154–159, doi: 10.4190/jjlac.4.154. Kikuchi T. Ichijo T. Yoshida Y. Kohono M. Murayama I. Takahashi C. Kimura Y. Satoh H. Bloody milk of the dairy cow: occurrence and somatic cell profiles in Miyagi Prefecture Jpn J Large Anim Clin 2013 4 154 159 doi 10.4190/jjlac.4.154Apri DOISearch in Google Scholar

Politis I.: Reevaluation of vitamin E supplementation of dairy cows: bioavailability, animal health and milk quality. Animal 2012, 6, 1427–1434, doi: 10.1017/S1751731112000225. Politis I. Reevaluation of vitamin E supplementation of dairy cows: bioavailability, animal health and milk quality Animal 2012 6 1427 1434 doi 10.1017/S1751731112000225Apri DOISearch in Google Scholar

Putman A.K., Brown J.L., Gandy J.C., Wisnieski L., Sordillo L.M.: Changes in biomarkers of nutrient metabolism, inflammation, and oxidative stress in dairy cows during the transition into the early dry period. J Dairy Sci 2018, 101, 9350– 9359, doi: 10.3168/jds.2018-14591. Putman A.K. Brown J.L. Gandy J.C. Wisnieski L. Sordillo L.M. Changes in biomarkers of nutrient metabolism, inflammation, and oxidative stress in dairy cows during the transition into the early dry period J Dairy Sci 2018 101 9350 9359 doi 10.3168/jds.2018-14591Apri DOISearch in Google Scholar

Senoh T., Oikawa S., Nakada K., Tagami T., Iwasaki T.: Increased serum malondialdehyde concentration in cows with subclinical ketosis. J Vet Med Sci 2019, 81, 817–820, doi: 10.1292/jvms.18-0777. Senoh T. Oikawa S. Nakada K. Tagami T. Iwasaki T. Increased serum malondialdehyde concentration in cows with subclinical ketosis J Vet Med Sci 2019 81 817 820 doi 10.1292/jvms.18-0777Apri DOISearch in Google Scholar

Sordillo L.M., Raphael W.: Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders. Vet Clin North Am Food Anim Pract 2013, 29, 267–278, doi: 10.1016/j.cvfa.2013.03.002. Sordillo L.M. Raphael W. Significance of metabolic stress, lipid mobilization, and inflammation on transition cow disorders Vet Clin North Am Food Anim Pract 2013 29 267 278 doi 10.1016/j.cvfa.2013.03.002Apri DOISearch in Google Scholar

Tsuchiya Y., Kawahara N., Kim Y.-H., Ichijo T., Sato S.: Changes in oxidative stress parameters in healthy and diseased Holstein cows during the transition period in Yamagata Prefecture, Japan. J Vet Med Sci 2020, 82, 955–961, doi: 10.1292/jvms.20-0024. Tsuchiya Y. Kawahara N. Kim Y.-H. Ichijo T. Sato S. Changes in oxidative stress parameters in healthy and diseased Holstein cows during the transition period in Yamagata Prefecture, Japan J Vet Med Sci 2020 82 955 961 doi 10.1292/jvms.20-0024Apri DOISearch in Google Scholar

Weiss W.P., Hogan J.S.: Effects of dietary vitamin C on neutrophil function and responses to intramammary infusion of lipopolysaccharide in periparturient dairy cows. J Dairy Sci 2007, 90, 731–739, doi: 10.3168/jds. S0022-0302(07)71557-6. Weiss W.P. Hogan J.S. Effects of dietary vitamin C on neutrophil function and responses to intramammary infusion of lipopolysaccharide in periparturient dairy cows J Dairy Sci 2007 90 731 739 doi 10.3168/jds.S0022-0302(07)71557-6Apri DOISearch in Google Scholar

Weiss W.P., Hogan J.S., Todhunter D.A., Smith K.L.: Effect of vitamin E supplementation in diets with a low concentration of selenium on mammary gland health of dairy cows. J Dairy Sci 1997, 80, 1728–1737, doi: 10.3168/jds. S0022-0302(97)76105-8. Weiss W.P. Hogan J.S. Todhunter D.A. Smith K.L. Effect of vitamin E supplementation in diets with a low concentration of selenium on mammary gland health of dairy cows J Dairy Sci 1997 80 1728 1737 doi 10.3168/jds.S0022-0302(97)76105-8Apri DOISearch in Google Scholar

Zobel G., Weary D.M., Leslie K.E., von Keyserlingk M.A.G.: Invited review: cessation of lactation: effects on animal welfare. J Dairy Sci 2015, 98, 8263–8277, doi: 10.3168/jds.2015-9617. Zobel G. Weary D.M. Leslie K.E. von Keyserlingk M.A.G. Invited review: cessation of lactation: effects on animal welfare J Dairy Sci 2015 98 8263 8277 doi 10.3168/jds.2015-961726409963Apri DOISearch in Google Scholar

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