Maternal late-gestation metabolic stress is associated with changes in immune and metabolic responses of dairy calves

Tahlia Ling, Marta Hernandez-Jover, Lorraine Sordillo, Angel Abuelo

Research output: Contribution to journalArticle

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Abstract

Metabolic stress in periparturient dairy cows is characterized by excessive lipid mobilization, inflammation, and oxidative stress (OS) that is associated with immune dysfunction. Thus, metabolic stress around the time calving is linked to the development of various early lactation health disorders. Maternal status during late pregnancy can have carry-over effects on several health and production variables of neonatal calves. However, the effects of metabolic stress during gestation on metabolic and immune responses of newborn calves remain unknown. Thus, this study aimed to investigate if metabolic stress in late gestation dairy cows is associated with changes in the metabolic and immune responses of their offspring during the first month of life. Holstein-Friesian cows (N=12) were blood sampled at 28 and 15 d before expected calving. The average between these 2 sampling points in the serum concentrations of non-esterified fatty acids (NEFA), haptoglobin (Hp), and oxidative stress index (OSi) –defined as the ratio between reactive oxygen and nitrogen species (RONS) and total antioxidant potential (AOP)– were calculated as indicators of the degree of lipid mobilization, inflammation, and OS, respectively. Calves were subsequently divided into groups (N=6 each) according to their dams’ high or low degree of lipid mobilization, inflammation, and OS. The metabolic responses of calves in each of these groups were compared weekly throughout their first month of life by assessing serum concentration of NEFA, Hp, and OSi. Additionally, whole blood was obtained from calves at each sampling period and subjected to a lipopolysaccharide (LPS)-stimulated tumor necrosis factor alpha (TNFα) production assay to assess cell-mediated innate immunity against induced inflammatory responses, using high (5 μg/mL of blood) and low (10 ng/mL) concentrations of LPS, at the same weekly intervals. Calves born to cows with higher NEFA or OSi showed lower BW at birth and throughout the study, whilst no association between any of the maternal groups and ADG at 4 wks. of age was identified. Serum concentrations of RONS were higher in calves exposed to higher maternal NEFA concentrations or OSi when compared to calves born to cows with lower values of these biomarkers. Calves exposed to high maternal OS also had higher circulating concentrations of Hp and TNFα, indicating greater basal inflammatory responses when compared to calves born to cows with a lower OSi. In contrast, LPS-induced inflammatory responses were less robust in calves exposed to higher maternal biomarkers of inflammation or OS, suggesting compromised immune responses to microbial agonists. Collectively, these data suggest that prenatal exposure to maternal parameters of metabolic stress may adversely impact some metabolic and inflammatory responses of the offspring that could influence disease susceptibility.
Original languageEnglish
Pages (from-to)6568-6580
Number of pages13
JournalJournal of Dairy Science
Volume101
Issue number7
Early online date02 May 2018
DOIs
Publication statusPublished - Jul 2018

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Physiological Stress
dairy calves
Oxidative Stress
Mothers
oxidative stress
pregnancy
calves
Pregnancy
inflammation
Lipid Mobilization
Haptoglobins
haptoglobins
free fatty acids
Fatty Acids
blood serum
Inflammation
Lipopolysaccharides
Reactive Nitrogen Species
lipopolysaccharides
cows

Cite this

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title = "Maternal late-gestation metabolic stress is associated with changes in immune and metabolic responses of dairy calves",
abstract = "Metabolic stress in periparturient dairy cows is characterized by excessive lipid mobilization, inflammation, and oxidative stress (OS) that is associated with immune dysfunction. Thus, metabolic stress around the time calving is linked to the development of various early lactation health disorders. Maternal status during late pregnancy can have carry-over effects on several health and production variables of neonatal calves. However, the effects of metabolic stress during gestation on metabolic and immune responses of newborn calves remain unknown. Thus, this study aimed to investigate if metabolic stress in late gestation dairy cows is associated with changes in the metabolic and immune responses of their offspring during the first month of life. Holstein-Friesian cows (N=12) were blood sampled at 28 and 15 d before expected calving. The average between these 2 sampling points in the serum concentrations of non-esterified fatty acids (NEFA), haptoglobin (Hp), and oxidative stress index (OSi) –defined as the ratio between reactive oxygen and nitrogen species (RONS) and total antioxidant potential (AOP)– were calculated as indicators of the degree of lipid mobilization, inflammation, and OS, respectively. Calves were subsequently divided into groups (N=6 each) according to their dams’ high or low degree of lipid mobilization, inflammation, and OS. The metabolic responses of calves in each of these groups were compared weekly throughout their first month of life by assessing serum concentration of NEFA, Hp, and OSi. Additionally, whole blood was obtained from calves at each sampling period and subjected to a lipopolysaccharide (LPS)-stimulated tumor necrosis factor alpha (TNFα) production assay to assess cell-mediated innate immunity against induced inflammatory responses, using high (5 μg/mL of blood) and low (10 ng/mL) concentrations of LPS, at the same weekly intervals. Calves born to cows with higher NEFA or OSi showed lower BW at birth and throughout the study, whilst no association between any of the maternal groups and ADG at 4 wks. of age was identified. Serum concentrations of RONS were higher in calves exposed to higher maternal NEFA concentrations or OSi when compared to calves born to cows with lower values of these biomarkers. Calves exposed to high maternal OS also had higher circulating concentrations of Hp and TNFα, indicating greater basal inflammatory responses when compared to calves born to cows with a lower OSi. In contrast, LPS-induced inflammatory responses were less robust in calves exposed to higher maternal biomarkers of inflammation or OS, suggesting compromised immune responses to microbial agonists. Collectively, these data suggest that prenatal exposure to maternal parameters of metabolic stress may adversely impact some metabolic and inflammatory responses of the offspring that could influence disease susceptibility.",
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Maternal late-gestation metabolic stress is associated with changes in immune and metabolic responses of dairy calves. / Ling, Tahlia; Hernandez-Jover, Marta; Sordillo, Lorraine; Abuelo, Angel.

In: Journal of Dairy Science, Vol. 101, No. 7, 07.2018, p. 6568-6580.

Research output: Contribution to journalArticle

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AB - Metabolic stress in periparturient dairy cows is characterized by excessive lipid mobilization, inflammation, and oxidative stress (OS) that is associated with immune dysfunction. Thus, metabolic stress around the time calving is linked to the development of various early lactation health disorders. Maternal status during late pregnancy can have carry-over effects on several health and production variables of neonatal calves. However, the effects of metabolic stress during gestation on metabolic and immune responses of newborn calves remain unknown. Thus, this study aimed to investigate if metabolic stress in late gestation dairy cows is associated with changes in the metabolic and immune responses of their offspring during the first month of life. Holstein-Friesian cows (N=12) were blood sampled at 28 and 15 d before expected calving. The average between these 2 sampling points in the serum concentrations of non-esterified fatty acids (NEFA), haptoglobin (Hp), and oxidative stress index (OSi) –defined as the ratio between reactive oxygen and nitrogen species (RONS) and total antioxidant potential (AOP)– were calculated as indicators of the degree of lipid mobilization, inflammation, and OS, respectively. Calves were subsequently divided into groups (N=6 each) according to their dams’ high or low degree of lipid mobilization, inflammation, and OS. The metabolic responses of calves in each of these groups were compared weekly throughout their first month of life by assessing serum concentration of NEFA, Hp, and OSi. Additionally, whole blood was obtained from calves at each sampling period and subjected to a lipopolysaccharide (LPS)-stimulated tumor necrosis factor alpha (TNFα) production assay to assess cell-mediated innate immunity against induced inflammatory responses, using high (5 μg/mL of blood) and low (10 ng/mL) concentrations of LPS, at the same weekly intervals. Calves born to cows with higher NEFA or OSi showed lower BW at birth and throughout the study, whilst no association between any of the maternal groups and ADG at 4 wks. of age was identified. Serum concentrations of RONS were higher in calves exposed to higher maternal NEFA concentrations or OSi when compared to calves born to cows with lower values of these biomarkers. Calves exposed to high maternal OS also had higher circulating concentrations of Hp and TNFα, indicating greater basal inflammatory responses when compared to calves born to cows with a lower OSi. In contrast, LPS-induced inflammatory responses were less robust in calves exposed to higher maternal biomarkers of inflammation or OS, suggesting compromised immune responses to microbial agonists. Collectively, these data suggest that prenatal exposure to maternal parameters of metabolic stress may adversely impact some metabolic and inflammatory responses of the offspring that could influence disease susceptibility.

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