Influence of management and lactation order in the serum concentrations of proteins, metabolites, minerals, and enzymes of Bonsmara breed cows

Fernando Cristino Barbosa Wilson Junior Oliveira João Gabriel Knychala Faria Felipe Cesar Gonçalves Ednaldo Carvalho Guimarães Antonio Vicente Mundim About the authors

Abstract

This study aimed to evaluate the influence of gestation and lactation order on serum concentrations of proteins, metabolites, minerals, and enzymes in first-, second-, and third-lactation order Bonsmara cows. The Bonsmara breed, originated in South Africa, stands out for its tolerance to heat and productive characteristics, such as meat quality, high fertility, sexual precocity, ease of calving, and good maternal ability. These characteristics make the breed a genetic alternative for crossbreeding with zebu breeds. Blood samples were collected from 34, 29, and 30 first-, second-, and third-lactation order cows, respectively, totaling 93 cows. The samples were processed in an automatic multichannel analyzer using Labtest Diagnóstica® kits. The Kruskal-Wallis test was chosen to compare the values between lactation orders. The Mann-Whitney test was used to compare pregnant and non-pregnant cows within lactation orders. Among the analyzed constituents, the lactation order significantly influenced only the serum albumin concentration (ALB) (p<0.0001). Gestation significantly influenced the A:G ratio (p=0.034) in third-lactation cows, and cholesterol (Chol) (p=0.004), triglycerides (TRI) (p<0.0001), inorganic phosphorus (iP) (p=0.033), iron (Fe) (p=0.001), aspartate aminotransferase (AST) (p=0.018), and alkaline phosphatase (ALP) (p=0.039) in second-lactation cows and the general group. Creatinine (Crea) (p<0.0001) was influenced only in the general group. Therefore, gestation and lactation order significantly influenced the concentration of several biochemical serum constituents in Bonsmara cows, especially second-lactation order cows.

Keywords:
Beef cattle; Production phases; Serum biochemistry; Metabolic profile

RESUMO

Objetivou-se avaliar a influência da gestação e ordem de lactação nas concentrações séricas de proteínas, metabólitos, minerais e enzimas de vacas da raça Bonsmara de primeira, segunda e terceira ordem de lactação. A raça Bonsmara, originada na África do Sul, se destaca por sua tolerância ao calor, e caracteristicas produtivas, como a qualidade da carne, a alta fertilidade, precocidade sexual, facilidade ao parto e boa habilidade materna. Essas características tornam a raça uma alternativa genética para realização de cruzamentos com raças zebuínas. Foram colhidas amostras de sangue de 93 vacas, sendo 34 de primeira ordem de lactação, 29 de segunda ordem de lactação e 30 de terceira ordem de lactação. As amostras foram processadas em analisador automático multicanal, utilizando kits da Labtest Diagnóstica®. Para confrontar os valores entre as ordens de lactação optou-se pelo teste Kruskall-Wallis. Para comparar vacas gestantes e não gestantes dentro das ordens de lactação, foi utilizado o teste de Mann-Whitney. Dos constituintes analisados, a ordem de lactação influenciou significativamente apenas a concentração sérica de albumina (ALB) (p<0,0001). A gestação influenciou significativamente na relação A:G (p=0,034), nas vacas de terceira lactação, no colesterol (COL) (p=0,004), triglicérides (TRI) (p<0,0001), fósforo inorgânico (Pi) (p=0,033), ferro (Fe) (p=0,001), aspartato aminotransferase (AST) (p=0,018) e fosfatase alcalina (FAL) (p=0,039) nas de segunda ordem e no valor do grupo geral. A creatinina (Crea) (p<0,0001) foi influenciada somente no grupo geral. Conclui-se que a gestação e ordem de lactação influenciou significativamente na concentração de vários constituintes bioquímicos séricos de vacas da raça Bonsmara, em especial nas de segunda ordem de lactação.

Palavras-chave:
Bovino de corte; Fases de produção; Bioquímica sérica; Perfil metabólico

Introduction

The serum biochemical profile provides information on the normal values of a breed and can be used as an indicator of the organism’s adaptive processes to nutritional and physiological challenges, specific metabolic and imbalances, and imbalances in energy, protein, and mineral metabolism.(11 González FHD, Scheffer JFS. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. In: González FHD, Campos R. Anais do I Simpósio de Patologia Clínica Veterinária da Região Sul do Brasil. Porto Alegre: Gráfica da Universidade Federal do Rio Grande do Sul, 2003. p.73-89. Disponível em: https://www.lume.ufrgs.br/bitstream/handle/10183/ 13177/000386508.pdf.
https://www.lume.ufrgs.br/bitstream/hand...
, 22 Puppel K, Kuczyńska B. Metabolic profiles of cow's blood; a review. Journal of the Science of Food and Agriculture. 2016;96(13):4321-4328. https://doi.org/10.1002/jsfa.7779 .
https://doi.org/10.1002/jsfa.7779...
) The interpretation of the serum biochemical profile is complex due to the mechanisms that control the blood concentrations of various metabolites and their high variation according to several factors, such as breed, age, stress, diet, management, climate, and physiological state (gestation and lactation).(11 González FHD, Scheffer JFS. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. In: González FHD, Campos R. Anais do I Simpósio de Patologia Clínica Veterinária da Região Sul do Brasil. Porto Alegre: Gráfica da Universidade Federal do Rio Grande do Sul, 2003. p.73-89. Disponível em: https://www.lume.ufrgs.br/bitstream/handle/10183/ 13177/000386508.pdf.
https://www.lume.ufrgs.br/bitstream/hand...
, 33 Otto F, Vilela F, Harun M, Taylor M, Baggasse P, Bogin E. Biochemical blood profile of Angoni cattle in Mozambique. Israel Journal of Veterinary Medicine. 2000;55(3):95-102. https://pdfs.semanticscholar.org/b007/bd6f653bbb194209b889271bf024ce842003.pdf?_ga=2.1798327.74392992.1564689619-48519492.1558912057 .
https://pdfs.semanticscholar.org/b007/bd...
)

The Bonsmara breed, originated in South Africa from the genetic combination of 5/8 Afrikaner, 3/16 Shorthorn, and 3/16 Hereford by researcher Prof. Jan Bonsma, was introduced in Brazil in 1997.(44 Strydom PE. Do indigenous Southern African cattle breeds have the right genetics for commercial production of quality meat? Meat Science. 2008;80(1):86-93. https://doi.org/10.1016/j.meatsci.2008.04.017
https://doi.org/10.1016/j.meatsci.2008.0...
) The productive characteristics, including its meat quality, are more similar to Bos taurus than to zebu breeds.(55 Strydom PE, Naude RT, Smith MF, Scholtz MM, Van Wyk JB. Characterisation of indigenous African cattle breeds in relation to meat quality traits. Meat Science. 2000;55(1):79-88. https://doi.org/10.1016/S0309-1740(99)00128-X
https://doi.org/10.1016/S0309-1740(99)00...
) These characteristics make the Bonsmara breed a genetic alternative for crossbreeding with Zebu breeds.

Physiological changes occur during gestation and lactation, increasing nutritional needs to support fetal growth and development, as well as maternal metabolism and the development of specific tissues for reproduction.(66 Pogliani FC, Azedo MR, Souza RM, Raimundo RFS, Birgel Junior EH. Influência da gestação e do puerpério no lipidograma de bovinos da raça holandesa. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2010;62(2):273-280. http://dx.doi.org/10.1590/S0102-09352010000200005
http://dx.doi.org/10.1590/S0102-09352010...
, 77 Piccione G, Messina V, Marafioti S, Casella S, Giannetto C, Fazio F. Changes of some haematochemical parameters in dairy cows during late gestation, post partum, lactation and dry periods. Veterinarija ir Zootechnika. 2012;58(80):59-64. https://vetzoo.lsmuni.lt/data/vols/ 2012/58/pdf/piccione.pdf.
https://vetzoo.lsmuni.lt/data/vols/ 2012...
) A higher development of placental, fetal, glandular, and mammary tissues occurs in the final third of gestation, contributing to increased energy demand.(77 Piccione G, Messina V, Marafioti S, Casella S, Giannetto C, Fazio F. Changes of some haematochemical parameters in dairy cows during late gestation, post partum, lactation and dry periods. Veterinarija ir Zootechnika. 2012;58(80):59-64. https://vetzoo.lsmuni.lt/data/vols/ 2012/58/pdf/piccione.pdf.
https://vetzoo.lsmuni.lt/data/vols/ 2012...
) Lactation is a physiological state in which adaptations in metabolism occur. Early lactation imposes severe metabolic changes, which challenge the organism to maintain a homeostatic balance to compensate for the expenditure of nutrients that lactogenesis requires.(88 Rossato W, Gonzáles FHD, Dias MM, Riccó D, Valle SF, Rosa VLLA, Conceição T, Duarte F, Wald V. Number of lactations affects metabolic profile of dairy cows. Archives of Veterinary Science. 2001;6(2):83-88. Disponível em: www.ufrgs.br/lacvet/restrito/pdf/rossato_numero_lacta_oes.pdf
www.ufrgs.br/lacvet/restrito/pdf/rossato...
) Assessment of the metabolic profile is more relevant during the lactation period, when the animals are more susceptible to metabolic changes, such as at the beginning of lactation, considering herd characteristics, geographic location, and physiological state of the animals.(88 Rossato W, Gonzáles FHD, Dias MM, Riccó D, Valle SF, Rosa VLLA, Conceição T, Duarte F, Wald V. Number of lactations affects metabolic profile of dairy cows. Archives of Veterinary Science. 2001;6(2):83-88. Disponível em: www.ufrgs.br/lacvet/restrito/pdf/rossato_numero_lacta_oes.pdf
www.ufrgs.br/lacvet/restrito/pdf/rossato...
, 99 Brscic M, Cozzi G, Lora I, Stefani AL, Contiero B, Ravarotto L, Gottardo F. Reference limits for blood analytes in Holstein late-pregnant heifers and dry cows: Effects of parity, days relative to calving, and season. Journal of Dairy Science. 2015;98(11):7886-7892. https://doi.org/10.3168/jds.2015-9345 .
https://doi.org/10.3168/jds.2015-9345...
)

Importantly, age, breed, physiological state, stage and order of lactation, individual productivity, climate, and diet reflect changes in the metabolic profile pattern of producing cows.(1010 Freitas Júnior JE, Rennó FP, Silva LFP, Gandra JR, Maturana Filho M, Foditsch C, Venturelli BC. Parâmetros sanguíneos de vacas leiteiras suplementadas com diferentes fontes de gordura. Ciência Rural. 2010;40(4):950-956. http://dx.doi.org/10.1590/S0103-84782010005000039
http://dx.doi.org/10.1590/S0103-84782010...
) Researchers have highlighted the importance of knowing the physiological changes that occur at these stages to avoid misdiagnosis of metabolic, nutritional, and infectious diseases.(1111 Cozzi G, Ravarotto L, Gottardo F, Stefani AL, Contiero B, Moro L, Brscic M, Dalvit P. Reference values for blood parameters in Holstein dairy cows: Effects of parity, stage of lactation, and season of production. Journal of Dairy Science. 2011;94(8):3895-3901. https://doi.org/10.3168/jds.2010-3687 .
https://doi.org/10.3168/jds.2010-3687...
, 22 Puppel K, Kuczyńska B. Metabolic profiles of cow's blood; a review. Journal of the Science of Food and Agriculture. 2016;96(13):4321-4328. https://doi.org/10.1002/jsfa.7779 .
https://doi.org/10.1002/jsfa.7779...
) Thus, considering the importance of knowing the serum biochemistry as a diagnostic tool and the lack of information in the literature regarding the variations in serum biochemical constituents of lactating, pregnant, and non-pregnant Bonsmara cows, this study aimed to evaluate the influence of gestation and lactation order on serum concentrations of proteins, metabolites, minerals, and enzymes in first-, second-, and third-lactation order Bonsmara cows.

Material and methods

The experiment was conducted from November 2018 to March 2019 on a property located in the city of Uberlândia, MG, Brazil, under the coordinates 18°55′0.7″S and 48°16′38″W. Ninety-three cows were divided into three groups according to the lactation order, 34 of which were first-lactation (10 pregnant and 24 non-pregnant), 29 of second-lactation (13 pregnant and 16 non-pregnant), and 30 of third-lactation order (16 pregnant and 14 non-pregnant). Only animals in good nutritional status and considered healthy, which did not present clinical or pathological signs, and a body score between 3 and 4, were included in the study, being monitored by a veterinarian, responsible for the sanitary, zootechnical, and reproductive management of the herd. The animals were maintained in pastures of Brachiaria brizantha cv. Marandu and BRS Piatã, B. ruziziensis, and B. decumbens, with water and mineralized salt ad libitum. They were vaccinated according to the regional sanitary calendar, and the control of ecto-and endoparasites was established according to the monitoring of infestations.

An aliquot of 10 mL of blood was collected from each animal by venipuncture of the middle coccygeal vein, using 25×8 mm needles attached to sterile tubes dried with clot activator (Vacutainer®), always in the morning. After collection, the blood samples were packed in isothermal boxes and transported to the Veterinary Clinical Laboratory of the Federal University of Uberlândia. The samples were immediately centrifuged at 720g for 10 minutes, the obtained serum was transferred in 1.0-mL aliquots to microtubes (Eppendorf®), and frozen at -20 °C for a maximum period of 48 hours until analyses. The samples were processed in a ChemWellTM automated multichannel analyzer previously calibrated (Calibra H®) and measured with universal control serum (Qualitrol®), using commercial kits from Labtest Diagnóstica®. The concentrations of total protein (TP) (biuret method), albumin (ALB) (bromocresol green), creatinine (Crea) (alkaline picrate), urea (UV enzymatic kinetic method), cholesterol (Chol) and triglycerides (TRI) (Trinder enzymatic method), calcium (Ca+) (cresolphthalein complexone - CPC method), inorganic phosphorus (iP) (UV kinetic method), magnesium (Mg) (Magon sulphonate method), iron (Fe) (modified Goodwin method), aspartate aminotransferase (AST), alanine aminotransferase (ALT), and alkaline phosphatase (ALP) (UV kinetic method - IFCC), and gamma-glutamyl transferase (GGT) (modified Szasz method). The globulin (Glob = TP - ALB), albumin to globulin ratio (A:G), and calcium to phosphorus ratio (Ca+:iP) values were calculated.

The data were analyzed by descriptive statistics and subjected to the Levene test to verify homoscedasticity and the Shapiro-Wilk test to verify normality. The medians and non-parametric Kruskal-Wallis test were used to compare the values between lactation orders as the data did not meet these assumptions. Mann-Whitney test at a 5% significance level was used to compare pregnant and non-pregnant cows within lactation orders.

The experiment followed the ethical principles of animal experimentation with approval from the Ethics Committee on the Use of Animals (CEUA) of the Federal University of Uberlândia, according to protocol 053/2018.

Results

The comparison of the serum concentrations of proteins, metabolites, minerals, and enzymes between lactation orders showed that ALB in second-lactation cows was significantly higher than that of first-lactation cows and similar to third-lactation cows. The other evaluated serum constituents did not differ statistically (Table 1).

Table 1
Median (MD), standard error (SE), mean (ME), and standard deviation (SD) of serum concentrations of proteins, metabolites, minerals, and enzymes of first-, second-, and third-lactation order Bonsmara cows, Uberlândia, MG, Brazil

The comparison of serum values of proteins, metabolites, minerals, and enzymes in pregnant and non-pregnant cows within each lactation order showed a higher value of the A:G ratio in pregnant cows in the third lactation. Serum concentrations of Chol, Fe, AST, and ALP in second-lactation pregnant cows were higher than those in non-pregnant ones. TRI and iP values were statistically higher in non-pregnant cows of the same group (Table 2). In the general group, Crea, Chol, Fe, and ALP showed significantly higher values in pregnant cows. TRI and iP showed higher values in non-pregnant cows (Table 2).

Table 2
Median and standard error (MD±SE) of serum concentrations of proteins, metabolites, minerals, and enzymes of pregnant and non-pregnant first-, second-, and third-lactation order Bonsmara cows, Uberlândia, MG, Brazil.

Discussion

The mean values of most of the analyzed constituents for the 93 cows (general group), regardless of being pregnant or not, were within or close to the intervals proposed by Kaneko et al.,(1212 Kaneko JJ, Harvey JW, Bruss ML. Clinical biochemistry of domestic animals. 6. ed. San Diego: Academic Press, 2008. 916p.) except for Glob, Chol, TRI, and ALT, which were above the maximum reference values. Ca+ and iP were slightly below the minimum reference value (Table 1). As the authors did not specify animal age, breed, reproductive status, or management conditions and methodologies used, these variables become imprecise and of little application to diagnose metabolic disorders. The means of TP, Crea, urea, Chol, TRI, Ca+, iP, ALP, and GGT remained within and the means of ALB and AST were slightly above the ranges found by Conceição et al.(1313 Conceição WLF, Brito DRB, Rocha TG, Silva DG, Chaves DP, Fagliari JJ. Perfil bioquímico sérico de vacas das raças Nelore e Girolando criadas no estado do Maranhão. Ciência Animal Brasileira. 2019;20(33796):1-7. https://doi.org/10.1590/1089-6891v20e-33796
https://doi.org/10.1590/1089-6891v20e-33...
) for non-pregnant and non-lactating Nelore and Girolando cows from 24 to 36 months of age raised in the State of Maranhão, Brazil.

The lower ALB value in first lactation cows (p<0.0001) can be explained by the high demand for amino acids necessary for the synthesis of milk proteins(22 Puppel K, Kuczyńska B. Metabolic profiles of cow's blood; a review. Journal of the Science of Food and Agriculture. 2016;96(13):4321-4328. https://doi.org/10.1002/jsfa.7779 .
https://doi.org/10.1002/jsfa.7779...
, 77 Piccione G, Messina V, Marafioti S, Casella S, Giannetto C, Fazio F. Changes of some haematochemical parameters in dairy cows during late gestation, post partum, lactation and dry periods. Veterinarija ir Zootechnika. 2012;58(80):59-64. https://vetzoo.lsmuni.lt/data/vols/ 2012/58/pdf/piccione.pdf.
https://vetzoo.lsmuni.lt/data/vols/ 2012...
) and the high nutritional demand due to the growth phase. According to Rossato et al.,(88 Rossato W, Gonzáles FHD, Dias MM, Riccó D, Valle SF, Rosa VLLA, Conceição T, Duarte F, Wald V. Number of lactations affects metabolic profile of dairy cows. Archives of Veterinary Science. 2001;6(2):83-88. Disponível em: www.ufrgs.br/lacvet/restrito/pdf/rossato_numero_lacta_oes.pdf
www.ufrgs.br/lacvet/restrito/pdf/rossato...
) the number of lactations can influence the serum values of the metabolic profile of cows. However, the serum albumin concentration can be influenced by the protein level in the diet and the reduced synthesis capacity in the liver due to fat accumulation.(11 González FHD, Scheffer JFS. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. In: González FHD, Campos R. Anais do I Simpósio de Patologia Clínica Veterinária da Região Sul do Brasil. Porto Alegre: Gráfica da Universidade Federal do Rio Grande do Sul, 2003. p.73-89. Disponível em: https://www.lume.ufrgs.br/bitstream/handle/10183/ 13177/000386508.pdf.
https://www.lume.ufrgs.br/bitstream/hand...
) The results obtained for ALB and urea show that protein was not a limiting factor, as a protein-deficient diet is characterized by serum albumin levels below 3.0 g/dL and urea levels below 15 mg/dL.(11 González FHD, Scheffer JFS. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. In: González FHD, Campos R. Anais do I Simpósio de Patologia Clínica Veterinária da Região Sul do Brasil. Porto Alegre: Gráfica da Universidade Federal do Rio Grande do Sul, 2003. p.73-89. Disponível em: https://www.lume.ufrgs.br/bitstream/handle/10183/ 13177/000386508.pdf.
https://www.lume.ufrgs.br/bitstream/hand...
) Liver function enzymes are within the physiological ranges for the species, which shows the non-impairment of the liver in these animals. These results corroborate with Alvarenga et al.,(1414 Alvarenga PB, Rezende AL, Justo FB, Rezende SR, Cesar JCG, Santos RM, Mundim AV, Saut JPE. Perfil metabólico de vacas Jersey clinicamente saudáveis. Pesquisa Veterinária Brasileira. 2017;37(2):195-203. http://dx.doi.org/10.1590/s0100-736x2017000200015
http://dx.doi.org/10.1590/s0100-736x2017...
) who found low albumin levels in Holstein and Jersey cows, with no hepatic alterations.

The serum values of Chol and TRI were significantly affected by the physiological state of the animals, with values above those proposed by Kaneko et al.(1212 Kaneko JJ, Harvey JW, Bruss ML. Clinical biochemistry of domestic animals. 6. ed. San Diego: Academic Press, 2008. 916p.) This result may be related to the high demand for regulatory mechanisms involved in all processes of milk synthesis and gestation,(77 Piccione G, Messina V, Marafioti S, Casella S, Giannetto C, Fazio F. Changes of some haematochemical parameters in dairy cows during late gestation, post partum, lactation and dry periods. Veterinarija ir Zootechnika. 2012;58(80):59-64. https://vetzoo.lsmuni.lt/data/vols/ 2012/58/pdf/piccione.pdf.
https://vetzoo.lsmuni.lt/data/vols/ 2012...
, 1515 Obućinski D, Soleša D, Kučević D, Prodanović R, Simin MT, Pelić DL, Đuragić O, Puvača N. Management of blood lipid profile and oxidative status in Holstein and Simmental dairy cows during lactation. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka 2019;69(2):116-124. https://doi.org/10.15567/mljekarstvo.2019.0206.
https://doi.org/10.15567/mljekarstvo.201...
) leading to changes in lipolysis and lipogenesis.(1616 Contreras GA, Strieder-Barboza C, de Koster J. Symposium review: Modulating adipose tissue lipolysis and remodeling to improve immune function during the transition period and early lactation of dairy cows. Journal Dairy Science. 2018;101(3):2737-2752. https://doi.org/10.3168/jds.2017-13340
https://doi.org/10.3168/jds.2017-13340...
) Lipid mobilization from stores in the adipose tissue involves the release of free fatty acids such as triglycerides into the bloodstream.(1616 Contreras GA, Strieder-Barboza C, de Koster J. Symposium review: Modulating adipose tissue lipolysis and remodeling to improve immune function during the transition period and early lactation of dairy cows. Journal Dairy Science. 2018;101(3):2737-2752. https://doi.org/10.3168/jds.2017-13340
https://doi.org/10.3168/jds.2017-13340...
) Despite metabolic variations, serum concentrations of AST and GGT enzymes remained within the ranges considered physiological, possibly characterizing the non-impairment of the liver function. Freitas Júnior et al.(1010 Freitas Júnior JE, Rennó FP, Silva LFP, Gandra JR, Maturana Filho M, Foditsch C, Venturelli BC. Parâmetros sanguíneos de vacas leiteiras suplementadas com diferentes fontes de gordura. Ciência Rural. 2010;40(4):950-956. http://dx.doi.org/10.1590/S0103-84782010005000039
http://dx.doi.org/10.1590/S0103-84782010...
) and Alvarenga et al.(1414 Alvarenga PB, Rezende AL, Justo FB, Rezende SR, Cesar JCG, Santos RM, Mundim AV, Saut JPE. Perfil metabólico de vacas Jersey clinicamente saudáveis. Pesquisa Veterinária Brasileira. 2017;37(2):195-203. http://dx.doi.org/10.1590/s0100-736x2017000200015
http://dx.doi.org/10.1590/s0100-736x2017...
) also observed this condition.

Serum concentrations of Ca+ and iP close to the lower limit established by Kaneko et al.(1212 Kaneko JJ, Harvey JW, Bruss ML. Clinical biochemistry of domestic animals. 6. ed. San Diego: Academic Press, 2008. 916p.) are possibly due to the fact that the cows in the present study were lactating and 39 (42%) were pregnant, showing a higher requirement for these minerals for milk production and fetal development. Grünwaldt et al.(1717 Grünwaldt EG, Guevara JC, Estevez OR, Vicente A, Rousselle H, Alcuten N, Aguerregaray D, Stasi CR. Biochemical and haematological measurements in beef cattle in Mendoza plain rangelands (Argentina). Tropical Animal Health and Production 2005;37(6):527-540. 2005. https://doi.org/10.1007/s11250-005-2474-5 .
https://doi.org/10.1007/s11250-005-2474-...
) also reported lower values of serum calcium in lactating Aberdeen Angus and Argentine Criollo cows. These authors observed serum iP values of 4.34 mg/dL, a value below the physiological range reported by Kaneko et al.,(1212 Kaneko JJ, Harvey JW, Bruss ML. Clinical biochemistry of domestic animals. 6. ed. San Diego: Academic Press, 2008. 916p.) which were attributed to the iP levels in the diet. According to Piccione et al.,(77 Piccione G, Messina V, Marafioti S, Casella S, Giannetto C, Fazio F. Changes of some haematochemical parameters in dairy cows during late gestation, post partum, lactation and dry periods. Veterinarija ir Zootechnika. 2012;58(80):59-64. https://vetzoo.lsmuni.lt/data/vols/ 2012/58/pdf/piccione.pdf.
https://vetzoo.lsmuni.lt/data/vols/ 2012...
) animals need minerals such as calcium, magnesium, and phosphorus for growth, reproduction, and lactation, also functioning as catalytic components of enzymes or regulating various mechanisms involved in gestation and lactation.

The serum activity of AST, ALP, and GGT enzymes within the physiological ranges for the species is consistent with the findings of Otto et al.(33 Otto F, Vilela F, Harun M, Taylor M, Baggasse P, Bogin E. Biochemical blood profile of Angoni cattle in Mozambique. Israel Journal of Veterinary Medicine. 2000;55(3):95-102. https://pdfs.semanticscholar.org/b007/bd6f653bbb194209b889271bf024ce842003.pdf?_ga=2.1798327.74392992.1564689619-48519492.1558912057 .
https://pdfs.semanticscholar.org/b007/bd...
) in lactating African Angoni cows. Serum ALT values in Bonsmara cows above the physiological limits for the species are related to their greater muscle mass although ALT is primarily used as a biomarker of liver damage.(1515 Obućinski D, Soleša D, Kučević D, Prodanović R, Simin MT, Pelić DL, Đuragić O, Puvača N. Management of blood lipid profile and oxidative status in Holstein and Simmental dairy cows during lactation. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka 2019;69(2):116-124. https://doi.org/10.15567/mljekarstvo.2019.0206.
https://doi.org/10.15567/mljekarstvo.201...
) Unlike AST, equine, swine, and ruminant hepatocytes do not present a high ALT activity and, therefore, the increase in the serum activity of the enzyme during liver injury is insignificant even in necrosis.(1818 Stojević Z, Piršljin J, Milinković-Tur S, Zdelar-Tuk M, Ljubić BB. Activities of AST, ALT and GGT in clinically healthy dairy cows during lactation and in the dry period. Veterinarski Arhiv. 2005;75(1):67-73. https://hrcak.srce.hr/67059
https://hrcak.srce.hr/67059...
) Therefore, the muscle should be considered as a potential source for increasing serum activity of the enzyme since the total muscle mass is much higher than liver mass.

The higher value of the A:G ratio in third-lactation pregnant cows is due to the higher ALB value although it did not differ statistically from non-pregnant ones. The A:G ratio increased with an increase in albumin.

The Crea value in pregnant cows in the general group was higher than in non-pregnant cows (p<0.0001) due to the higher serum concentration in third-lactation pregnant cows, not differing statistically from non-pregnant ones. Importantly, most of the energy required by the metabolism and growth of the fetus in the pregnant cow is supplied by glucose and amino acids, which can lead to glucose reduction and consequent muscle protein catabolism.(99 Brscic M, Cozzi G, Lora I, Stefani AL, Contiero B, Ravarotto L, Gottardo F. Reference limits for blood analytes in Holstein late-pregnant heifers and dry cows: Effects of parity, days relative to calving, and season. Journal of Dairy Science. 2015;98(11):7886-7892. https://doi.org/10.3168/jds.2015-9345 .
https://doi.org/10.3168/jds.2015-9345...
, 1111 Cozzi G, Ravarotto L, Gottardo F, Stefani AL, Contiero B, Moro L, Brscic M, Dalvit P. Reference values for blood parameters in Holstein dairy cows: Effects of parity, stage of lactation, and season of production. Journal of Dairy Science. 2011;94(8):3895-3901. https://doi.org/10.3168/jds.2010-3687 .
https://doi.org/10.3168/jds.2010-3687...
) During gestation, the cow assumes the load of organic residues from the fetus through the fetal maternal circulation. Thus, an increase in serum creatinine in pregnant cows of the general group can also be attributed to the development of fetal muscles.(77 Piccione G, Messina V, Marafioti S, Casella S, Giannetto C, Fazio F. Changes of some haematochemical parameters in dairy cows during late gestation, post partum, lactation and dry periods. Veterinarija ir Zootechnika. 2012;58(80):59-64. https://vetzoo.lsmuni.lt/data/vols/ 2012/58/pdf/piccione.pdf.
https://vetzoo.lsmuni.lt/data/vols/ 2012...
) This result differs from that found by Otto et al.,(33 Otto F, Vilela F, Harun M, Taylor M, Baggasse P, Bogin E. Biochemical blood profile of Angoni cattle in Mozambique. Israel Journal of Veterinary Medicine. 2000;55(3):95-102. https://pdfs.semanticscholar.org/b007/bd6f653bbb194209b889271bf024ce842003.pdf?_ga=2.1798327.74392992.1564689619-48519492.1558912057 .
https://pdfs.semanticscholar.org/b007/bd...
) who observed similar values of the metabolite in pregnant and non-pregnant Angoni cows.

The probable reason for the higher value of serum Chol in second-lactation pregnant cows and the general group (p=0.004) is the higher mobilization of previously stored body fat and the release of fatty acids and glycerol into the bloodstream.(1515 Obućinski D, Soleša D, Kučević D, Prodanović R, Simin MT, Pelić DL, Đuragić O, Puvača N. Management of blood lipid profile and oxidative status in Holstein and Simmental dairy cows during lactation. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka 2019;69(2):116-124. https://doi.org/10.15567/mljekarstvo.2019.0206.
https://doi.org/10.15567/mljekarstvo.201...
, 1616 Contreras GA, Strieder-Barboza C, de Koster J. Symposium review: Modulating adipose tissue lipolysis and remodeling to improve immune function during the transition period and early lactation of dairy cows. Journal Dairy Science. 2018;101(3):2737-2752. https://doi.org/10.3168/jds.2017-13340
https://doi.org/10.3168/jds.2017-13340...
) Pregnant females aim to save the consumption of glucose and amino acids to meet the requirements of the fetus,(33 Otto F, Vilela F, Harun M, Taylor M, Baggasse P, Bogin E. Biochemical blood profile of Angoni cattle in Mozambique. Israel Journal of Veterinary Medicine. 2000;55(3):95-102. https://pdfs.semanticscholar.org/b007/bd6f653bbb194209b889271bf024ce842003.pdf?_ga=2.1798327.74392992.1564689619-48519492.1558912057 .
https://pdfs.semanticscholar.org/b007/bd...
) as lipids participate in a small proportion in the direct supply of energy to the fetus.(99 Brscic M, Cozzi G, Lora I, Stefani AL, Contiero B, Ravarotto L, Gottardo F. Reference limits for blood analytes in Holstein late-pregnant heifers and dry cows: Effects of parity, days relative to calving, and season. Journal of Dairy Science. 2015;98(11):7886-7892. https://doi.org/10.3168/jds.2015-9345 .
https://doi.org/10.3168/jds.2015-9345...
) Lactating cows may present physiological hypercholesterolemia due to the lipid mobilization caused by lactation and the increase in lipoprotein synthesis.(1919 Contreras GA, O`Boyle NJ, Herd TH, Sordillo LM. Lipomobilization in periparturient dairy cows influences the composition of plasma nonesterified fatty acids and leukocyte phospholipid fatty acids. Journal Dairy Science. 2010;93(6):2508-2516. https://doi.org/10.3168/jds.2009-2876
https://doi.org/10.3168/jds.2009-2876...
) In addition, cholesterol levels during gestation reach maximum values because of the synthesis of gonadal steroids. Pogliani et al.(66 Pogliani FC, Azedo MR, Souza RM, Raimundo RFS, Birgel Junior EH. Influência da gestação e do puerpério no lipidograma de bovinos da raça holandesa. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2010;62(2):273-280. http://dx.doi.org/10.1590/S0102-09352010000200005
http://dx.doi.org/10.1590/S0102-09352010...
) observed similar values for serum Chol in pregnant and non-pregnant Holstein heifers, showing that gestation did not influence the serum levels of the metabolite. The discrepancy between Chol values in cows of the present study and those of the literature is attributed to the use of pluriparous lactating cows in the present study to evaluate the possible influence of lactation order on the evaluated serum constituents.

The higher serum TRI concentration in second-lactation non-pregnant cows and the general group (p<0.0001) differs from the findings of Pogliani et al.,(66 Pogliani FC, Azedo MR, Souza RM, Raimundo RFS, Birgel Junior EH. Influência da gestação e do puerpério no lipidograma de bovinos da raça holandesa. Arquivo Brasileiro de Medicina Veterinária e Zootecnia. 2010;62(2):273-280. http://dx.doi.org/10.1590/S0102-09352010000200005
http://dx.doi.org/10.1590/S0102-09352010...
) who observed no statistically significant differences in the serum TRI concentrations in pregnant and non-pregnant cows. The difference between the findings in this study and those in the literature is attributed to the fact that the non-pregnant cows were in the first months of lactation, a period of higher milk production and, therefore, with higher demand for nutrients. However, pregnant cows were at the end of lactation, a period of lower milk production and, consequently, lower nutrient demand. Also, as lactation progresses, and with changes in the endocrine profiles during gestation, lipolysis decreases and lipogenesis replenishes the stores of triglycerides in the adipose tissue, which will later be used after delivery and the beginning of lactation.(1919 Contreras GA, O`Boyle NJ, Herd TH, Sordillo LM. Lipomobilization in periparturient dairy cows influences the composition of plasma nonesterified fatty acids and leukocyte phospholipid fatty acids. Journal Dairy Science. 2010;93(6):2508-2516. https://doi.org/10.3168/jds.2009-2876
https://doi.org/10.3168/jds.2009-2876...
)

The lower serum iP value in second-lactation pregnant cows (p=0.033) and the general group can be attributed to the passage of iP through the placenta to meet the needs of fetal development and the negative effect of parathyroid hormone (PTH), increasing urinary iP elimination.(2020 Yokus B, Cakir UD. Seasonal and physiological variations in serum chemistry and mineral concentrations in cattle. Biological Trace Element Research. 2006;109(3):255-266. https://doi.org/10.1385/BTER:109:3:255
https://doi.org/10.1385/BTER:109:3:255...
)

The higher serum Fe activity in second-lactation pregnant cows and the general group is attributed to an increase in Fe demand for fetal hematopoiesis and the fact that they were at the final third of lactation, a phase of lower milk production and, consequently, less mineral excretion in the milk.

The higher serum AST concentration (p=0.018) in second-lactation order pregnant cows can be attributed to the state of lipomobilization in the pregnant, which is a mechanism of physiological adaptation.(1616 Contreras GA, Strieder-Barboza C, de Koster J. Symposium review: Modulating adipose tissue lipolysis and remodeling to improve immune function during the transition period and early lactation of dairy cows. Journal Dairy Science. 2018;101(3):2737-2752. https://doi.org/10.3168/jds.2017-13340
https://doi.org/10.3168/jds.2017-13340...
) It results in increased hepatocyte membrane permeability, causing varying degrees of elevation in serum concentrations of the enzyme.(1515 Obućinski D, Soleša D, Kučević D, Prodanović R, Simin MT, Pelić DL, Đuragić O, Puvača N. Management of blood lipid profile and oxidative status in Holstein and Simmental dairy cows during lactation. Mljekarstvo: časopis za unaprjeđenje proizvodnje i prerade mlijeka 2019;69(2):116-124. https://doi.org/10.15567/mljekarstvo.2019.0206.
https://doi.org/10.15567/mljekarstvo.201...
) On the other hand, cholestasis was not evidenced since the serum GGT values were similar for pregnant and non-pregnant cows, remaining within the reference range proposed by Kaneko et al.(1212 Kaneko JJ, Harvey JW, Bruss ML. Clinical biochemistry of domestic animals. 6. ed. San Diego: Academic Press, 2008. 916p.) The increase in protein catabolism in the muscle tissue to supply the organism energy demand via gluconeogenesis must be considered.(22 Puppel K, Kuczyńska B. Metabolic profiles of cow's blood; a review. Journal of the Science of Food and Agriculture. 2016;96(13):4321-4328. https://doi.org/10.1002/jsfa.7779 .
https://doi.org/10.1002/jsfa.7779...
, 1111 Cozzi G, Ravarotto L, Gottardo F, Stefani AL, Contiero B, Moro L, Brscic M, Dalvit P. Reference values for blood parameters in Holstein dairy cows: Effects of parity, stage of lactation, and season of production. Journal of Dairy Science. 2011;94(8):3895-3901. https://doi.org/10.3168/jds.2010-3687 .
https://doi.org/10.3168/jds.2010-3687...
)

The higher serum ALP concentration (p=0.039) in second-lactation pregnant cows and the general group may be related to the fetal growth and the release of bone enzymes and isoenzymes of placental origin. Similar results were observed by Yokus and Cakir(2020 Yokus B, Cakir UD. Seasonal and physiological variations in serum chemistry and mineral concentrations in cattle. Biological Trace Element Research. 2006;109(3):255-266. https://doi.org/10.1385/BTER:109:3:255
https://doi.org/10.1385/BTER:109:3:255...
) in pregnant cows and Brscic et al.(99 Brscic M, Cozzi G, Lora I, Stefani AL, Contiero B, Ravarotto L, Gottardo F. Reference limits for blood analytes in Holstein late-pregnant heifers and dry cows: Effects of parity, days relative to calving, and season. Journal of Dairy Science. 2015;98(11):7886-7892. https://doi.org/10.3168/jds.2015-9345 .
https://doi.org/10.3168/jds.2015-9345...
) in pregnant heifers and primiparous and multiparous cows.

The predominance of differences between second-lactation pregnant and non-pregnant cows is possibly due to the higher loss of body reserves during the first lactation. The transition from gestation to lactation generates major endocrine and metabolic changes due to childbirth and higher demand for nutrients for milk production. According to Rossato et al.,(88 Rossato W, Gonzáles FHD, Dias MM, Riccó D, Valle SF, Rosa VLLA, Conceição T, Duarte F, Wald V. Number of lactations affects metabolic profile of dairy cows. Archives of Veterinary Science. 2001;6(2):83-88. Disponível em: www.ufrgs.br/lacvet/restrito/pdf/rossato_numero_lacta_oes.pdf
www.ufrgs.br/lacvet/restrito/pdf/rossato...
) first- and second-calving cows undergo higher loss of body reserves during lactation than cows with three or more lactations.

It is worth mentioning that this is one of the first studies on the serum biochemical profile of Bonsmara cows in Brazil and we expect that it could be a stimulus for further studies on the subject.

Conclusion

Gestation and lactation order are factors with significant influence on the concentration of several biochemical serum constituents of Bonsmara cows, especially in the second-lactation order. Therefore, these production phases are factors of variability that must be considered for the correct interpretation of the serum biochemical profile.

Acknowledgments

To the School of Veterinary Medicine (FAMEV-UFU) and the Veterinary Hospital of the Federal University of Uberlândia for supporting the experiment. To the owner of Fazenda Barra Grande for providing the facilities and animals to carry out this study.

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Publication Dates

  • Publication in this collection
    02 May 2022
  • Date of issue
    2022

History

  • Received
    23 Nov 2021
  • Accepted
    17 Feb 2022
Universidade Federal de Goiás Universidade Federal de Goiás, Escola de Veterinária e Zootecnia, Campus II, Caixa Postal 131, CEP: 74001-970, Tel.: (55 62) 3521-1568, Fax: (55 62) 3521-1566 - Goiânia - GO - Brazil
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