Dynamics of biochemical parameters in lambs during the first four months of life

Damaris Ferreira de Souza Thayla Sara Soares Stivari Reijers Susana Gilaverte Thiago Augusto da Cruz Fernando Hentz Bruno de Queiroz Castilhos Rosangela Locatelli Dittrich Alda Lúcia Gomes Monteiro About the authors

ABSTRACT

We aimed to verify whether age influences the biochemical profile of healthy lambs during the first four months of life by characterizing the dynamics of its parameters and verifying whether there are differences between the profiles of growing animals and the reference values established for adults. Blood samples of 34 ½ White Dorper × ½ Suffolk female lambs were collected at 30, 60, 90, and 120 days of age, and the serum concentrations of total proteins, total globulins, albumin, urea, creatinine, bilirubins (total, conjugated, and unconjugated), total cholesterol, triglycerides, glucose, gamma-glutamyltransferase, aspartate aminotransferase, and creatine kinase were determined. Descriptive statistics of these parameters were performed to compare them with the reference intervals used for adult sheep. Age influenced the dynamics of all the biochemical parameters between 30 and 120 days of age. Moreover, except for the total, conjugated and unconjugated bilirubins, total cholesterol, and aspartate aminotransferase means, the values of the lambs differed from the reference intervals established for adults. In conclusion, there is an influence of age on biochemical parameters in healthy female lambs in the first four months of life, and often the biochemical parameters of young animals differ from those of adults. Therefore, the interpretation of tests performed on growing animals should be made based on specific reference intervals for this age group.

Keywords:
age; blood; clinical biochemistry; metabolic profile; sheep

1. Introduction

Examination of the biochemical profile is an important clinical tool that assists in the differential diagnosis of various diseases ( Russell and Roussel, 2007Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
). In ruminants, a biochemical analysis can also be applied to populations for the evaluation of so-called metabolic profiles, mainly evaluating the nutritional management, reproductive performance, and incidence of diseases in livestock ( Peixoto and Osório, 2007Peixoto, L. A. O. and Osório, M. T. M. 2007. Perfil metabólico protéico e energético na avaliação do desempenho reprodutivo em ruminantes. Revista Brasileira de Agrociência 13:299-304. ).

For this to be possible, prior knowledge of the reference values in healthy animals and of the functioning of metabolic dynamics in normal situations and in cases of physiological, nutritional, and/or pathological alterations is essential ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Lima et al., 2015Lima, M. B.; Monteiro, M. V. B.; Jorge, E. M.; Campello, C. C.; Rodrigues, L. F. S.; Viana, R. B.; Monteiro, F. O. B. and Costa, C. T. C. 2015. Intervalos de referência sanguíneos e a influência da idade e sexo sobre parâmetros hematológicos e bioquímicos de ovinos da raça Santa Inês criados na Amazônia Oriental. Acta Amazonica 45:317-322. https://doi.org/10.1590/1809-4392201402115
https://doi.org/10.1590/1809-43922014021...
). For correct laboratory interpretation, factors that act on metabolic mechanisms and those that interfere with the analysis of results, such as species, breed, sex, production system, feeding, reproductive stage, climate, and differences in techniques used in each laboratory must be considered ( Meira Jr et al., 2009Meira Jr, E. B. S.; Rizzo, H.; Benesi, F. J. and Gregory, L. 2009. Influence of age and sex on total serum protein and albumin and aspartato-aminotransferase and gama-glutamiltransferase serum activities on Santa Inês sheep. Brazilian Journal of Veterinary Research and Animal Science 46:448-454. https://doi.org/10.11606/S1413-95962009000600003
https://doi.org/10.11606/S1413-959620090...
; Braun et al., 2010Braun, J. P.; Trumel, C. and Bézille, P. 2010. Clinical biochemistry in sheep: A selected review. Small Ruminant Research 92:10-18. https://doi.org/10.1016/j.smallrumres.2010.04.002
https://doi.org/10.1016/j.smallrumres.20...
).

In recent years, there has been an increase in researchers' interest in establishing reference intervals for different breeds, sexes, and age groups of the Brazilian sheep flock ( Batista et al., 2009Batista, M. C. S.; Castro, R. S.; Rego, E. W.; Carvalho, F. A. A.; Silva, S. M. M. S.; Carvalho, C. C. D. and Riet-Correa, F. 2009. Hematology and blood biochemistry in sheep with conidiobolomycosis in northeastern Brazil. Pesquisa Veterinária Brasileira 29:17-24. https://doi.org/10.1590/S0100-736X2009000100002
https://doi.org/10.1590/S0100-736X200900...
; Meira Jr et al., 2009Meira Jr, E. B. S.; Rizzo, H.; Benesi, F. J. and Gregory, L. 2009. Influence of age and sex on total serum protein and albumin and aspartato-aminotransferase and gama-glutamiltransferase serum activities on Santa Inês sheep. Brazilian Journal of Veterinary Research and Animal Science 46:448-454. https://doi.org/10.11606/S1413-95962009000600003
https://doi.org/10.11606/S1413-959620090...
; Santana et al., 2009Santana, A. M.; Silva, D. G.; Bernardes, P. A.; Pizauro, L. J. L.; Maluta, R. P.; Aquino, G. V.; Garcia, K. O.; Ávila, F. A. and Fagliari, J. J. 2009. Hemogram and serum biochemical profile of slaughter-age sheep. Ciência Animal Brasileira 10(Supplement 1):286-289. ; Madureira et al., 2013Madureira, K. M.; Gomes, V.; Barcelos, B.; Zani, B. H.; Shecaira, C. L.; Baccili, C. C. and Benesi, F. J. 2013. Hematological and biochemical parameters of Dorper ewes. Semina: Ciências Agrárias 34:811-816. https://doi.org/10.5433/1679-0359.2013v34n2p811
https://doi.org/10.5433/1679-0359.2013v3...
; Carlos et al., 2015Carlos, M. M. L.; Leite, J. H. G. M.; Chaves, D. F.; Vale, A. M.; Façanha, D. A. E.; Melo, M. M. and Soto-Blanco, B. 2015. Blood parameters in the Morada Nova sheep: influence of age, sex, and body condition score. The Journal of Animal and Plant Sciences 25:950-955. ; Lima et al., 2015Lima, M. B.; Monteiro, M. V. B.; Jorge, E. M.; Campello, C. C.; Rodrigues, L. F. S.; Viana, R. B.; Monteiro, F. O. B. and Costa, C. T. C. 2015. Intervalos de referência sanguíneos e a influência da idade e sexo sobre parâmetros hematológicos e bioquímicos de ovinos da raça Santa Inês criados na Amazônia Oriental. Acta Amazonica 45:317-322. https://doi.org/10.1590/1809-4392201402115
https://doi.org/10.1590/1809-43922014021...
; Souza et al., 2016Souza, B. C.; Sena, L. S.; Loureiro, D.; Raynal, J. T.; Sousa, T. J.; Bastos, B. L.; Meyer, R. and Portela, R. W. 2016. Determinação de valores de referência séricos para os eletrólitos magnésio, cloretos, cálcio e fósforo em ovinos das raças Dorper e Santa Inês. Pesquisa Veterinária Brasileira 36:167-173. https://doi.org/10.1590/S0100-736X2016000300004
https://doi.org/10.1590/S0100-736X201600...
). However, even in these studies, animals in the growth phase are categorized as a generalized age group, without a specific assessment of the changes in metabolic dynamics within the neonatal and growth periods. In the literature, there are still few studies covering this phase in detail ( Devendran et al., 2009Devendran, P.; Jayachandran, S.; Visha, P.; Nanjappan, K. and Panneerselvam, S. 2009. Hematological and blood biochemical profile of Coimbatore sheep. The Indian Journal of Small Ruminants 15:98-101. ; Lepherd et al., 2009Lepherd, M. L.; Canfield, P. J.; Hunt, G. B. and Bosward, K. L. 2009. Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs. Australian Veterinary Journal 87:5-11. https://doi.org/10.1111/j.1751-0813.2008.00382.x
https://doi.org/10.1111/j.1751-0813.2008...
; Silva et al., 2010Silva, D. F. M.; Costa, J. N.; Araújo, A. L.; Costa Neto, A. O.; Almeida, M. A. O. and Carvalho, V. S. 2010. Proteinograma sérico de cordeiros mestiços (Santa Inês x Dorper) do nascimento até o desmame: Efeito do desenvolvimento etário e do monitoramento da ingestão do colostro. Ciência Animal Brasileira 11:794-805. https://doi.org/10.5216/cab.v11i4.4848
https://doi.org/10.5216/cab.v11i4.4848...
; Antunović et al., 2012Antunović, Z.; Šperanda, M.; Senčić, Đ.; Novoselec, J.; Steiner, Z. and Djidara, M. 2012. Influence of age on some blood parameters of lambs in organic production. Macedonian Journal of Animal Science 1:11-15. ; Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
; Cruz et al., 2017Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
); thus, often the reference intervals used in the evaluation of lambs are still based on values determined for adults.

However, the highest mortality rates are observed in lambs, and metabolic disorders in the first months of life, if not properly treated, will impair productivity in the following periods ( Magalhães et al., 2016Magalhães, K. A.; Souza, J. D. F.; Guimarães, V. P.; Barbosa, C. M. P.; Martins, E. C. and Holanda Filho, Z. F. 2016. Características da produção de ovinos e caprinos em propriedades modais da BA, MS, RS e MG. Boletim Ativos de Ovinos e Caprinos 3:1-2. ). There is a consensus that age has an important effect on the concentration of many metabolites, especially before puberty ( Lepherd et al., 2009Lepherd, M. L.; Canfield, P. J.; Hunt, G. B. and Bosward, K. L. 2009. Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs. Australian Veterinary Journal 87:5-11. https://doi.org/10.1111/j.1751-0813.2008.00382.x
https://doi.org/10.1111/j.1751-0813.2008...
; Antunović et al., 2012Antunović, Z.; Šperanda, M.; Senčić, Đ.; Novoselec, J.; Steiner, Z. and Djidara, M. 2012. Influence of age on some blood parameters of lambs in organic production. Macedonian Journal of Animal Science 1:11-15. ). This is already well established in calves ( Feitosa et al., 2007Feitosa, F. L. F.; Mendes, L. C. N.; Peiró, J. R.; Cadioli, F. A.; Yanaka, R.; Bovino, F.; Féres, F. C. and Perri, S. H. V. 2007. Influência da faixa etária nos valores de enzimas hepáticas e de uréia e creatinina em bezerros Holandeses do nascimento até os 365 dias de vida. Ciência Veterinária nos Trópicos 10:54-61. ; Delfino et al., 2014Delfino, J. L.; Barbosa, V. M.; Gondim, C. C.; Oliveira, P. M.; Nasciutti, N. R.; Oliveira, R. S. B. R.; Tsuruta, S. A.; Mundim, A. V. and Saut, J. P. E. 2014. Perfil bioquímico sérico de bezerros senepol nos primeiros 120 dias de idade. Semina: Ciências Agrárias 35:1341-1350. https://doi.org/10.5433/1679-0359.2014v35n3p1341
https://doi.org/10.5433/1679-0359.2014v3...
); however, a better understanding of the influence of this factor on the biochemical profile of lambs is required.

Therefore, the objective of this study was to verify whether there is indeed an influence of age on the biochemical profile of healthy lambs during the first four months of life, by characterizing the dynamics of its parameters during this period. Moreover, we aimed to verify whether there are differences between the profiles of growing animals and the reference values established for adults.

2. Material and Methods

Research on animals was conducted according to the institutional committee on animal use (case no. 016/2011 of August 04, 2011). The study was carried out in Pinhais, Paraná State, Southern Brazil (25°38' S, 49°14' W, and 953 m altitude).

Thirty-four ½ White Dorper × ½ Suffolk female lambs, monitored from birth to 120 days of age, were used. The evaluation period extended from October to March (Spring/Summer).

As prophylactic measures, we certified that the colostration was adequate, and the postpartum umbilical disinfection was performed as well as disinfection of the premises; vaccinations against clostridiosis (Sintoxan Polivalente T®, Merial) and ecthyma contagiosum (Ectima Vac®, CEVA) were performed at 41 days of age, on average; we also performed weighing [body weight (BW) at birth and at 18-day intervals] and calculations of average daily weight gain (ADG) and body condition score (BCS) according to Russel et al. (1969)Russel, A. J. F.; Doney, J. M. and Gunn, R. G. 1969. Subjective assessment of body fat in live sheep. Journal Agricultural Science 72:451-454. https://doi.org/10.1017/S0021859600024874
https://doi.org/10.1017/S002185960002487...
, and parasitological monitoring [by observation of clinical signs such as diarrhea and the application of the Famacha method according to Molento et al. (2004)Molento, M. B.; Tasca, C.; Gallo, A.; Ferreira, M.; Bononi, R. and Stecca, E. 2004. Método Famacha como parâmetro clínico individual de infecção por Haemonchus contortus em pequenos ruminantes. Ciência Rural 34:1139-1145. https://doi.org/10.1590/S0103-84782004000400027
https://doi.org/10.1590/S0103-8478200400...
]. Because of the initial small size of the animals, there was difficulty in obtaining the required amount of feces for the parasitological exams, and, therefore, the count of eggs per gram of feces (EPG) was not carried out. No complication was observed after these interventions. The animals showed normal complete blood count and no lesions or apparent pathological signs throughout the experiment.

The lambs presented growth according to NRC (2007)NRC - National Research Council. 2007. Nutrient requirements of small ruminants: sheep, goats, cervids and new world camelids. National Academy of Sciences, Washington, D.C. . The mean and standard error (M±SE) for birth weight was 4.6±0.2 kg, and the values of BW and ADG recorded during the experiment are in Table 1 . Also, the means for Famacha grade and BCS were 1.6±0.2 and 2.8±0.1, respectively, indicating that the lambs presented adequate sanitary status.

Table 1
Performance of ½ White Dorper × ½ Suffolk lambs in the first four months of age

The lambs remained housed with their mothers in collective pens from birth to weaning, which occurred between 70 and 80 days of age. From 14 days of age, they had access to feed in creep feeding composed of corn silage and protein-energy concentrate ( Table 2 ), provided as total mixed ration (TMR), twice a day (at 08.00 and 16.00 h). The diet of the ewes was composed of the same silage provided to the lambs plus energy concentrate ( Table 2 ), adjusted for the category of lactating ewes according to NRC (2007)NRC - National Research Council. 2007. Nutrient requirements of small ruminants: sheep, goats, cervids and new world camelids. National Academy of Sciences, Washington, D.C. . Lambs were fed corn silage ad libitum from 61 to 90 days of age ( Table 3 ), allowing leftovers of up to 200 g kg−1 of the fresh matter offered to not limit the feed intake.

Table 2
Ingredients of the energy and protein-energy concentrates and chemical composition of energy and protein-energy concentrates, corn silage, and limpograss samples collected by simulated grazing during the experiment
Table 3
Nutritional requirements, estimated diet intake, and nutritional balance for ½ White Dorper × ½ Suffolk lambs in the first four months of age

After weaning, the lambs remained housed in collective pens until 90 days of age. From this age, they were allocated to limpograss pastures [ Hemarthria altissima ; whose chemical composition was determined from two samples collected in the last evaluation period by the grazing simulation method, according to Burns et al. (1989)Burns, J. C.; Lippke, H. and Fisher, D. S. 1989. The relationship of herbage mass and characteristics to animal responses in grazing experiments. p.7-20. In: Grazing Research: design, methodology and analysis. Marten, G. C., ed. Crop Science Society of America, Madison. https://doi.org/10.2135/cssaspecpub16.c2
https://doi.org/10.2135/cssaspecpub16.c2...
; Table 2 ] during the daytime (from 08.00 h), being gathered in the fold in the evening (after 16.00 h) when they received supplementation in the trough (of the same composition of TMR provided in the creep feeding during pre-weaning; Table 2 ), and remained overnight.

The diets were formulated to meet the nutritional requirements recommended for growing lambs, with maturity of 0.3 at four months of age and expressing 200 g day−1 of mean daily gain, according to NRC (2007)NRC - National Research Council. 2007. Nutrient requirements of small ruminants: sheep, goats, cervids and new world camelids. National Academy of Sciences, Washington, D.C. . The requirements of dry matter intake, crude protein, and metabolizable energy were adjusted to the BW of lambs at the ages of 14, 30, 60, 75 (considered as the weaning day), 90, and 120 days, and milk intake (from 14 days of age until weaning) was estimated. The diets were provided to complement the milk intake until weaning and to allow the lambs to achieve the pre-stablished performance ( Table 3 ).

The biochemical tests for each of the 34 female lambs were performed at 30, 60, 90, and 120 days of age, totaling 134 samples. Blood samples (4 mL) were collected by jugular venipuncture in vacuum tubes without anticoagulant, after a 10-h fasting (without water deprivation). All collections were performed in the period between 06.00 and 09.00 h. The samples were rested until clot formation and then centrifuged at 2,400 × g for 10 min. The obtained serum was transferred and stored in Eppendorf tubes at −20 °C until analysis.

The serum samples were thawed at room temperature and then processed in an automated biochemical analyzer (BS-200, Myndray®), previously calibrated with commercial control serum (Control Lab®). The evaluated parameters and the respective methods applied were as follows: the concentration of total proteins (biuret method, Katal®), albumin (bromocresol green method, Katal®), total globulins (by the difference between the total proteins and albumin), urea (UV enzymatic method of urease-GLDH, Kovalent®), creatinine (Jaffé method, Kovalent®), total and conjugated bilirubins (Jendrassik Grof method, Dialab®), unconjugated bilirubin (by the difference between the total and conjugated bilirubins), total cholesterol (CHOD-PAP enzymatic method, Kovalent®), triglycerides (GPO-PAP enzymatic method, Kovalent®), glucose (glucose enzymatic method, Katal®), gamma-glutamyltransferase (GGT; kinetic method of GGT, Katal®), aspartate aminotransferase (AST; UV kinetic method of AST, Katal®), and creatine kinase (CK; UV kinetic method of CK, Katal®).

The data were analyzed in a mixed model with repeated measures on time (PROC MIXED), in which the time represented the age of lambs and was the fixed effect, and the animal was the random effect. The analyses were performed using the model:

Y ^ ij = μ + A i + lamb j + ε ij ,

in which Y^ij = value of dependent variable for the j-th lamb at the i-th age; µ = mean value of dependent variable (constant); Ai = effect of the i-th age; lambj = random effect of j-th lamb; and εij = random error. The best covariance structure for each dependent variable was selected based on the corrected Akaike (AICC) and Bayesian (BIC) information criteria. The means were fitted to the statistical model and compared between ages by Tukey's test (PROC LSMEANS).

A regression analysis (PROC REG) in which the age of lambs was considered the independent variable was performed up to the second order (quadratic), according to:

Y ^ ij = β 0 + β 1 A i1 + β 2 A i2 + γ ij + ε ij ,

in which Y^ij = value of the dependent variable for the j-th lamb at the i-th age; β0 = regression intercept; Ai = independent variable (age); β1 = linear regression coefficient for the dependent variable; β2 = quadratic coefficient of regression for the dependent variable; γij = regression deviations; and εij = random error.

Differences between ages in the mixed models and the adjustment of regression equations were considered at a 0.05 significance level.

To verify the differences between lambs and adult sheep, the intervals for the blood biochemical parameters of the lambs between 30 and 120 days of age were determined, with the lower and upper limits of the 0.95 confidence interval, the median, and the mean and standard deviation (M±SD) through descriptive analyses (PROC MEANS). The values of serum triglycerides were compared with those found for ewes by Caldeira et al. (2007)Caldeira, R. M.; Belo, A. T.; Santos, C. C.; Vazques, M. I. and Portugal, A. V. 2007. The effect of body condition score on blood metabolites and hormonal profiles in ewes. Small Ruminant Research 68:233-241. https://doi.org/10.1016/j.smallrumres.2005.08.027
https://doi.org/10.1016/j.smallrumres.20...
, and the values of other parameters were compared to the reference interval for adult sheep established by Kaneko et al. (2008)Kaneko, J. J.; Harvey, J. W. and Bruss, M. L. 2008. Clinical biochemistry of domestic animals. 6th ed. Academic Press, San Diego. .

All statistical analyses were carried out by SAS software (Statistical Analysis System, version 9.0).

3. Results

There was an effect of age on all protein parameters ( Tables 4 and 5 ). The means for total protein showed a linear response, increasing between 30 and 60 days and stabilization until 120 days. The means for total globulin showed a linear increase with advancing age. A quadratic effect was observed for albumin concentrations, which showed an increase between 30 and 90 days, although with its inflection point at 78 days, so that a decrease was observed at 120 days.

Table 4
Means and standard errors (M±SE) for blood biochemical parameters in ½ White Dorper × ½ Suffolk lambs until four months of age
Table 5
Regression equations for blood biochemical parameters in relation to age of ½ White Dorper × ½ Suffolk lambs

There was an effect of age on the kidney function parameters ( Tables 4 and 5 ). The urea concentration showed an increasing linear response with an increase between 60 and 90 days, peaking at 54.29 mg dL−1 at 120 days of age. The mean creatinine concentrations remained constant between 30 and 90 days and showed a decrease at 120 days, in a quadratic response with the inflection point at 65 days.

The total bilirubin concentration showed a peak of 0.39 mg dL−1 at 30 days, which was followed by a gradual decrease until 90 days and a subtle increase between 90 and 120 days, in a quadratic response with its inflection point at 115 days ( Tables 4 and 5 ). The conjugated bilirubin concentration showed a linear behavior, although oscillating, with an increase between 30 and 60 days, decrease at 90 days, and a further increase at 120 days, when it reached its peak of 0.26 mg dL−1. On the opposite way, through a quadratic effect, the peak of the unconjugated bilirubin concentration occurred at 30 days (0.20 mg dL−1), then decreased gradually until reaching 0.05 mg dL−1 at 120 days of age.

A quadratic effect of age on the energy profile of the lambs was noted ( Tables 4 and 5 ). The total cholesterol and triglycerides concentrations presented a similar dynamics, marked by peaks at 30 days, which were followed by a gradual decrease until 90 days (with their inflection points at 90 and 86 days, respectively) and a further increase at 120 days, although showing lower values than the initial concentrations. The glucose concentration showed a decrease between 30 and 60 days, with an inflection point at 71 days, from which there was a gradual increase of the values until 120 days.

Regarding the enzymatic profile, there was also an effect of age on the serum concentrations of GGT, AST, and CK ( Tables 4 and 5 ). The GGT concentration linearly decreased between 30 and 120 days of age. On the other hand, the AST concentration linearly increased throughout the study. The CK means decreased between 30 and 60 days and then remained stable until 120 days, in a quadratic effect with its inflection point at 92 days.

With respect to the comparison of biochemical parameters of lambs with those for adult sheep ( Table 6 ), the mean values for total protein in lambs were lower than the reference interval for adults, such that even when the mean was added to the standard deviation (60.6 g L−1), it remained close to the lower limit of the reference. Similarly, the mean for total globulins, even when added to its standard deviation (25.6 g L−1), remained well below the lower limit of the reference interval. Conversely, the value of the lower limit for the albumin concentration of the lambs exceeded the upper value of the reference interval for adults.

Table 6
Descriptive analysis of biochemical parameters in ½ White Dorper × ½ Suffolk lambs in the first four months of age and reference intervals reported for adult sheep

The urea and creatinine concentration values of the lambs were also not within those referenced for adults. However, the mean for urea when subtracted from its standard deviation (34.25 mg dL−1) was within of the reference, whereas the mean for creatinine added to its standard deviation (0.83 mg dL−1) was much lower than the lower limit of the reference.

The means for total, conjugated, and unconjugated bilirubins were included within the reference interval for adults, although both the mean values for conjugated and unconjugated bilirubin when added to their standard deviations (0.31 and 0.18 mg dL−1, respectively) were higher than the values of the upper limits of the reference interval for these metabolites in older animals.

The mean for total cholesterol of lambs was also inserted in the interval for adults, although its value when added to its standard deviation (93.41 mg dL−1) exceeded the upper value of the reference interval. The mean for triglycerides, even when subtracted from its standard deviation (17.18 mg dL−1), remained higher than the mean referenced for adults. The mean glucose level was a little over the upper limit of the reference, reaching a value of 91.15 mg dL−1 when added to its standard deviation.

The GGT values of the lambs were also higher than those of the reference, and even when standard deviation was subtracted from the mean (49.9 U L−1), its value remained very close to the upper limit of the interval established for adults. The AST values remained within the reference interval for adults, although when the standard deviation was subtracted from the mean (62.9 U L−1), the value was very close to the lower limit of the reference. The mean for CK was at least 14 times higher than the upper value of the interval determined for adults.

4. Discussion

The total protein concentrations are directly influenced by the dynamics of total globulins ( Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
). Therefore, the lower values for total proteins and globulins verified at 30 days probably represent the transition period in the immunoglobulin content in the bloodstream, which is characterized by the end of the degradation process of immunoglobulins passively received via colostrum and by the initial phase of active production of immunoglobulins by the animal itself ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Silva et al., 2010Silva, D. F. M.; Costa, J. N.; Araújo, A. L.; Costa Neto, A. O.; Almeida, M. A. O. and Carvalho, V. S. 2010. Proteinograma sérico de cordeiros mestiços (Santa Inês x Dorper) do nascimento até o desmame: Efeito do desenvolvimento etário e do monitoramento da ingestão do colostro. Ciência Animal Brasileira 11:794-805. https://doi.org/10.5216/cab.v11i4.4848
https://doi.org/10.5216/cab.v11i4.4848...
). In subsequent months, the increase in values results mainly from the increase in gamma globulin concentrations resulting from the antigenic stimulation of lambs (exposure to antigens in the extrauterine environment and by vaccination) and from the maturation of the immune system ( Silva et al., 2010Silva, D. F. M.; Costa, J. N.; Araújo, A. L.; Costa Neto, A. O.; Almeida, M. A. O. and Carvalho, V. S. 2010. Proteinograma sérico de cordeiros mestiços (Santa Inês x Dorper) do nascimento até o desmame: Efeito do desenvolvimento etário e do monitoramento da ingestão do colostro. Ciência Animal Brasileira 11:794-805. https://doi.org/10.5216/cab.v11i4.4848
https://doi.org/10.5216/cab.v11i4.4848...
; Delfino et al., 2014Delfino, J. L.; Barbosa, V. M.; Gondim, C. C.; Oliveira, P. M.; Nasciutti, N. R.; Oliveira, R. S. B. R.; Tsuruta, S. A.; Mundim, A. V. and Saut, J. P. E. 2014. Perfil bioquímico sérico de bezerros senepol nos primeiros 120 dias de idade. Semina: Ciências Agrárias 35:1341-1350. https://doi.org/10.5433/1679-0359.2014v35n3p1341
https://doi.org/10.5433/1679-0359.2014v3...
; Santos et al., 2017Santos, R. P.; Macedo Junior, G. L.; Silva, S. P.; Sousa, L. F. and Andrade, M. E. B. 2017. Inclusion of propylene glycol in the diet of sheep and its effect on their lambs' protein and mineral metabolites. Acta Scientiarum. Animal Sciences 39:297-302. https://doi.org/10.4025/actascianimsci.v39i3.35101
https://doi.org/10.4025/actascianimsci.v...
).

The albumin concentrations also affect the total protein levels. Albumin is the main plasma protein synthesized by the liver and corresponds to approximately 35 to 50% of total serum proteins and is responsible for 80% of the colloid osmotic pressure ( Kaneko et al., 2008Kaneko, J. J.; Harvey, J. W. and Bruss, M. L. 2008. Clinical biochemistry of domestic animals. 6th ed. Academic Press, San Diego. ). It is influenced by dietary protein intake and is considered the most sensitive indicator for the determination of protein nutritional status in the long term, since changes in its concentrations are detected only after a minimum period of one month due to its low rate of synthesis and degradation ( Peixoto and Osório, 2007Peixoto, L. A. O. and Osório, M. T. M. 2007. Perfil metabólico protéico e energético na avaliação do desempenho reprodutivo em ruminantes. Revista Brasileira de Agrociência 13:299-304. ). According to Silva et al. (2010)Silva, D. F. M.; Costa, J. N.; Araújo, A. L.; Costa Neto, A. O.; Almeida, M. A. O. and Carvalho, V. S. 2010. Proteinograma sérico de cordeiros mestiços (Santa Inês x Dorper) do nascimento até o desmame: Efeito do desenvolvimento etário e do monitoramento da ingestão do colostro. Ciência Animal Brasileira 11:794-805. https://doi.org/10.5216/cab.v11i4.4848
https://doi.org/10.5216/cab.v11i4.4848...
and Chai et al. (2015)Chai, J.; Diao, Q.; Wang, H.; Tu, Y.; Tao, X. and Zhang, N. 2015. Effects of weaning age on growth, nutrient digestibility and metabolism, and serum parameters in Hu lambs. Animal Nutrition 1:344-348. https://doi.org/10.1016/j.aninu.2015.11.007
https://doi.org/10.1016/j.aninu.2015.11....
, lambs older than 30 days already present rumination and become proficient in the use of nitrogenous compounds from the diet, which causes a gradual increase in albumin concentrations until 90 days, as observed in this study. The decrease observed at 120 days, as a delayed response from albumin, in turn, might have been caused mainly by weaning, since depriving the lambs of milk reduces the total dietary protein and energy intake (as observed at 76-90 days; Table 3 ) and, consequently, the use of available forage protein and albumin synthesis ( Fernandes et al., 2012Fernandes, S. R.; Monteiro, A. L. G.; Dittrich, R. L.; Salgado, J. A.; Silva, C. J. A.; Silva, M. G. B.; Beltrame, O. C. and Pinto, P. H. N. 2012. Early weaning and concentrate supplementation on the performance and metabolic profile of grazing lambs. Revista Brasileira de Zootecnia 41:1292-1300. https://doi.org/10.1590/S1516-35982012000500029
https://doi.org/10.1590/S1516-3598201200...
; Santos et al., 2017Santos, R. P.; Macedo Junior, G. L.; Silva, S. P.; Sousa, L. F. and Andrade, M. E. B. 2017. Inclusion of propylene glycol in the diet of sheep and its effect on their lambs' protein and mineral metabolites. Acta Scientiarum. Animal Sciences 39:297-302. https://doi.org/10.4025/actascianimsci.v39i3.35101
https://doi.org/10.4025/actascianimsci.v...
). It is noteworthy that the dynamics of albumin is not only changed by nutrition, but also by the ability of the liver to synthesize it, which, during the neonatal period, is still influenced by the development and maturation of hepatic metabolic processes ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
).

Regarding the parameters related to kidney function, it is known that shortly after birth, with the rupture of the umbilical cord, the kidneys assume the hydroelectrolytic control and excretory functions previously performed by the placenta, and there is a gradual increase in the efficiency of kidney function with age ( Benesi et al., 2005Benesi, F. J.; Coelho, C. S.; Leal, M. L. R.; Mirandola, R. M. S. and Lisbôa, J. A. N. 2005. Biochemical parameters for evaluation of renal function and fluid and electrolyte balance of healthy female Holstein calves during the first month of life. Brazilian Journal of Veterinary Research and Animal Science 42:291-298. https://doi.org/10.11606/issn.1678-4456.bjvras.2005.26424
https://doi.org/10.11606/issn.1678-4456....
). In sheep, it is important to remember that although urea is not considered a very accurate metabolite for renal evaluation, it is a quick and sensitive indicator of the protein nutritional status, since it is directly related to the input of degradable proteins and to the energy:protein ratio of the diet ( González and Scheffer, 2002González, F. H. D. and Scheffer, J. F. S. 2002. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. p.5-17. In: Avaliação metabólico-nutricional de vacas leiteiras por meio de fluídos corporais (sangue, leite e urina). Anais do 29º Congresso Brasileiro de Medicina Veterinária. Gramado, RS. ; Peixoto and Osório, 2007Peixoto, L. A. O. and Osório, M. T. M. 2007. Perfil metabólico protéico e energético na avaliação do desempenho reprodutivo em ruminantes. Revista Brasileira de Agrociência 13:299-304. ; Braun et al., 2010Braun, J. P.; Trumel, C. and Bézille, P. 2010. Clinical biochemistry in sheep: A selected review. Small Ruminant Research 92:10-18. https://doi.org/10.1016/j.smallrumres.2010.04.002
https://doi.org/10.1016/j.smallrumres.20...
). In fact, serum urea concentration is proportional to the ammonia levels produced in the rumen ( Karimizadeh et al., 2017Karimizadeh, E.; Chaji, M. and Mohammadabadi, T. 2017. Effects of physical form of diet on nutrient digestibility, rumen fermentation, rumination, growth performance and protozoa population of finishing lambs. Animal Nutrition 3:139-144. https://doi.org/10.1016/j.aninu.2017.01.004
https://doi.org/10.1016/j.aninu.2017.01....
). Most of the protein ingested is degraded by ruminal microorganisms, releasing ammonia, which is used for microbial protein synthesis ( Geron et al., 2018Geron, L. J. V.; Garcia, J.; Aguiar, S. C.; Costa, F. G.; Silva, A. P.; Sousa Neto, E. L.; Carvalho, J. T. H.; Roberto, L. S.; Coelho, K. S. M. and Santos, I. S. 2018. Effect of slow release urea in sheep feed on nitrogen balance. Semina: Ciências Agrárias 39:683-696. https://doi.org/10.5433/1679-0359.2018v39n2p683
https://doi.org/10.5433/1679-0359.2018v3...
). However, when large amounts of protein are fermented in combination with low availability of energy from carbohydrate degradation, a high rumen ammonia concentration is generated. The capacity of ammonia utilization by ruminal microorganisms is exceeded, so the excess is absorbed into the enterohepatic circulation, and in the liver is converted into urea, which, added to urea from amino acid metabolism, constitutes the major portion of plasma urea ( Fernandes et al., 2012Fernandes, S. R.; Monteiro, A. L. G.; Dittrich, R. L.; Salgado, J. A.; Silva, C. J. A.; Silva, M. G. B.; Beltrame, O. C. and Pinto, P. H. N. 2012. Early weaning and concentrate supplementation on the performance and metabolic profile of grazing lambs. Revista Brasileira de Zootecnia 41:1292-1300. https://doi.org/10.1590/S1516-35982012000500029
https://doi.org/10.1590/S1516-3598201200...
; Karimizadeh et al., 2017Karimizadeh, E.; Chaji, M. and Mohammadabadi, T. 2017. Effects of physical form of diet on nutrient digestibility, rumen fermentation, rumination, growth performance and protozoa population of finishing lambs. Animal Nutrition 3:139-144. https://doi.org/10.1016/j.aninu.2017.01.004
https://doi.org/10.1016/j.aninu.2017.01....
; Geron et al., 2018Geron, L. J. V.; Garcia, J.; Aguiar, S. C.; Costa, F. G.; Silva, A. P.; Sousa Neto, E. L.; Carvalho, J. T. H.; Roberto, L. S.; Coelho, K. S. M. and Santos, I. S. 2018. Effect of slow release urea in sheep feed on nitrogen balance. Semina: Ciências Agrárias 39:683-696. https://doi.org/10.5433/1679-0359.2018v39n2p683
https://doi.org/10.5433/1679-0359.2018v3...
). However, it can be observed that the energy requirement for the lambs in this study was practically met ( Table 3 ), with only a small deficit in its balance at 91-120 days, while the protein deficit was much higher (not being the protein requirement fully met). In this case, then, the increase in urea from 90 days onwards probably reflected the increase in urea recycled by the nitrogen conservation mechanism, through which part of the urea synthesized in the liver, after being released into the bloodstream, returns to the rumen through the bloodstream itself (by difusion through the ruminal wall) or via saliva ( Santos and Pedroso, 2011Santos, F. A. P. and Pedroso, A. M. 2011. Metabolismo de proteínas. p.265-298. In: Nutrição de ruminantes. 2.ed. Berchielli, T. T.; Pires, A. V. and Oliveira, S. G., eds. Funep, Jaboticabal. ).

In contrast, creatinine is less influenced by external factors and, therefore, is the main marker for the glomerular filtration rate in ruminants ( Russell and Roussel, 2007Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
). Carlos et al. (2015)Carlos, M. M. L.; Leite, J. H. G. M.; Chaves, D. F.; Vale, A. M.; Façanha, D. A. E.; Melo, M. M. and Soto-Blanco, B. 2015. Blood parameters in the Morada Nova sheep: influence of age, sex, and body condition score. The Journal of Animal and Plant Sciences 25:950-955. and Lima et al. (2015), when comparing sheep in different age groups (from less than six months to over 24 months), observed an increase in creatinine concentrations with advancing age, which would be due to the expansion of creatinine reservoirs in the organism as a consequence of the increase in muscular mass deposition with growth, or a possible reduction in serum thyroxine levels that would trigger a decrease in glomerular filtration rate. However, just as among the lambs in this study, Feitosa et al. (2007)Feitosa, F. L. F.; Mendes, L. C. N.; Peiró, J. R.; Cadioli, F. A.; Yanaka, R.; Bovino, F.; Féres, F. C. and Perri, S. H. V. 2007. Influência da faixa etária nos valores de enzimas hepáticas e de uréia e creatinina em bezerros Holandeses do nascimento até os 365 dias de vida. Ciência Veterinária nos Trópicos 10:54-61. , Mohri et al. (2007)Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
, and Delfino et al. (2014)Delfino, J. L.; Barbosa, V. M.; Gondim, C. C.; Oliveira, P. M.; Nasciutti, N. R.; Oliveira, R. S. B. R.; Tsuruta, S. A.; Mundim, A. V. and Saut, J. P. E. 2014. Perfil bioquímico sérico de bezerros senepol nos primeiros 120 dias de idade. Semina: Ciências Agrárias 35:1341-1350. https://doi.org/10.5433/1679-0359.2014v35n3p1341
https://doi.org/10.5433/1679-0359.2014v3...
when evaluating calves, and Cruz et al. (2017)Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
studying lambs, observed higher values of creatinine in the first days of life that would be correlated with renal immaturity and muscle wasting caused by the onset of locomotion. Also, according to these authors, the subsequent decrease during the growth phase would be attributed to the renal clearance improvement from the first week of life and the decrease in phosphocreatine demand for muscle weight gain after 61 days of age.

In cattle, the effect of age on the total bilirubin dynamics is notorious, such that neonatal calves have concentrations significantly higher than those observed in older animals ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Russell and Roussel, 2007Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
). Similarly, the highest values of total and unconjugated bilirubin concentrations observed in the lambs at 30 days of age appear to represent the end of the physiological hyperbilirubinemia process of newborns, which is characterized by the widespread destruction of fetal erythrocytes in the mononuclear phagocytic system of the liver and spleen ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
). In the following ages, the dynamics of the total, conjugated, and unconjugated bilirubins probably still reflect the phase of morphofunctional adaptation of the liver to extrauterine life ( Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
).

Concerning the energy profile, it is known that cholesterol has two sources: exogenous, derived from food, and endogenous, synthesized from acetyl-CoA in the liver, under the regulation of exogenous cholesterol intake ( González and Scheffer, 2002González, F. H. D. and Scheffer, J. F. S. 2002. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. p.5-17. In: Avaliação metabólico-nutricional de vacas leiteiras por meio de fluídos corporais (sangue, leite e urina). Anais do 29º Congresso Brasileiro de Medicina Veterinária. Gramado, RS. ). The lambs in this study, as verified among the animals evaluated in the studies by Santos et al. (2015)Santos, R. P.; Sousa, L. F.; Sousa, J. T. L.; Andrade, M. E. B.; Macedo Júnior, G. L. and Silva, S. P. 2015. Parâmetros sanguíneos de cordeiros em crescimento filhos de ovelhas suplementadas com níveis crescentes de propilenoglicol. Revista Brasileira de Ciências Agrárias (Agrária) 10:473-478. https://doi.org/10.5039/agraria.v10i3a4924
https://doi.org/10.5039/agraria.v10i3a49...
and Cruz et al. (2017)Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
, showed a decrease in total cholesterol concentrations with advancing age as a consequence of the modifications to the diet during the first months of life. The dynamics of this parameter is directly influenced by the level of milk intake and metabolizable energy in the diet ( Table 3 ). Initially, the concentrations tend to be high due to the intake of colostrum and milk rich in fats; however, as the animals are weaned and begin to ingest a diet with a higher amount of fodder and concentrated ration with a lower energy content in the form of lipids, the cholesterolemia should decrease ( Fernandes et al., 2012Fernandes, S. R.; Monteiro, A. L. G.; Dittrich, R. L.; Salgado, J. A.; Silva, C. J. A.; Silva, M. G. B.; Beltrame, O. C. and Pinto, P. H. N. 2012. Early weaning and concentrate supplementation on the performance and metabolic profile of grazing lambs. Revista Brasileira de Zootecnia 41:1292-1300. https://doi.org/10.1590/S1516-35982012000500029
https://doi.org/10.1590/S1516-3598201200...
; Santos et al., 2015Santos, R. P.; Sousa, L. F.; Sousa, J. T. L.; Andrade, M. E. B.; Macedo Júnior, G. L. and Silva, S. P. 2015. Parâmetros sanguíneos de cordeiros em crescimento filhos de ovelhas suplementadas com níveis crescentes de propilenoglicol. Revista Brasileira de Ciências Agrárias (Agrária) 10:473-478. https://doi.org/10.5039/agraria.v10i3a4924
https://doi.org/10.5039/agraria.v10i3a49...
).

The dynamics of triglycerides observed in the first months of life of the lambs resembled that observed by Cruz et al. (2017)Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
, showing a drop in triglyceride concentrations after 30 days of age. As in the case of cholesterol, this variation might have been caused by the restriction in milk intake and changes in feeding management ( Table 3 ), as well as by the improvement in hepatic maturation and the ability to metabolize lipids ( Bennis et al., 1992Bennis, A.; La Farge, F.; Bézille, P.; Valdiguié, P.; Rico, A. G. and Braun, J. P. 1992. Effects of age of newborn and delivery by female goats on plasma lipids and lipoproteins. Small Ruminant Research 9:243-253. https://doi.org/10.1016/0921-4488(92)90154-V
https://doi.org/10.1016/0921-4488(92)901...
; Delfino et al., 2014Delfino, J. L.; Barbosa, V. M.; Gondim, C. C.; Oliveira, P. M.; Nasciutti, N. R.; Oliveira, R. S. B. R.; Tsuruta, S. A.; Mundim, A. V. and Saut, J. P. E. 2014. Perfil bioquímico sérico de bezerros senepol nos primeiros 120 dias de idade. Semina: Ciências Agrárias 35:1341-1350. https://doi.org/10.5433/1679-0359.2014v35n3p1341
https://doi.org/10.5433/1679-0359.2014v3...
).

On the other hand, the glycemia in ruminants is not influenced much by feeding, since it is regulated by an efficient hormonal homeostatic mechanism that aims to keep its concentration constant ( González and Scheffer, 2002González, F. H. D. and Scheffer, J. F. S. 2002. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. p.5-17. In: Avaliação metabólico-nutricional de vacas leiteiras por meio de fluídos corporais (sangue, leite e urina). Anais do 29º Congresso Brasileiro de Medicina Veterinária. Gramado, RS. ). Despite the performance of this mechanism, in the neonatal period and during the growth phase, glycemia is greatly influenced by age ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Bórnez et al., 2009Bórnez, R.; Linares, M. B. and Vergara, H. 2009. Haematological, hormonal and biochemical blood parameters in lamb: Effect of age and blood sampling time. Livestock Science 121:200-206. https://doi.org/10.1016/j.livsci.2008.06.009
https://doi.org/10.1016/j.livsci.2008.06...
; Cruz et al., 2017Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
) and is related to the intake of colostrum and milk, and also to the maturation of the liver, pancreas, and enzymatic activities, as well as to the adaptation of the organism to the extrauterine environment ( Kaneto et al., 2004Kaneto, F. M.; Coelho, C. S.; Leal, M. L. R.; Lisboa, J. A. N. and Benesi, F. J. 2004. Blood glucose and Anion Gap of healthy female Holstein calves during the first month of life. Ars Veterinaria 20:291-298. ). Thus, it is believed that the decrease in glucose observed in the lambs at 60 days of age is still the result of the action of these factors associated with age.

Concerning the enzymatic profile, it is recognized that GGT is localized mainly in the kidneys, pancreas, and intestines and shows high activity in the liver. Therefore, it is considered hepatospecific and an important indicator for hepatobiliary diseases and cholestasis in sheep ( Russell and Roussel, 2007Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
; Kaneko et al., 2008Kaneko, J. J.; Harvey, J. W. and Bruss, M. L. 2008. Clinical biochemistry of domestic animals. 6th ed. Academic Press, San Diego. ). It is also present in the epithelium of the ducts of the mammary glands, so that ovine colostrum has high concentrations of GGT. Thus, under normal conditions, such as among the lambs in this study, its high serum concentration at 30 days of age would still result from its high absorption via colostrum in the first 24-48 h of life, using the same mechanism of absorption as for immunoglobulin G (IgG), and its decrease would be due to its deactivation and/or physiological degradation with advancing age ( Britti et al., 2005Britti, D.; Massimini, G.; Peli, A.; Luciani, A. and Boari, A. 2005. Evaluation of serum enzyme activities as predictors of passive transfer status in lambs. Journal of the American Veterinary Medical Association 226:951-955. https://doi.org/10.2460/javma.2005.226.951
https://doi.org/10.2460/javma.2005.226.9...
; Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
).

Aspartate aminotransferase is present in several tissues, but is localized mainly in the liver, in skeletal and cardiac muscle tissue, erythrocytes, and kidneys ( González and Scheffer, 2002González, F. H. D. and Scheffer, J. F. S. 2002. Perfil sanguíneo: ferramenta de análise clínica, metabólica e nutricional. p.5-17. In: Avaliação metabólico-nutricional de vacas leiteiras por meio de fluídos corporais (sangue, leite e urina). Anais do 29º Congresso Brasileiro de Medicina Veterinária. Gramado, RS. ). Britti et al. (2005)Britti, D.; Massimini, G.; Peli, A.; Luciani, A. and Boari, A. 2005. Evaluation of serum enzyme activities as predictors of passive transfer status in lambs. Journal of the American Veterinary Medical Association 226:951-955. https://doi.org/10.2460/javma.2005.226.951
https://doi.org/10.2460/javma.2005.226.9...
and Cruz et al. (2017)Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
also observed a positive correlation between AST concentration and age of lambs. It is believed that the gradual increase in AST up to 120 days of age resulted from the combination of an increase in mass and muscle activity and an improvement in the endogenous production of this enzyme with the development of the animal ( Feitosa et al., 2007Feitosa, F. L. F.; Mendes, L. C. N.; Peiró, J. R.; Cadioli, F. A.; Yanaka, R.; Bovino, F.; Féres, F. C. and Perri, S. H. V. 2007. Influência da faixa etária nos valores de enzimas hepáticas e de uréia e creatinina em bezerros Holandeses do nascimento até os 365 dias de vida. Ciência Veterinária nos Trópicos 10:54-61. ; Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Cruz et al., 2017Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
).

Creatine kinase is a muscle-specific enzyme characterized as a very sensitive bioindicator of the degree of activity, damage and/or muscular effort ( Russell and Roussel, 2007Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
; Bórnez et al., 2009Bórnez, R.; Linares, M. B. and Vergara, H. 2009. Haematological, hormonal and biochemical blood parameters in lamb: Effect of age and blood sampling time. Livestock Science 121:200-206. https://doi.org/10.1016/j.livsci.2008.06.009
https://doi.org/10.1016/j.livsci.2008.06...
). Bórnez et al. (2009)Bórnez, R.; Linares, M. B. and Vergara, H. 2009. Haematological, hormonal and biochemical blood parameters in lamb: Effect of age and blood sampling time. Livestock Science 121:200-206. https://doi.org/10.1016/j.livsci.2008.06.009
https://doi.org/10.1016/j.livsci.2008.06...
verified that in different stress conditions, older lambs show higher levels of CK than lambs still in suckling, and Antunović et al. (2012)Antunović, Z.; Šperanda, M.; Senčić, Đ.; Novoselec, J.; Steiner, Z. and Djidara, M. 2012. Influence of age on some blood parameters of lambs in organic production. Macedonian Journal of Animal Science 1:11-15. did not observe CK variation among lambs with 30 and 70 days of age. According to Braun et al. (2010)Braun, J. P.; Trumel, C. and Bézille, P. 2010. Clinical biochemistry in sheep: A selected review. Small Ruminant Research 92:10-18. https://doi.org/10.1016/j.smallrumres.2010.04.002
https://doi.org/10.1016/j.smallrumres.20...
, CK has high intramuscular activity and sensitivity and might vary quickly after minimal damage. Russell and Roussel (2007)Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
and Lepherd et al. (2009)Lepherd, M. L.; Canfield, P. J.; Hunt, G. B. and Bosward, K. L. 2009. Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs. Australian Veterinary Journal 87:5-11. https://doi.org/10.1111/j.1751-0813.2008.00382.x
https://doi.org/10.1111/j.1751-0813.2008...
reported variations caused by the instability of this enzyme even in the face of common activities of routine management, such as restraint and weighing of animals, or as a result of intramuscular injections, exercise, or physical effort. Therefore, the possibility that the variations in the present study might have occurred due to subtle differences in movement and the time for animal restraint for the blood collection at different times of evaluation cannot be ruled out.

Observing the comparison of biochemical parameters between the lambs and adult sheep, it was confirmed that the biochemical values of younger animals often differ from the reference intervals for adults. Values for total globulins, creatinine, triglycerides, and CK are still far from the values established for adults. However, some other parameters are close to the adult reference interval (total proteins, albumin, urea, glucose, and GGT), but could still result in a misinterpretation of findings, and others are within the intervals of normal physiological variation for adults of the species (as in the case of total, conjugated, and unconjugated bilirubins, total cholesterol, and AST).

In the case of triglycerides, although Kaneko et al. (2008)Kaneko, J. J.; Harvey, J. W. and Bruss, M. L. 2008. Clinical biochemistry of domestic animals. 6th ed. Academic Press, San Diego. did not present values for comparison, Caldeira et al. (2007)Caldeira, R. M.; Belo, A. T.; Santos, C. C.; Vazques, M. I. and Portugal, A. V. 2007. The effect of body condition score on blood metabolites and hormonal profiles in ewes. Small Ruminant Research 68:233-241. https://doi.org/10.1016/j.smallrumres.2005.08.027
https://doi.org/10.1016/j.smallrumres.20...
found a value of 12.22 mg dL−1 in ewes with balanced metabolic status, which corresponds to less than half the value observed in the lambs. However, the values of the lambs were below the value of 40.7 mg dL−1 observed by Carlos et al. (2015)Carlos, M. M. L.; Leite, J. H. G. M.; Chaves, D. F.; Vale, A. M.; Façanha, D. A. E.; Melo, M. M. and Soto-Blanco, B. 2015. Blood parameters in the Morada Nova sheep: influence of age, sex, and body condition score. The Journal of Animal and Plant Sciences 25:950-955. in Morada Nova lambs aged less than six months, possibly due to the difference between the breeds and food management, and approached the value of 32.6 mg dL−1 observed by Cruz et al. (2017)Cruz, R. E. S.; Rocha, F. M.; Sena, C. V. B.; Noleto, P. G.; Guimarães, E. C.; Galo, J. A. and Mundim, A. V. 2017. Effects of age and sex on blood biochemistry of Dorper lambs. Semina: Ciências Agrárias 38:3085-3094. https://doi.org/10.5433/1679-0359.2017v38n5p3085
https://doi.org/10.5433/1679-0359.2017v3...
in Dorper lambs between 15 and 121 days of age, still remaining slightly lower, probably due to the greater precocity in the initial age of the evaluations by these authors.

It is also important to note that the CK values of the lambs are much higher than those of the adults, which would lead to serious misinterpretations if compared directly with the reference values of Kaneko et al. (2008)Kaneko, J. J.; Harvey, J. W. and Bruss, M. L. 2008. Clinical biochemistry of domestic animals. 6th ed. Academic Press, San Diego. , but they are close to the reference interval established by Lepherd et al. (2009)Lepherd, M. L.; Canfield, P. J.; Hunt, G. B. and Bosward, K. L. 2009. Haematological, biochemical and selected acute phase protein reference intervals for weaned female Merino lambs. Australian Veterinary Journal 87:5-11. https://doi.org/10.1111/j.1751-0813.2008.00382.x
https://doi.org/10.1111/j.1751-0813.2008...
for weaned Merino lambs between nine to 16 weeks of age (ranging from 180 to 454 U L−1).

During the first months of life, the age factor is naturally associated with several processes of changes, whether due to variations in feed management (colostrum intake, suckling, weaning, inclusion of solid feeds in the diet), or changes from intrauterine to extrauterine environment, which triggers new biological challenges and intense changes in the maturation of organs, body systems, and metabolic activity, or by evident changes in the body growth of the animal. These changes alter the blood biochemical profile, so that this variation structure cannot be considered normal in other ages ( Kaneto et al., 2004Kaneto, F. M.; Coelho, C. S.; Leal, M. L. R.; Lisboa, J. A. N. and Benesi, F. J. 2004. Blood glucose and Anion Gap of healthy female Holstein calves during the first month of life. Ars Veterinaria 20:291-298. ; Benesi et al., 2005Benesi, F. J.; Coelho, C. S.; Leal, M. L. R.; Mirandola, R. M. S. and Lisbôa, J. A. N. 2005. Biochemical parameters for evaluation of renal function and fluid and electrolyte balance of healthy female Holstein calves during the first month of life. Brazilian Journal of Veterinary Research and Animal Science 42:291-298. https://doi.org/10.11606/issn.1678-4456.bjvras.2005.26424
https://doi.org/10.11606/issn.1678-4456....
; Fernandes et al., 2012Fernandes, S. R.; Monteiro, A. L. G.; Dittrich, R. L.; Salgado, J. A.; Silva, C. J. A.; Silva, M. G. B.; Beltrame, O. C. and Pinto, P. H. N. 2012. Early weaning and concentrate supplementation on the performance and metabolic profile of grazing lambs. Revista Brasileira de Zootecnia 41:1292-1300. https://doi.org/10.1590/S1516-35982012000500029
https://doi.org/10.1590/S1516-3598201200...
; Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
).

For example, the evaluation of the metabolic profile according to age, during suckling or fattening, can expose specific nutritional mistakes, which could otherwise be undetectable because animal uses its own body reserves ( Antunović et al., 2012Antunović, Z.; Šperanda, M.; Senčić, Đ.; Novoselec, J.; Steiner, Z. and Djidara, M. 2012. Influence of age on some blood parameters of lambs in organic production. Macedonian Journal of Animal Science 1:11-15. ). Also, in this period, higher values for albumin, urea, triglycerides, glucose, and GGT, together, can be related to the morphofunctional adaptation of the liver, but in adults, they would probably indicate some kind of liver problem ( Feitosa et al., 2007Feitosa, F. L. F.; Mendes, L. C. N.; Peiró, J. R.; Cadioli, F. A.; Yanaka, R.; Bovino, F.; Féres, F. C. and Perri, S. H. V. 2007. Influência da faixa etária nos valores de enzimas hepáticas e de uréia e creatinina em bezerros Holandeses do nascimento até os 365 dias de vida. Ciência Veterinária nos Trópicos 10:54-61. ; Souza et al., 2014Souza, D. F.; Monteiro, A. L. G.; Dittrich, R. L.; Schmidt, E. M. S.; Fernandes, S. R. and Beltrame, O. C. 2014. Dinâmica pré e pós-colostral de parâmetros bioquímicos em cordeiros. Ciência Animal Brasileira 15:313-321. https://doi.org/10.1590/1809-6891v15i324807
https://doi.org/10.1590/1809-6891v15i324...
).

It is still important to remember that some diseases are more predisposed to certain ages. Thus, being able to rule out normal changes due to age in the clinical biochemical profile ensures a greater accuracy for this evaluation, a better chance to confirm the diagnosis of a disease, and a quick and effective intervention, preventing it from becoming chronic or leading to death. In addition, it allows surgical procedures to be performed with greater safety ( Mohri et al., 2007Mohri, M.; Sharifi, K. and Eidi, S. 2007. Hematology and serum biochemistry of Holstein dairy calves: Age related changes and comparison with blood composition in adults. Research in Veterinary Science 83:30-39. https://doi.org/10.1016/j.rvsc.2006.10.017
https://doi.org/10.1016/j.rvsc.2006.10.0...
; Russell and Roussel, 2007Russell, K. E. and Roussel, A. J. 2007. Evaluation of the ruminant serum chemistry profile. Veterinary Clinics of North America: Food Animal Practice 23:403-426. https://doi.org/10.1016/j.cvfa.2007.07.003
https://doi.org/10.1016/j.cvfa.2007.07.0...
; Kaneko et al., 2008Kaneko, J. J.; Harvey, J. W. and Bruss, M. L. 2008. Clinical biochemistry of domestic animals. 6th ed. Academic Press, San Diego. ; Delfino et al., 2014Delfino, J. L.; Barbosa, V. M.; Gondim, C. C.; Oliveira, P. M.; Nasciutti, N. R.; Oliveira, R. S. B. R.; Tsuruta, S. A.; Mundim, A. V. and Saut, J. P. E. 2014. Perfil bioquímico sérico de bezerros senepol nos primeiros 120 dias de idade. Semina: Ciências Agrárias 35:1341-1350. https://doi.org/10.5433/1679-0359.2014v35n3p1341
https://doi.org/10.5433/1679-0359.2014v3...
).

5. Conclusions

The biochemical parameters of healthy ½ White Dorper × ½ Suffolk female lambs are influenced by age until four months of life. However, the magnitude of variation in the parameters within this period is small and is often associated with the nutritional, immunological, and adaptation physiological factors. Except for the total, conjugated, and unconjugated bilirubins, total cholesterol, and AST means, the values of the biochemical parameters of female lambs differ from the reference intervals established for adult sheep. Thus, it is recommended that the interpretation of tests performed on animals in the growth phase should be made based on specific reference intervals for this age group.

Acknowledgments

The authors thank God and all the students and staff of the LAPOC-UFPR (especially Raquel Cristina Bredt Greca) and of the Laboratório de Patologia Clínica Veterinária of the Universidade Federal do Paraná. Alda Lúcia Gomes Monteiro is member of the MARCARNE Network, funded by CYTED (ref. 116RT0503). Alda Lúcia Gomes Monteiro thanks the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq) for the researcher fellowship.

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Publication Dates

  • Publication in this collection
    25 Sept 2020
  • Date of issue
    2020

History

  • Received
    22 Aug 2019
  • Accepted
    17 June 2020
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