Indian Journal of Animal Research

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Indian Journal of Animal Research, volume 57 issue 3 (march 2023) : 353-359

Relationship of Oxidative Stress and Some Blood Parameters with Quarters Affected by Mastitis in Dairy Cows

T. Akkuş1,*, P.F. Polat Dinçer2, M. Ekici3, Z. Yerlikaya4
1Department of Obstetrics and Gynaecology, Faculty of Veterinary Medicine, Harran University, Sanliurfa-Turkey.
2Department of Internal Medicine, Faculty of Veterinary Medicine, Dokuz Eylül University, Izmir-Turkey.
3Department of Physiology, Faculty of Veterinary Medicine, Cumhuriyet University, Sivas-Turkey.
4Department of Microbiology, Faculty of Veterinary Medicine, Firat University, Elazig-Turkey.
Cite article:- Akkuş T., Dinçer Polat P.F., Ekici M., Yerlikaya Z. (2023). Relationship of Oxidative Stress and Some Blood Parameters with Quarters Affected by Mastitis in Dairy Cows . Indian Journal of Animal Research. 57(3): 353-359. doi: 10.18805/IJAR.BF-1590.
Background: This study was conducted to evaluate the relationship between oxidative stress and some blood parameters in different number of quarters affected with and without sub-clinical mastitis (SM). 

Methods: A total of 50 lactating Holstein dairy cows were used in the study. The study groups were as follows; Group 1 (negative test results and no SM), Group 2 (SM in one quarter), Group 3 (SM in two quarters), Group 4 (SM in three quarters) Group 5 (SM in four quarters). Milk samples were obtained from the infected quarters for both Somatic Cell Count (SCC) measurement and bacteriological growth/bacterial identification. Blood was collected for analysis of oxidative stress parameters (total oxidative capacity and total antioxidant capacity) and some blood parameters (glucose, total cholesterol, total bilirubin, aspartate aminotransferase [AST], alanine aminotransferase [ALT]). 

Result: Somatic Cell Count (SCC) was significantly lower in Group 1 than in Groups 2, 3, 4 and 5 (P<0.001). Glucose and total cholesterol levels were significantly higher in Group 5 than in Groups 1, 2, 3 and 4 (P<0.001). A significant difference was determined between all groups in respect of AST and ALT activities (P<0.001). The Total Oxidative Capacity (TOC) and oxidative stress index value (OSI) levels were significantly lower in Group 1 than in Groups 2, 3, 4 and 5 (P<0.001), while Total Antioxidant Capacity (TAC) levels were significantly higher (P<0.001). In conclusion, it was found that oxidative stress and blood-biochemistry values are significantly affected in dairy cows with sub-clinical mastitis.
Mastitis is one of the most important diseases in dairy farming and is closely related to oxidative stress (Abuelo et al., 2015). Reactive oxygen products (ROS) are the most common oxidant substances in biological systems, which are required at physiological levels for reproductive functions, including oocyte maturation, folliculogenesis, luteolysis, ovulation and cyclic endometrial changes. However, ROS at higher than physiological levels contribute to various pathological conditions that may affect reproductive performance such as retained placenta, quarter edema, mastitis and infertility (Puppel et al., 2015). ROS are enzymatpically repaired by antioxidant substances, but when the generation of free radicals exceeds the defence capacity of antioxidants, oxidative stress develops. Oxidative stress damages the macro components such as DNA, lipids and proteins, thereby disrupting cell structure, especially immune cells. Furthermore, it is known that excessive oxidative stress can result in pathological disorders of tissues and organs. These pathological disorders develop with impairments of especially the heart, skeletal muscle, liver and blood cell functions that require high energy and immunological deficiencies (Kuhn et al., 2018). Antioxidant and oxidant indices are biomarkers which have been recently used for the detection of sub-clinical mastitis. Polymorphonuclear leukocytes (PMNs), which are the dominant cell type in mammary tissues, and secretions during inflammation show their bactericidal effects through a respiratory burst that produces ROS and reactive nitrogen species (RNS). Therefore, an increase in the number and activity of PMNs in milk resulting from mastitis will be associated with changes in the oxidative markers in milk (Amiri et al., 2020). Serum or plasma concentrations of different oxidants/antioxidants can be measured individually in laboratories, but these measurements are time-consuming, expensive and require complex techniques. Since the individual measurement of different oxidant/antioxidant molecules is not practical, the total oxidant/antioxidant capacity of a sample is measured and this is known as the total antioxidant capacity (TAC), and total oxidant capacity (TOC) (Erel, 2005; Erel, 2004). The diagnosis of mastitis can be made by clinical examination of udder and milk, and the chemical, physical, cellular and microbiological examination of milk. In addition, the biochemical changes caused by this disease in blood and body fluids can be determined in various laboratory tests (Kitchen et al., 1980). Enzymes (aspartate aminotransferase, lactate dehydrogenase, and alkaline phosphatase) found in the milk and blood of infected animals are considered biomarkers of udder health because the levels increase during inflammation in animals with mastitis. Increased levels of these enzymes in milk and blood serum may be associated with tissue damage in the udder parenchyma (Kalantari et al., 2013). Examining the concentration of bilirubin, albumin, glucose and cholesterol in the blood serum, as well as the activity of AST, ALT enzymes, and the appropriate markers for liver function both allow an overall assessment of liver status and provide information about the production potential of dairy cows (Djokovic et al., 2013).

The aim of this study was to reveal the relationship between oxidant-antioxidant status and some blood parameters in different number of quarters affected with and without sub-clinical mastitis in dairy cows.
Selection of animals and test protocol
 
This study was conducted on 50 Holstein breed dairy cows, aged 2-5 years, selected by a random sampling method (a total of 200 quarter milk samples). All the cows had the same nutrition of grass silage, corn silage, and hay, together with concentrated feed based on factory feed and barley and were managed under the same conditions on a privately owned dairy farm in Eyyübiye District of Şanlıurfa province, south-east Turkey and the study was carried out in March-April 2021. The cows included in the study were those that had a normal previous calving and had not received any treatment for the last three months according to the farm records. First, milk samples were obtained following the asepsis/antisepsis rules and CMT was performed (Jackson and Cockcroft, 2002). The groups were formed according to the quarters with mastitis. According to the test results, 5 study groups were created; Group 1 were cows negative in all 4 quarters and the cows in Groups 2-5 had sub-clinical mastitis in one, two, three or four quarters, respectively. Each study group consisted of 10 animals. All cows in the study were in the mid-lactation period (100-200 days following birth). None of the cows had been given antibiotic treatment in the last month, and quarters appeared normal on clinical examination but had CMT positivity. Milk samples were taken from the infected quarters of the animals in each group for SCC measurement and bacterial culture/bacteria identification. Blood samples were taken and after centrifugation at 3000 rpm for 10 min, the serum was removed for analysis of oxidative stress parameters (TOC and TAC) and some blood parameters (ALT, AST, Glucose, Total Cholesterol, Total Bilirubin).

California mastitis test (CMT) and somatic cell count (SCC)
 
Milk samples taken from each of the four quarters were transferred into the test container with four separate compartments. For the CMT, an equal amount of milk was mixed with the test solution containing bromocresol purple and anionic detergent (2 ml milk and 2 ml test solution). By rotating the test plate slowly, alterations such as color changes or gel formation were evaluated. Milk SCC was determined using an automatic somatic cell counter (Lactoscan SCC ®, Nova Zagora, Bulgaria) on a private dairy farm. According to the CMT and SCC results, 10 cows were CMT negative (mixed liquid, no sediment) and SCC<400,000/ml, and 40 cows were CMT +1 positive (with marked sediment, no gel form) and SCC>400,000/ml (Ruegg and Reinemann, 2002).
 
Milk and blood samples
 
Quarters were wiped with 70% alcohol. After removing  few strips of milk to remove saprophyte microorganisms, a 10 ml milk sample was taken from each quarter into falcon tubes. The milk samples taken were sent to Firat University, Faculty of Veterinary Medicine, Department of Microbiology, under cold chain conditions for the bacteria isolation to be performed. Blood samples of 10 ml taken from vena jugularis into tubes containing clotting activator were transported to the laboratory in ice within 30 min, then centrifuged at 3000 g for 10 minutes, and the serum obtained was stored at -80°C until TAC-TOC measurement and biochemistry analyses were performed.
 
Bacteria isolation and identification
 
In the laboratory, cultures were prepared by adding 0.1 ml of the milk samples to the general and selective media (blood agar, MacConkey agar and Edward’s medium). The cultures were incubated at 37°C for 24-48 hours under aerobic conditions, then were evaluated in respect of colony growth during incubation. Macroscopic examination of the growing colonies in the culture environments was made and the colonies were purified and classified according to the MALDI-TOF MS system (Matrix-mediated laser desorption ionization-flight time mass spectrometry database v2.0, bioMerieux, France) (Koneman et al., 1997).
 
Some blood parameters, determination of total antioxidant capacity (TAC), total oxidant capacity (TOC) and oxidative stress index value (OSI)
 
Glucose, T-cholesterol, BUN, T-bilirubin, AST and ALT activities were measured using an Arkray Spotchem EZ SP-4430 dry system biochemistry analyzer (Koka-Shi ®, Shiga, Japan) (Dülgeroglu, 2018). Serum TAC levels were measured using a commercial kit (Rel Assay Diagnostics kit, Mega Medicine®, Gaziantep, Turkey) at 660 nm spectrophotometrically (Molecular Device SpectraMax M5 Plate Reader®, Pleasanton, California, United States) (Erel, 2004). Serum TOC levels were determined using a commercial kit (Rel Assay Diagnostics kit, Mega Medicine, Gaziantep, Turkey) at 530 nm spectrophotometrically (Molecular Device SpectraMax M5 Plate Reader, Pleasanton, California, United States) (Erel, 2005). The ratio of TOC level to TAC level was defined as the Oxidative Stress Index (OSI) (Kaya et al., 2016).
 
Statistical analysis
 
Statistical analysis of the data was performed using Statistical Package for the Social Sciences (SPSS for Windows; version 22.0) software. The conformity of variables to normal distribution was examined using visual (histogram and probability graphs) and analytical methods (Kolmogorov-Smirnov/Shapiro-Wilk tests). Descriptive analyses were stated as mean ± standard error of mean values for normally distributed variables. Data showing normal distribution were evaluated using the One-way ANOVA test. If there was a significant difference between the groups, the comparison was performed using the post-hoc Scheffe test. The homogeneity of the variances was determined with the Levene test. A value of P<0.05 was accepted as statistically significant.
The CMT results of the study groups are presented in Table 1. All the quarters of the 10 animals in Group 1 were CMT and bacteriology negative.

Table 1: Determination of cows with sub-clinical mastitis.



In Groups 2-5, the number of positives CMT were according to scheduling 1-4 quarters respectively. In milk samples taken from CMT positive quarters, aerobic bacteria were isolated in 8 (80%) in Group 2, in 14 (70%) in Group 3, in 23 (76.6%) in Group 4, and in 32 (80%) in Group 5. When evaluated as a total, aerobic bacteria isolation was achieved in 77 (77%) of 100 CMT positive quarters of 40 lactating cows.
 
Bacteria isolated from cultivated milk
 
The bacteria isolated from the milk sample cultures according to the groups are presented in Table 2. The micro-organisms isolated from 77 milk samples were as follows: Staphylococcus aureus in 35 (45.4%), Streptococcus agalactiae in 15 (19.4%), Streptococcus dysgalactiae in 10 (12.9%), Micrococcus spp. in 4 (5.1%), Coagulase Negative Staphylococcus (CNS) in 3 (3.8%), Corynebacterium bovis in 3 (3.8%), Escherichia coli in 3 (3.8%), Bacillus spp. in 1 (1.2%), Arcanobacterium pyogenes in 1 (1.2%), Pasteurella multocida in 1 (1.2%) and Citrobacter diversus in 1 (1.2%).

Table 2: Bacteria species isolated with MALDI-TOF MS (Matrix-mediated laser desorption ionization-flight time mass spectrometry database v2.0, bioMerieux, France).



In a previous study, the rates of micro-organisms isolated and identified from 125 CMT positive quarter milk samples were as follows: 47.3% Staph. aureus, 16.3% C. pyogenes, 8.2% E. coli, 6.5% Candida albicans, 6% S. agalactiae and 15.7% other micro-organisms (Ates et al., 1991). In other studies, Staph. aureus has been reported to be the main pathogen most frequently isolated in sub-clinically infected quarters in Belgium and other regions and countries (Sampimon et al., 2005; Pitkale et al., 2004; Wilson et al., 1997). Similar to the findings of previous research, the present study showed that Staph. aureus appears to be the most commonly isolated bacteria in milk with sub-clinical mastitis. When other factors were considered, although the rates varied, the bacteria isolated were similar to those in other studies. Changes in the prevalence of Staph. aureus in the herd can be explained by differences between herds regarding post-milking teat dipping and dry-term udder treatment (Hogan et al., 1987). Studies have reported that the prevalence of Str agalactiae varies between 8.5% (Wilson et al., 1997), 0.1% (Pitkale et al., 2004) and 1-2% (Andersen et al., 2003). In the present study, this rate was found to be 19.4%. This situation, which is contrary to the literature, was thought to be due to the fact that the mammary health control program was not fully implemented on the farm where the study was conducted. In addition, coliform bacteria, which are generally included in short-term acute clinical mastitis cases, have been reported to have a low prevalence in parallel with the current study (Hoblet et al., 1991).
 
Some blood parameters
 
The blood biochemistry values are presented in Table 3. Glucose and total cholesterol were significantly higher in Group 5 than in Groups 1, 2, 3 and 4 (P<0.001).

Table 3: Blood biochemical parameters in the groups.



There was no significant difference between Groups 1, 2, 3 and 4 (P>0.05). Total bilirubin was significantly lower in Group 1 compared to Groups 2, 3, 4 and 5 (P<0.001). It was significantly lower in Group 2 than in Groups 4 and 5 (P<0.001). It was significantly lower in Group 3 than in Group 5 (P<0.001). There was no significant difference between Groups 2 and 3, Groups 3 and 4 and Groups 4 or 5 (P>0.05).

In this study, the relationship was evaluated between blood-biochemistry values such as glucose, T-cholesterol, T-bilirubin, AST and ALT, measured to assess liver function. Previous studies have reported that activities of AST and ALT enzymes increase in accordance with the elevation in CMT score (Qayyum et al., 2018). In another study, milk and blood AST and ALT activities were higher in camels with sub-clinical mastitis compared to healthy animals (Ali et al., 2016). In the current study, the increase in the values measured from the cows with sub-clinical mastitis was seen to be consistent with the data found in literature. When the effect of the number of infected quarters on the blood-biochemistry values is examined, glucose and T-cholesterol levels were determined to be lowest in Group 1 and highest in Group 5. While there was no statistically significant difference in these measurements between Groups 1, 2, 3, and 4, the difference between these groups and Group 5 was statistically significant, suggesting that the liver metabolic load may have increased due to the number of affected quarters. Similarly, T-bilirubin, AST and ALT were measured at the lowest activity in Group 1 and at the highest level in Group 5. The difference in the total bilirubin levels between Group 1 and the other groups (with sub-clinical mastitis) was found to be increasingly significant. The AST and ALT activities were significantly different in all the groups as the number of infected quarters increased. With the increase in the number of infected quarters, so the activities of liver enzyme parameters increased significantly (Ali et al., 2016). This increase was thought to be related to microcirculation permeability as a result of tissue damage caused by free radicals in the quarter. It was thought that evaluations of sub-clinical mastitis should be made not only on an animal basis but also in terms of infected quarters.
 
Findings related to somatic cell count (SCC)
 
Ten cows in each group; from all CMT negative quarters in Group 1, 10 CMT positive in Group 2, 20 CMT positive in Group 3, 30 CMT positive in Group 4 and 40 CMT positive quarters in Group 5 SCC levels were established by taking the average of milk samples. When the SCC and CMT results were compared, the average SCC in the quarters in Group 1, which was CMT negative, was 155.05 cells/ml, 792.08 cells/ml in Group 2, 754.55 cells/ml in Group 3, 605.84 cells/ml in Group 4, and 695.33 cells/ml in Group 5 quarters. The difference in mean SCC values between Group 1 and the other groups was statistically significant (P<0.001), and no significant difference was observed between the sub-clinical mastitis groups (P>0.001) (Fig 1).

Fig 1: The number of somatic cell count (SCC) in the groups. ***: P<0.001. The values in the column chart represent the mean ± SEM.


 
Total oxidant capacity (TOC), total antioxidant capacity (TAC) and oxidative stress index (OSI) measurements
 
Total Oxidative Capacity (TOC) and oxidative stress index value (OSI) levels were significantly lower in Group 1 than in Groups 2, 3, 4 and 5 (P<0.001), while Total Antioxidant Capacity (TAC) levels were significantly higher (P<0.001), (Fig 2, Fig 3, Fig 4).

Fig 2: Total oxidant capacity (TOC) in the groups. ***: P<0.001. The values in the column chart represent the mean ± SEM.



Fig 3: Total antioxidant capacity (TAC) in the groups. ***: P<0.001. The values in the column chart represent the mean ± SEM.



Fig 4: Oxidative stress index (OSI) value in the groups (arbitrary unit). ***: P<0.001. The values in the column chart represent the mean ± SEM.



Studies on oxidative stress are among current topics and many scientific studies have been conducted in this area (Abuelo et al., 2013). Oxidative stress is defined as an imbalance in favor of oxidants between oxidant and antioxidant substances (Puppel et al., 2015). When free radicals and antioxidant substances encounter each other in the body, antioxidants prevent damage by inhibiting target molecules or by delaying oxidation thereby protecting the organism against tissue damage (Puppel et al., 2015). Antioxidants have been found to have an antilipolytic effect, but free radicals disrupt the insulin mechanism, thereby stimulating lipolysis. In the case of oxidative stress, lipolysis is constantly active, and liver metabolic load increases in this case (Abuelo et al., 2016). Tissue damage caused by intramammary inflammation results in the generation of reactive oxygen species (ROS), increasing the incidence of oxidative stress in mammary tissue, which can lead to increased permeability of microcirculatory arteries due to free radical injury. In a previous study investigating the oxidant/antioxidant status in cows with sub-clinical mastitis, it was emphasized that MDA and NO levels were higher than that of healthy control groups, and TAC and GSH levels were lower, indicating the contribution of udder-related oxidative stress and potential oxidative damage (Saleh et al., 2022; Sadek et al., 2017). Similarly, it has been reported that MDA and H2O2 (Hydrogen peroxide) levels are increased and TAC levels are decreased in blood and milk serum of cows with sub-clinical mastitis compared to the control group (Nedić et al., 2019). Moreover, TAC and MDA concentrations have been reported to increase significantly over time in untreated cows with sub-clinical mastitis (Tabatabaee et al., 2021). Higher SCCs have also been strongly correlated with higher MDA levels (Yakan et al., 2021). Total antioxidant capacity can be used to provide a simple understanding of the antioxidant status in the body (Farghali et al., 2021; Abdel-Saeed and Salem, 2019). The importance of TAC and TOC levels in monitoring oxidative stress-related diseases such as mastitis and the transition period in dairy cows has been emphasized (Amiri et al., 2020; Kurt et al., 2019; Turk et al., 2017; Andrei et al., 2016; Aydilek et al., 2014; Atakisi et al., 2010; Mandebvu et al., 2003). In previous studies, milk with sub-clinical mastitis has been compared with cow and goat milk samples without sub-clinical mastitis and milk with mastitis has been reported to have higher TOC levels and lower TAC levels (Silanikove et al., 2014; Atakisi et al., 2010). In another study, the TAC level was high in low-SCC milk and low in high-SCC milk in the samples taken according to the density of the somatic cells (Nedić et al., 2019; Andrei et al., 2016). In our study, the serum TOC-TAC level was measured according to the number of infected quarters and the increase in TAC level and decrease in TOC level in animals with sub-clinical mastitis were consistent with the literature data (Silanikove et al., 2014; Atakisi et al., 2010). The use of antioxidants increases as a result of the effect of free radicals that occur due to inflammation, which occurs in mastitis cases, and as a result, the levels of antioxidants decrease. In mammary gland inflammation, more oxygen is used depending on the activity of phagocytic cells that have migrated of phagocytic cells to the site of inflammation. The oxidative stress parameter measurements were determined to have a strong relationship with the number of infected quarters.
In conclusion, it was found that oxidative stress and some blood parameters are significantly affected by infected quarters in cases with sub-clinical mastitis. Staph. aureus was determined to be the main cause of sub-clinical mastitis in the dairy cows in this study, in line with data from other countries. Therefore, udder health control programs should be expanded in dairy cattle enterprises. It can be considered that this study will be of guidance for future studies with greater numbers of animals and examinations at every stage of lactation, especially after birth.
This study was conducted with the permission of the Harran University Animal Experiments Local Ethics Committee (decision no: 2020/04, dated: 09/07/2020).
None of the authors of this article has any conflict of interest.

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