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ISSN : 2287-5824(Print)
ISSN : 2287-5832(Online)
Journal of The Korean Society of Grassland and Forage Science Vol.44 No.4 pp.270-278
DOI : https://doi.org/10.5333/KGFS.2024.44.4.270

Comparison of Nutritional Value, Immunoglobulin G Content and Microbial Community of the Colostrum from Holstein Cows Following Heat Treatment

Gyeongjin Kim1, Chang Seok Park3, Minjung Yoon1,2, Junyoung Kim1, Minseok Kim4, Seunghyun Mun4, Yong Bum Cho5, Miyoung Won6, Eun Joong Kim1,2*
1Department of Animal Science and Biotechnology, Kyungpook National University, Sangju, 37224, Korea
2Research Institute for Innovative Animal Science, Kyungpook National University, Sangju, 37224, Korea
3Yecheon Agricultural Technology Center, Yecheon, 36819, Korea
4Division of Animal Science, College of Agriculture and Life Sciences, Chonnam National University, Gwangju, 61186, Korea
5Department of Animal Resource Science, Sahmyook University, Seoul, 01795, Korea
6Subtropical Livestock Research Institute, National Institute of Animal Science, Rural Development Administration, Jeju, 63242, Korea

†These authors contributed equally to this work. corresponding author


* Corresponding author: Eun Joong Kim, Department of Animal Science and Biotechnology, Kyungpook National University, Sangju, 37224, Korea, Tel: +82-54-530-1228, E-mail: ejkim2011@knu.ac.kr
September 19, 2024 December 23, 2024 December 23, 2024

Abstract


This study was conducted to investigate changes in immunoglobulin G (IgG) concentration, nutrient content, and microbial communities of fresh and heat-treated Holstein colostrum collected from a colostrum bank operated by a local agricultural technology center in Gyeongsangbuk-do, South Korea. Of the 16 colostrum samples, 8 were heated at 60℃ for 30 min under a pressure of 0.9–1 bar. The colostrum samples were stored at −70℃ until use, at which time they were thawed at 50–55℃ in a water bath to analyze IgG levels, chemical composition, and microbiome, which was identified by 16S rRNA gene sequencing using the Illumina MiSeq-PE250 platform. The IgG concentrations were similar in fresh and heat-treated colostrum. The fat, protein, and lactose contents also did not differ in these samples. However, somatic cell count (SCC) was lower in heat-treated colostrum than those in fresh colostrum (p<0.05). At the phylum level for the microbiome of fresh colostrum, Proteobacteria (44.16%) was the most abundant taxa, followed by Bacteroidota (33.26%), Firmicutes (10.04%), Actinobacteriota (7.14%), and a marginal difference in the order of abundance was observed in heat-treated colostrum. At the genus level, bacteria belonging to Sphingomonas, Delftia, Ochrobactrum, Simplicispira, and Lactobacillus were more abundant (p<0.05) in the heat-treated colostrum, while the abundance of Acinetobacter in the fresh colostrum was four times more (p<0.05) than that in the heat-treated colostrum. Our results demonstrated that heating does not affect IgG level and colostrum composition but reduces SCC (p<0.05), suggesting that heat-treated colostrum can potentially be put to further use (e.g., feeding Hanwoo calves) without compromising its quality. Differences in the microbiome between the fresh and heat-treated colostrum were limited. Further studies are required to extensively investigate the quality and safety of colostrum collected from dairy farms to ensure better utilization and processing at a local agricultural technology center.


Colostrum bank , Immunity , Holstein , Hanwoo , Microbiome

초록

    Ⅰ. INTRODUCTION

    After birth, the calf must consume immunoglobulins, especially immunoglobulin G (IgG), by feeding on the colostrum from its dam because the cow’s placenta is not suitable for the delivery of macromolecules, such as immunoglobulins (Morrill et al., 2012). Colostrum reduces the incidence of disease or mortality in calves by the passive transfer of immunoglobulin and has a significant impact on growth and development (Donahue et al., 2012). Hence, consuming colostrum early after birth is critical for the calf’s health and subsequent growth and development (Donahue et al., 2012).

    In the Korean system of cattle raising, supplying colostrum to Hanwoo (Korean beef cattle breed) calves is often difficult because the dam produces low amounts of colostrum after calving (Ahmadi et al., 2021). To solve this problem, experts have suggested that recent supplies of surplus colostrum produced by Holstein cows procured from dairy farms may be frozen for storing and thawed for feeding. However, bacteria, such as Mycobacterium avium spp., Paratuberculosis, Listeria monocytogenes, Campylobacter jeiuni, Escherichia coli, and Salmonella spp., may proliferate during storage by fecal contamination during colostrum collection or toxins may be transmitted to the calves when they ingest the colostrum (Fasse et al., 2021). Contaminated colostrum can cause disease (Elizondo-Salazar et al., 2010); hence, appropriate processing of the colostrum (e.g., heat treatment) has been proposed by experts and beef farmers. Bacteria bind to antibodies and prevent their absorption from the intestines (Johnson et al., 2007). Heating colostrum is known to reduce the bacteria and improve IgG absorption (Johnson et al., 2007); however, when the IgG level in the colostrum reduces to <10 mg/mL because of heat treatment, the calf will not receive sufficient antibodies, i.e., failure of passive transfer occurs (Godden, 2008), which increases the risk of exposure to disease (Smith and Foster, 2007).

    In Korea, local governments operate colostrum banks where Holstein colostrum is stored and supplied mainly to Hanwoo farmers. However, research regarding changes in IgG concentration, nutrients, and the presence of pathogens in fresh and processed colostrum is limited. Therefore, the objective of this study was to investigate changes in IgG levels, nutrient concentration, and microbial communities in fresh and heat-treated colostrum collected from a colostrum bank operated by a local agricultural technology center.

    Ⅱ. MATERIALS AND METHODS

    1. Colostrum preparation

    Sixteen colostrum samples, including the fresh (8 samples) and their heat-treated colostrum (8 samples) from the colostrum bank operated by the Yecheon Agricultural Technology Center, Gyeongsangbuk-do, South Korea, were used.

    Briefly, on the day of calving, colostrum was collected once only through a bucket milking system, followed by twice a day until the third day after calving. Dairy farmers cooperating with the colostrum bank stored this colostrum at -20°C until collected. Once the frozen colostrum was transferred to the colostrum banks, it was then thawed in a 55°C water bath in a speedy manner and filtered through a mesh to remove any hair or potential dirty materials from a mother cow. Then, a kit (AniCheck bovine IgG Blood and Colostrum, Protia, Seoul, South Korea) was used to determine the IgG level in the colostrum instantly and pooled only if the level of the IgG was over 40 g/L. If the level of IgG is lower than 40 g/L, the colostrum was discarded with the thought that this level of IgG in the colostrum might not help improve the passive immunity of Hanwoo calves. At this stage, approximately a 100 mL colostrum was sampled as a “fresh colostrum.” The rest of the colostrum underwent a heat treatment using the equipment established by the colostrum bank (60°C for 30 min). Following the heat treatment, another set of samples was collected as the “heat-treated,” and all samples were stored at -70°C until further analysis. The facilities for heat treatment at the Yecheon Agricultural Technology Center were certified based on the hazard analysis critical control points regulation system. The “fresh” and “heat-treated” colostrum were transferred to our laboratory at Kyungpook National University and analyzed for the level of IgG, nutritive values, and microbiome.

    2. IgG concentration

    After the colostrum samples were diluted 1,000,000 times in 1× dilution buffer C provided by the manufacturer, a bovine IgG enzyme-linked immunosorbent assay (ELISA) kit (catalog number: E11-118, Bethyl Laboratories Inc., Montgomery, TX, USA) was used to determine IgG concentration by following the manufacturer’s instructions. This analysis is based on the sandwich ELISA principle. The antigen (IgG in colostrum) is captured by the antibody that has been adsorbed on the surface of the plate well. Subsequently, an anti-IgG detection antibody is added, and the IgG concentration is determined colorimetrically. Seven standard solutions (167, 55.6, 18.5, 6.17, 2.06, 0.69, 0 ng/mL IgG) were prepared by diluting the standard IgG solution (500 ng/mL) by two times using a dilution buffer. The diluted standard solution and 100 μL colostrum were added to the plate well, incubated at room temperature for 1 h, and washed. Next, 100 μL anti-IgG detection antibody was added, bound to the IgG adsorbed onto the sample, and washed off. Streptavidin-conjugated horseradish peroxidase (HRP) and 3, 3′,5,5′-tetramethylbenzidine (TMB) were added. When the solution turned yellow through a colorimetric reaction, the reaction was stopped using a stop solution. The absorbance of the sample was measured at a wavelength of 450 nm using a Sunrise absorbance microplate reader (Tecan, Männedorf, Switzerland), and the concentration of IgG in each colostrum sample was calculated based on the standard curve.

    3. Colostrum composition

    Colostrum composition (fat, protein, lactose), pH, and somatic cell count (SCC) were analyzed using Lactoscope FTIR Advanced (Delta instruments, Netherlands) and Soma scope MK2 (Delta instruments, Netherlands).

    4. Microbiome analysis of colostrum

    Metagenomic DNA was extracted from colostrum samples using a PowerMax soil DNA isolation kit (Qiagen, Valencia, CA, USA). The universal primers 341F (5ʹ-CCTACGGGNGGCWGCAG-3ʹ) and 805R (5ʹ-GACTA CHVGGGTATCTAATCC-3ʹ) were used to amplify 16S rRNA gene amplicons (Eom et al., 2024), which were then sequenced using the Illumina MiSeq platform (Illumina, San Diego, CA, USA). The resultant 16S rRNA gene amplicon sequences were analyzed using the Quantitative Insights into Microbial Ecology (QIIME2, version 2023.5) software packages (Bolyen et al., 2019). The paired-end amplicon sequences were preprocessed to remove low-quality and chimeric sequences using the DADA2 pipeline (Callahan et al., 2016). Amplicon sequence variants (ASVs) were classified into taxa against the SILVA taxonomy database (version 138). Output data from QIIME2 were visualized using the MicobiomeAnalyst program (Dhariwal et al., 2017).

    5. Statistical analysis

    The paired t-test was used to analyze the changes in colostrum composition, including SCC, pH, and IgG levels, between fresh and heat-treated colostrum. Statistical analysis was performed using IBM SPSS Statistics for Windows, version 26 (IBM Corp., Armonk, NY, USA). To analyze the microbiome, the difference in abundance of taxa between fresh and heat-treated colostrum was identified using linear discriminant analysis (LDA) effect size (LEfSe) (LDA score>2) (Segata et al., 2011). The significance level and tendency were set at 5% (p<0.05) and 10% (0.05<p<0.1), respectively.

    Ⅲ. RESULTS AND DISCUSSION

    1. IgG concentrations in colostrum

    The concentration of IgG in individual cows ranged from 29.40 g/L to 112.12 g/L (data not shown) and did not differ between the fresh and heat-treated colostrum (Table 1). A few studies from Korea conducted over a decade have reported the immunoglobulin concentration (mainly IgG) in bovine colostrum with respect to processing methods (Lee et al., 2001;Jeong et al., 2009), breed comparison (Eom et al., 2024), and immune quality (Kim et al., 2013). However, to the best of our knowledge, the current study is the first to compare fresh and heat-treated colostrum by considering various aspects, including immunity and nutritive values, to examine the quality of colostrum supplied to Hanwoo calves. In previous studies, the IgG concentration reported varied substantially from 16.2 g/L (Lee et al., 2001) to 147.93 g/L (Eom et al., 2024). This might have occurred because Lee et al. (2001) determined IgG levels in the colostrum of a mixed sample 5 days after birth, whereas Eom et al. (2024) used colostrum obtained immediately after the birth of a calf from Holstein cows. Hence, a collection protocol is necessary to accurately compare IgG concentration and understand its significance. This is more important when the colostrum is intended to be used for inducing passive immunity in Hanwoo calves.

    Nevertheless, a significant variation in terms of IgG concentration in the fresh colostrum is not fully understood because the experts in the local colostrum bank had manually mixed the collected colostrum based on their measurements of IgG levels so that the colostrum from the bank could provide consistent levels of IgG for Hanwoo calves after the heat treatment. We assumed that the initial levels of the IgG and the volume of the colostrum from cows could be important factors for this variation. Yet, further research is imperative to minimize the variation in the IgG level of the colostrum.

    Regardless of the collection method, some studies have suggested that successful passive transfer in dairy calves occurs when calves are fed a high concentration of IgG (>50 g/L), wherein the level was determined by radial immunodiffusion or the IgG in calf serum reached 10 g/L (Godden, 2008;Elizondo-Salazar et al., 2010;Gelsinger et al., 2014). However, achieving this IgG concentration for a local colostrum bank is challenging because IgG concentration is likely to decrease during colostrum processing owing to factors such as thawing, heating temperature, and heating time (McMartin et al., 2006;Jeong et al., 2009;Elizondo-Salazar et al., 2010). A study by a domestic research group reported that the IgG content of bovine colostrum declined by 38.3% after heat treatment at 65°C for 30 min (Jeong et al., 2009). Heat treatment at a higher temperature further damages IgG, diminishing its concentration, and presumably, heating even at temperatures ≥65°C can denature immunoproteins in colostrum (Lee et al., 2001).

    We found that although IgG concentrations varied in individual colostrum samples, heating at 60°C for 30 min did not decrease the IgG concentration. This result conforms to the findings of previous studies (Godden et al., 2006;McMartin et al., 2006), which demonstrated no difference in IgG concentration between raw colostrum and colostrum heated at 60°C in a Rapid Visco Analyzer for 120 min. Considering that IgG concentration did not change significantly, heating fresh colostrum at the right temperature (e.g., 60°C) can not only prevent infection by potentially pathogenic microorganisms from other breeds or nearby farms but also induce immunity in Hanwoo calves when fed appropriately.

    2. Nutritive value of colostrum

    Colostrum composition (fat, protein, lactose) and pH values did not differ between fresh and heat-treated colostrum. In contrast, the SCC was lower (p<0.05) in heat-treated colostrum than that in fresh colostrum (Table 2). Bovine colostrum is defined as the first milk produced after birth (Playford and Weiser, 2021) or as the first mammary gland secretions after parturition (McGee and Earley, 2019). Colostrum is collected from dairy cows for diverse reasons, such as for human use (Arslan et al., 2021) and to provide dairy and beef calves (McGee and Earley, 2019). Hence, colostrum produced over a few days after calving is often collected for further treatment. Therefore, in different studies, the nutritive values of the colostrum tend to vary, and finding appropriate results to compare with ours was difficult. Moreover, research regarding heat-treated colostrum is rare because most studies focused on IgG concentration and/or pathogen loads. Jeong et al. (2009) analyzed pooled colostrum collected between the first and fourth days from Holstein cows. The fat, protein, and lactose contents of the pooled colostrum were 4.34%, 6.99%, and 3.37%, respectively. However, Eom et al. (2024) reported values of 5.85%, 16.24%, and 2.68% for fat, protein, and lactose contents, respectively in Holstein. Thus, two studies conducted in Korea demonstrated very different results. A review by Playford and Weiser (2021) showed that the fat, protein, and lactose content in bovine colostrum ranged from 6% to 7%, 14% to 16%, and 2% to 3%, respectively; however, our results slightly differed from these values. The reasons for this (e.g., time to colostrum harvest, seasonality, parity, dry period length) have been documented by Westhoff et al. (2024). Nevertheless, we did not observe differences in nutritive values between the fresh and heat-treated colostrum, thus proving the potential for providing heat-treated colostrum to Hanwoo calves. However, as expected, heat treatment substantially decreased the SCC (p<0.01).

    3. Microbiome of colostrum

    The changes in the microbial population of the fresh and heat-treated colostrum are presented in Fig. 1 and 2, and the results of LEfSe are presented in Tables 3 and 4. Ten significant phyla and eight genera of microorganisms were observed. Of the 10 phyla, Proteobacteria (44.16%) was the most abundant, followed by Bacteroidota (33.26%), Firmicutes (10.04%), Actinobacteriota (7.14%), and Planctomycetota (1.19%) in the fresh colostrum. Marginal differences in the order of abundance were observed in the heat-treated colostrum (Proteobacteria [39.78%], Bacteroidota [39.64%], Actinobacteriota [9.39%], Firmicutes [6.69%], and Acidobacteriota [1.00%]; Table 3). Our results conform to those of Eom et al. (2024), who reported a similar microbial community in the colostrum obtained from Holstein and Jersey cows, with some differences. They found that Proteobacteria was the most dominant (40.28%) taxon, followed by Firmicutes (32.4%), Bacteroidetes (11.23%), Actinobacteria (10.19%), and Deniococcus-Thermus (3.02%). Likewise, Proteobacteria was the most abundant phylum observed in the study by Van Hese et al. (2022), who reported that in the microbiome of the colostrum from Holstein Friesian and Belgian Blue cows, Firmicutes, Bacteroidetes, and Actinobacteria were the dominant phyla, although the proportions were different.

    Unexpectedly, heat treatment did not affect the microbiome of the colostrum at the phylum level. We speculated that the microbiome of fresh and heat-treated colostrum would differ significantly because heating at 60°C reduced the SCC (Table 2). However, limited differences in the microbiome were observed, which, in our speculation, may be attributed to the preservation of DNA in the heat-treated colostrum. Although certain bacteria in the fresh colostrum lost viability after heating for 30 min at 60°C, reasonably intact cells or cells with minimally damaged DNA might have remained in the heat-treated colostrum. This DNA was amplified during the sequencing procedure; consequently, the microbial populations in fresh and heat-treated colostrum appeared similar.

    Nevertheless, some differences in the microbiome of lesser dominant genera were observed at the genus level when the results were compared using LEfSe (Table 4; please note that only significantly different genera were presented). In the heat-treated colostrum, Sphingomonas, Delftia, Ochrobactrum, Simplicispira, and Lactobacillus were more abundant (p<0.05), while the abundance of Acinetobacter was four times more (p<0.05) in the fresh colostrum than that in the heat-treated colostrum (Fig. 2 and Table 4). In the report of Van Hese et al. (2022), the abundance of Acinetobacter was 16.2% in the colostrum of Holstein Friesian and Belgian Blue cows, while this value was found to be 3.49% in a study by Silva et al. (2022), which suggests that the relative abundance of this genus varies depending on the experimental conditions. Eom et al. (2024) demonstrated that the relative abundance of Acinetobacter declined with the time of colostrum collection, ranging from the moment after calving to 12 and 24 h after calving (8.80%, 6.13% and 3.54% in colostrum collected 0, 12 and 24 h post-calving, respectively). Pang et al. (2018) demonstrated the prevalence of Acinetobacter in the microbiota of milk from cows with subclinical mastitis. This genus was found in various mammary tissues, leading to contamination in milk tanks (Gurung et al., 2013). Furthermore, it is known to have antibiotic resistance (Bergogne-Berezin and Towner, 1996), although it is unclear whether this genus is more prone to heat treatment.

    Ⅳ. CONCLUSIONS

    The present study examined the nutritional values, IgG content, and microbial community of colostrum from Holstein cows before and after heat treatment. The IgG concentration in the heat-treated colostrum was not different from that of the fresh colostrum. The fat, protein, and lactose contents were similar in fresh and heat-treated colostrum. However, SCC was reduced significantly after heat treatment. The significant phyla and genera of the microbial communities in the fresh and heat-treated colostrum were identified by 16S rRNA gene sequencing using the Illumina MiSeq-PE250 platform. However, the differences in bacterial communities between the fresh and heat-treated colostrum were negligible. To date, this study is the first to report the IgG content, chemical composition, and microbiome of heat-treated colostrum from Holstein cows. These results can expand our understanding of the composition of fresh and heat-treated colostrum, thereby providing insights into the processing of colostrum obtained from nearby dairy farms for Hanwoo calves.

    Ⅴ. ACKNOWLEDGMENTS

    This study was supported by the Yecheon Agricultural Technology Center.

    Figure

    KGFS-44-4-270_F1.gif

    Relative abundance of bacteria in fresh and heat-treated colostrum from Holstein cows at the phylum level. (odd numbers on the X-axis represent fresh colostrum and even numbers, heat-treated colostrum)

    KGFS-44-4-270_F2.gif

    Relative abundance of bacteria in fresh and heat-treated colostrum from Holstein cows at the genus level. (odd numbers on the X-axis represent fresh colostrum and even numbers, heat-treated colostrum)

    Table

    Immunoglobulin G concentration in fresh and heat-treated colostrum from Holstein cows

    SEM: standard error of the mean.

    Chemical composition and pH of fresh and heat-treated colostrum from Holstein cows

    SCC: somatic cell count.
    SEM: standard error of the mean.

    Linear discriminant analysis effect size of fresh and heat-treated colostrum from Holstein cows at the phylum level

    LDA: linear discriminant analysis.

    Linear discriminant analysis effect size of fresh and heat-treated colostrum from Holstein cows at the genus level1

    LDA: linear discriminant analysis.
    1 Only a few significantly different taxa (p<0.05) are presented.

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