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Article

Sialyloligosaccharides Content in Mature Milk of Different Cow Breeds

by
Carmela Lovallo
1,*,
Cinzia Marchitelli
2,
Francesco Napolitano
2,
Salvatore Claps
1 and
Alessandra Crisà
2
1
Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria (CREA) (Council for Agricultural Research and Economics), Centro di Ricerca Zootecnia e Acquacoltura (Research Centre for Animal Production and Aquaculture), 85051 Potenza, Italy
2
Consiglio per la Ricerca in Agricoltura e l’Analisi dell’Economia Agraria (CREA) (Council for Agricultural Research and Economics), Centro di Ricerca Zootecnia e Acquacoltura (Research Centre for Animal Production and Aquaculture), 00016 Rome, Italy
*
Author to whom correspondence should be addressed.
Sustainability 2022, 14(5), 2805; https://doi.org/10.3390/su14052805
Submission received: 17 January 2022 / Revised: 22 February 2022 / Accepted: 23 February 2022 / Published: 28 February 2022
(This article belongs to the Special Issue Biodiversity 2021: Agriculture, Environment and Wellbeing)
Browse Figure
Versions Notes

Abstract

:
Sialyloligosaccharides (SOS) are bioactive molecules that play an important role in brain development and the increase in immunity in infants. In adults, they act as prebiotics, enhancing protection against microbial pathogens. In the present work, we aimed to analyze the levels of SOS in mature milk, at days 60 and 120 after calving in four cow breeds: Holstein (HO), Simmental × Holstein (SM × HO), Simmental (SM), all fed with total mixed ration (TMR) in intensive production, and Podolica (POD) raised on pasture in an extensive system. The concentrations of SOS (3′-sialyllactose = 3′-SL, 6′-sialyllactose = 6′-SL, 6′-Sialyl-N-acetyllactosamine = 6′-SLN, disialyllactose = DSL, expressed in mg/L) were determined using HPAEC-PAD, a high-performance anion-exchange chromatography with pulsed amperometric detection. Results showed both breed and lactation effects. The contents of 3′-SL, 6′-SL, 6′-SLN, and DSL were higher at 60 than 120 days (p < 0.001), as well as in POD, as compared to the other breeds (p < 0.001). Furthermore, SM showed a significantly greater level of 3′-SL than HO (p < 0.001), as well as a significantly higher level of 6′-SLN in SM than HO (p < 0.001) and SM × HO (p < 0.001). Our findings may have implications for several areas of sustainability that might be used in the cattle management system.

1. Introduction

Milk oligosaccharides (OS) represent a class of bioactive molecules with potential beneficial effects on human health [1,2,3,4,5] OS are formed from three to ten monosaccharide units from monomers, including glucose (Glc), galactose (Gal), and N-acetylglucosamine (GlcNAc), fucose (Fuc), and sialic acids (NeuAc) [6]. The central unit present at the reducing end of milk oligosaccharides is lactose (Gal (b1–4) Glc) or N-acetyl-lactosamine (Gal (b1–4) GlcNAc) [7]. After lactose and lipid, OS represent the third-largest solid component of milk, and human mature milk (HMO) and colostrum contain 12–13 g/L and 22–24 g/L of milk oligosaccharides, respectively [7]. Bovine milk contains a lower concentration of oligosaccharides with a smaller number of structures [7,8,9,10,11], and the OS content in bovine colostrum immediately after calving is around 1 g/L and rapidly decreases after a few hours [12,13]. In breast milk and colostrum, mass spectrometry detected nearly 130 OS, and of these, 93 structures were determined [14]. In bovine milk, however, about 40 OS have been identified [15,16], and the structures of 15 acid OS and 13 neutral OS have been elucidated [14]. The dominant bovine milk oligosaccharides (BMO) are sialylated (3′-SL, 6′-SL, DSL, 6′-SLN) with a lactose core structure, while in HMO mainly contains fucosylated OS, with a lacto-N-tetraose core structure [17].
In the mammary gland, enzymes involved in the synthesis of glycoconjugates of intestinal cells also contribute to OS production. For this reason, OS can act as bait and inhibit the adhesion of pathogens to the intestinal epithelial surfaces of the host [18,19,20,21]. Furthermore, OS have biological activities such as prebiotics (promoting the growth of beneficial microbiota) [22,23], protection against microbial pathogens [8,24,25], anti-infective agents [26], and immune modulators [27]. Sialic acid, a component of BMO, plays an important role in brain development, cognitive function, and the improvement of immunity in infants [24,28,29]. Considering the prebiotic action on the bacterial flora with the improvement of the immune defenses and the intestinal microbiota [30], OS become important, certainly in the diet of children but also in adult nutrition.
Furthermore, whey, a by-product of cheese production, contains a high amount of OS [31,32,33]. Barile et al. [34] identified 7 of 15 OS in whey permeate from Gorgonzola cheese with the same composition as HMO. Starting from whey, Weinborn et al. [35] synthesized nine oligosaccharides, modifying them with the addition of fucose or and/or sialic acid, which had identical composition to the known HMO. Whey permeate is an environmental pollutant and a waste that is difficult to dispose of; therefore, exploiting it to isolate OS become important both in terms of sustainability and environmental protection Weinborn et al. [35] and as the development of strategies to recover OS from the dairy industry and use them as functional ingredients in infant and adult foods [36].
The literature contains information on the concentration of oligosaccharides during bovine lactation; this is often limited to the first phase of lactation or refers to bulk milk or milk principally from Holstein–Friesian and Jersey breeds [12,13,15,16,17,37,38,39,40,41,42]. The first aim of this study was to analyze the milk of four cow breeds reared in intensive farming (Holstein, Simmental × Holstein, Simmental) and an extensive system (Podolica). Furthermore, in this study, the concentration of OS in mature milk at 60 and 120 days of lactation was evaluated.
Considering the enrolled breeds, the Holstein is a highly productive breed, and in quantitative terms, it represents the cosmopolitan breed with the highest milk production [43]. The Simmental breed is a dual-purpose breed selected for the production of milk and meat; it is also a good grazer and adapts to all territories, even in difficult environmental conditions [44,45]. The crossbreeding of Holstein and Simmental breeds aims to use the positive characteristics of each breed [46], and by exploiting heterosis, the likelihood of inbreeding depression is reduced, and heterozygosity increases [47].
The Podolica cattle breed is mainly reared in southern Italy [48]. The breed had a triple aptitude (work, meat, and milk), whereas today, the production concerns meat, milk, and derivatives of high quality and great potential (Caciocavallo cheese). From a comparison between Podolica and Friesian, Podolica milk had a higher protein (3.68% vs. 3.15%) and fat (4.07% vs. 3.31%) content [49]. The Podolica breed is adaptable and able to exploit scarce forage resources to produce a valuable commodity [50]. Podolica cattle are essential for environmental sustainability, fire prevention, land maintenance, and biodiversity conservation.
The experimental design, including two rearing systems, a crossbreed and a traditional local breed was driven by the wide demand for sustainable animal products [51]. The expectation was to provide new insight that could be exploited for the valorization of a local breed and a crossbred cow.

2. Materials and Methods

2.1. Animals, Management Conditions and Milk Collections

The study was carried out in 4 breeds: Holstein (HO), Simmental (SM), Simmental × Holstein (SM × HO), and Podolica (POD).
SM (sire) × HO (dam) crossbreed is the result of rotation crossbreeding. This herd was established as part of the “REDDBOV” project, funded by MIPAAF, DM 19735/7303/12. HO, SM and SM × HO were reared in the CREA (Research Centre for Animal Production and Aquaculture) experimental farm in Monterotondo (Italy). All three breed groups were kept under the same management and feeding conditions (Table 1) with a total mixed ration (TMR). The fourth group was of Podolica cattle reared on a farm in the Basilicata region. The breeding system is based on grazing, with differences in forage essences and chemical composition depending on the spring and summer sampling. The spring pasture showed higher nutrients than the summer pasture, presenting a lower percentage of total fiber (25.8% vs. 29.8%), in particular as regards lignin (7.2% vs. 9.2%).
The enrolled cows were both primiparous and multiparous with average lactation numbers of HO 1.8 ± 0.7, SM × HO 1.9 ± 0.79, SM 2.4 ± 1.7, and POD 4.1 ± 2.1. Individual milk samples from the same 30 cows within each breed, at days 60 and days 120 of lactation, were taken from morning milking. A total of 240 milk samples (50–100 mL each) were stored frozen −20 °C until analysis.

2.2. Analytical Procedures

2.2.1. Chemicals and Standards

Sodium hydroxide solution 50% (NaOH), 3′-Sialyllactose (3′-SL, >97% pure), 6′-Sialyllactose (6′-SL, >97% pure) standards were purchased from Sigma–Aldrich (St. Louis, MO, USA). Disialyllactose (DSL, 90% pure) and 6′-Sialyl-N-acetyllactosamine (6′-SLN >95% pure) were obtained from Carbosynth Ltd. (Compton Berkshire, UK). Zinc sulfate heptahydrate (ZnSO4·7H2O) was from VWR chemicals (Radnor, PA, USA). Sodium acetate anhydrous (NaOAc) and barium hydroxide octahydrate (Ba(OH)2·8H2O) were from Honeywell Fluka (Seelze, Germany).

2.2.2. Oligosaccharides Preparation and Chromatographic Quantification

OS were isolated from individual milk samples as described by McJarrow and van Amelsfort-Schoonbeek [37,52]. Briefly, after centrifugation at 2000× g at 4 °C for 10 min, the supernatant lipid layer was removed, and the proteins were precipitated by the addition of 0.5 volumes of 1.8 g 100 mL−1 Ba(OH)2·8H2O and 0.5 volumes of 2 g 100 mL−1 ZnSO4·7H2O. The blend was mixed by vortex and centrifuged at 12,000× g in a microfuge for 10 min at 4 °C. The supernatant was carefully removed and centrifuged again at the same speed. The second supernatant was filtered with a nylon filter at 0.45 µm pore size. Total OS fraction was separated using high-performance anion-exchange chromatography (HPAEC) on a Dionex CarboPac PA100 column (Thermo Fisher Scientific, Sunnyvale, CA, USA), the operating conditions and programming of eluents are reported previously by Claps et al. [52]. The eluting fractions were monitored by pulsed amperometric detection (Dionex ED50), and the gradient was controlled by a Varian ProStar pump system, able to keep a flow rate of 1 mL/min for the duration of the run. Data were collected and analyzed by Clatity Lite 7.4 Software (Data Apex Ltd., Prague, Czech Republic), and 3′-SL, 6′-SL, 6′-SLN, and DSL external standards were used to obtain standard curves.

2.2.3. Chemical Composition of the Diets

The chemical compositions of the diets (Table 1) were measured by taking a sample of TMR from the mixer wagon, and for grazing, a sample was taken in the spring and another sample in the summer season. Food samples, dried at 60 °C to constant weight and finely chopped, were stored frozen −20 °C until analysis. Proximate composition (dry matter, crude protein, ash, ether extract) was analyzed according to AOAC [53].
Neutral Detergent Fiber (NDF), Acid Detergent Fiber (ADF), and Acid Detergent Lignin (ADL) contents were quantified according to the method described by Van Soest et al. [54].

2.3. Statistical Analysis

The STATISTICA© 12.0 package (StatSoft Inc., Tulsa, OK, USA) was used both for descriptive statistics analyses and GLM procedure, according to the following mixed linear model.
Yijklmnopqr = μ + Bi + Pj + Sk+ Tl + (Bi × Tl) + β(MY)ijklm+ β(FAT)ijkln + β(PROTEIN)ijklo + β(Lactose)ijklp + β(log10SCC)ijklq + β(DIM)ijklr + eijklmnopqr
where: Yiklmnopqr is the observation vector for each trait, μ is total average, Bi is the breed effect (4 levels): HO, SM × HO, SM, POD), Pj is the parity effect (3 levels): (1, 2, ≥3); Sk is the season effect (4 levels): autumn, winter, spring, summer; Tl is the sampling day class effect (2 levels): days 60, days 120 relative to calving, β(MY)ijklm is the covariate for milk yield, β(FAT)ijkln is the covariate for fat%, β(PROTEIN)ijklo is the covariate for protein %, β(Lactose)ijklp is the covariate for lactose content, β(log10SCC)ijklq is the covariate for somatic cell count, β(DIM)ijklr is the covariate for the effective day in milking and eijklmnopq is the casual error.
A post hoc correction was made with the Tukey test, and a p value <0.001 was considered significant.

3. Results

The concentrations of 3′-SL, 6′-SL, 6′-SLN, DSL in our milk samples (240) showed an average value of 77.9 mg/L, 21.3 mg/L, 7.2 mg/L, and 1.8 mg/L, respectively. All SOS were statistically highly correlated between them (0.40 ≤ x ≤ 0.82) (p < 0.001).
A significant effect of breed and sampling time on SOS content was observed, and this was more evident in the Podolica breed. For all the phenotypes, SOS content at day 60 was significantly higher (p < 0.001) than on day 120 (Table 2).
Considering the breed effect on SOS concentration (Table 3), POD animals showed the highest value of each SOS (p < 0.001). Furthermore, SM showed a significantly higher level of 3′-SL content than HO (p < 0.001); 6′-SLN content was significantly higher in SM than HO (p < 0.001) and SM × HO (p < 0.001).
Analyzing the interaction effect of breed and sampling time on SOS concentration (Table 4 and Table 5), 3′-SL content at both day 60 and day 120 was significantly the highest (p < 0.001) in the POD breed. Furthermore, SM showed a significantly higher level of 3′-SL at days 60 than HO (p < 0.001). 6′-SL, 6′-SLN, and DSL content, both at day 60 and day 120, was significantly higher (p < 0.001) in POD than all other breeds. Moreover, 6′-SLN content, both at days 60 and days 120, was significantly higher in SM compared to HO (p < 0.001) and SM × HO (p < 0.001).
Our results underlined a significant effect of parity and season on the content of the SOS. As regards the parity effect (Figure 1), the multiparous cows (parity ≥ 3) showed higher significant values of 3′-SL (p < 0.0001), 6′-SL (p < 0.01), 6′-SLN (p < 0.0001), and DSL (p < 0.01) than the 1th parity cows; moreover 3′-SL (p < 0.0001), 6′-SL (p < 0,0001), 6′-SLN (p < 0.0001) content was higher than 2th parity cows. Considering the season effect for all SOS, significantly higher values (p < 0.001) were observed in spring than in the other seasons (data not shown).

4. Discussion

In this work, we evaluated milk SOS at two lactation stages not previously investigated, near the lactation peak (day 60) and in the middle of lactation (day 120). In addition, a crossbred and a native breed were included in the study. Beyond the research interest, the study aimed to produce new insights that could be applied in the field, given the industry’s demand for a fresh or transformed product (cheese) to be consumed by humans.
The most abundant SOS observed in our investigation, as well as in many other literature reports, was 3′-SL; in these articles, colostrum and the first lactation days were evaluated in particular [12,13,15,16,17,37,38,39,40,41,42]. The concentrations of 3′-SL and 6′-SL detected in HO milk samples (Table 3) are similar to those found in the Goto et al. [55] study, which found SOS values of 83.10 mg/L and 22.22 mg/L in Holstein milk at days 70 and 120 post-calving, respectively. In agreement with McJarrow and van Amelsfort-Schoonbeek [37] and partially with Martin-Sosa et al. [38], the 3′-SL value was followed by 6′-SL, 6′SLN, and DSL. Moreover, in our study, a decreasing trend in SOS concentration from days 60 to days 120 was observed. The mean concentrations of 3′-SL (112 µM) and 6′-SL (34.7 µM) in HO at day 60 can be compared to the Kelly et al. [56] experiment, which collected milk samples during peak lactation in a large Holstein herd. 3′-SL and 6′-SL were measured in milk samples from Jersey and Holstein–Jersey crossbred animals in the same study, and higher values were found in the Jersey breed than in the Holstein breed. Furthermore, the Holstein–Jersey crossbreed’s mean 3′-SL and 6′-SL concentrations were intermediate between Holstein and Jersey. Our research revealed a similar phenomenon, with SM × HO crossbreeds showing intermediate value in comparison to pure breeds not just for 3′-SL and 6′-SL, but also for 6′-SLN and DSL. Individual milk samples from Holstein and Jersey breeds were collected in late lactation (between days 132–232) by Sundekilde et al. [57], and results showed that 3′SL was more abundant than 6′SL and that the 3′-SL isomer was more abundant in Jersey milk than in Holstein milk. Our result showed a high correlation between SOS content overall in the experiment, compared to what was reported in Liu et al. [58], in which OS content was analyzed in 19 Holstein cows around peak lactation. The authors found a correlation only of 3′SL with DSL. The high correlations found by us can be explained considering that the correlated pairs are structurally related and linked by a precursor-product relationship (for example, 3′-SL-/DSL, whereas DSL has one more unit of sialic acid compared with 3′-SL).
It is still unclear if dietary factors influence OS content [59,60,61] or whether grazing management can raise sialoglycoconjugate concentrations in milk [59]. The Podolica cattle breed, which is the only breed in this study that was fed on pasture, had a greater SOS level than the other breeds, which could be attributable to a dietary effect. However, diet is not the only factor that influences OS abundance, and a breed effect could be suspected. In the CREA herd, with animals under the same management system, SM, a dual-purpose breed, showed the highest SOS content. OS are more plentiful in beef cattle milk than dairy breeds, according to Sischo et al. [62]. Their findings show that, in contrast to dairy cows, which are selected to increase milk production and optimize milk components for commercial use, the selection procedure for beef to optimize calf survivability may also optimize milk components for calf health [62]. Even non-dairy breeds have a significant proportion of OS, according to Goto et al. [55]. Most of the studies in the literature are related to cosmopolitan and dairy breeds, and this does not allow us to establish whether the abundance of SOS can be influenced by milk yield. However, other native breeds (8 cow breeds from the geographical area: Norway, Sweden, Finland, Denmark, Iceland, and Lithuania) also showed higher levels of oligosaccharides than commercial milk [63], similar results were observed in Podolica cattle breed in our study.
Our findings showed that parity has a significant effect on SOS content, with multiparous cows having a larger OS content than primiparous cows. Robinson et al. [36] and Quin et al. [42] found that first lactation cows had lower 6′-SL values than second and third parity cows, and in Fischer-Tlustos et al. [40], except for DSL, the multiparous cows had a concentration of 6′-SLN, 3′-SL and 6′-SL higher than the primiparous cows. Increased cow mammary gland growth in conjunction with increasing parity may result in the upregulation of glycosylation-related genes. This hypothesis is, however, speculative because little is known about the synthesis of OS in the bovine mammary gland [64,65].

5. Conclusions

Differences in milk SOS abundance between cow breeds found in our study could be due to a range of reasons such as sampling time, management method, hereditary characteristics, and then endocrine and metabolic changes of the mammary gland. It is worth emphasizing that the Podolica not only provides milk rich in nutraceutical elements but represents a type of breeding that prioritizes animal and environmental welfare. Indeed, the production and sale of Caciocavallo Podolico cheese exemplify economic sustainability, while extensive farming in rural areas provides chances for social sustainability.
The use of a crossbred herd results in an intensive system that is more economically and environmentally sustainable. Farmers benefit from crossbreeding since male calves sell for more money and veterinary costs are lower because the animals are more disease resistant. Furthermore, the goal is to reduce antimicrobial soil contamination.
Finally, recent articles have demonstrated the impact of genetic variables on OS with a medium heritability, and these findings can be used to improve cattle breeds in the future to receive naturally nutraceutical milk.

Author Contributions

Conceptualization, C.L., S.C. and A.C.; sampling, C.M., F.N. and A.C.; methodology, C.L., data curation, C.L.; software, C.L. and C.M.; writing—original draft preparation, C.L. and S.C.; writing—review and editing C.L., S.C., C.M., F.N. and A.C.; supervision, S.C. and A.C.; funding acquisition and project administration, A.C. All authors have read and agreed to the published version of the manuscript.

Funding

This research was funded by the Italian Ministry of Agriculture (MIPAAF) in the national research project MIQUALAT (D.M. 16844/7100/2019).

Institutional Review Board Statement

The ethical review and approval were not applied for this study because the milk samples were collected only by the normal routine milking of animals without any interference with animal health and welfare. The dairy herds involved in this study were raised by routine standard farming practices without interfering with their welfare.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Conflicts of Interest

The authors declare no conflict of interest. The funders had no role in the design of the study, in the collection, analyses and interpretation of data, in writing the manuscript and in the decision to publish the results.

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Sustainability 14 02805 g001 550
Figure 1. Boxplot presenting distribution of 3′-SL (a), 6′-SL (b), 6′-SLN (c), DSL (d) concentration of the first, second, and ≥third parity in all breeds. The ends of the whiskers of each boxplot represent the minimum and maximum of the data, the top and bottom of the box are the first and the third quartiles, the bold band is the median, and the cross is the media. ns: not significant; *: p < 0.01, ** p < 0.0001.
Figure 1. Boxplot presenting distribution of 3′-SL (a), 6′-SL (b), 6′-SLN (c), DSL (d) concentration of the first, second, and ≥third parity in all breeds. The ends of the whiskers of each boxplot represent the minimum and maximum of the data, the top and bottom of the box are the first and the third quartiles, the bold band is the median, and the cross is the media. ns: not significant; *: p < 0.01, ** p < 0.0001.
Sustainability 14 02805 g001
Table
Table 1. Composition of diets of HO, SM and SM × HO cows fed with TMR (total mixed ration), and Podolica raised on pasture.
Table 1. Composition of diets of HO, SM and SM × HO cows fed with TMR (total mixed ration), and Podolica raised on pasture.
Chemical Composition TMR *Spring PastureSummer Pasture
Dry matter, DM (%)59.4344.5376.53
Crude Protein (% of DM)18.114.49.5
Crude Fiber (% of DM)19.525.832.8
Ether extract (% of DM)3.62.61.8
Nitrogen free extract (% of DM)52.6450.548.4
Ash (% of DM)6.166.77.5
NDF 1 (% of DM)26.457.861.9
ADF 2 (% of DM)17.130.738.4
ADL 3 (% of DM)2.37.49.2
1 NDF: Neutral Detergent Fibre; 2 ADF: Acid Detergent Fibre; 3 ADL: Acid Detergent Lignin; * TMR, total mixed ration: composed by alfalfa (Medicago sativa italicus L.) hay, polyphyta hay, sorghum silage, barley, corn, triticale, soybean).
Table
Table 2. Effect of sampling days on SOS concentration. Values are expressed in Least Square Means ± SE.
Table 2. Effect of sampling days on SOS concentration. Values are expressed in Least Square Means ± SE.
Days 3′-SL (mg/L)6′-SL (mg/L)6′-SLN (mg/L) DSL (mg/L)
6086.03 A ± 2.8822.47 A ± 0.59.30 A ± 0.552.03 A ± 0.14
12068.47 B ± 3.0319.51 B ± 1.005.01 B ± 0.581.59 B ± 0.14
Values in the same column with different letters are significantly different (A, B: p < 0.001).
Table
Table 3. Breed effect on SOS concentration. Values are expressed in Least Square Means ± SE.
Table 3. Breed effect on SOS concentration. Values are expressed in Least Square Means ± SE.
Breed 3′-SL (mg/L)6′-SL (mg/L)6′-SLN (mg/L) DSL (mg/L)
HO64.33 D ± 1.3220.76 B ± 0.445.22 C ± 0.251.67 B ± 0.06
SM × HO68.66 C ± 1.2020.44 B ± 0.405.31 C ± 0.231.66 B ± 0.06
SM73.43 B ± 1.1621.32 B ± 0.387.19 B ± 0.221.80 B ± 0.05
POD102.58 A ± 2.5021.45 A ± 0.8210.89 A ± 0.482.12 A ± 0.12
Values in the same column with different letters are significantly different (A, B, C, D: p < 0.001).
Table
Table 4. Content of different oligosaccharides (values are expressed as Least Square Means ± SE) in different breeds at day 60 of lactation.
Table 4. Content of different oligosaccharides (values are expressed as Least Square Means ± SE) in different breeds at day 60 of lactation.
Breed 3′-SL (mg/L)6′-SL (mg/L)6′-SLN (mg/L) DSL (mg/L)
HO71.10 C ± 3.3422.38 B ± 1.107.21 C ± 0.641.86 B ± 0.16
SM × HO76.63 BC ± 3.2822.00 B ± 1.087.14 C ± 0.621.85 B ± 0.15
SM82.28 B± 3.3322.78 B ± 1.109.38 B ± 0.632.03 B ± 0.16
POD114.13 A ± 3.7022.73 A ± 1.2213.47 A ± 0.702.39 A ± 0.17
Values in the same column with different letters are significantly different (A, B, C: p < 0.001).
Table
Table 5. Content of different oligosaccharides (values are expressed as Least Square Means ± SE) in different breeds at days 120 of lactation.
Table 5. Content of different oligosaccharides (values are expressed as Least Square Means ± SE) in different breeds at days 120 of lactation.
Breed 3′-SL (mg/L)6′-SL (mg/L)6′-SLN (mg/L) DSL (mg/L)
HO57.56 C ± 3.3619.13 B ± 1.113.23 C ± 0.641.47 B ± 0.16
SM × HO60.70 BC ± 3.4018.88 B ± 1.123.4 C ± 0.651.46 B ± 0.16
SM64.58 B ± 3.101985 B ± 1.025.01 B ± 0.591.57 B ± 0.15
POD91.03 A ± 4.1120.18 A ± 1.368.31 A ± 0.781.84 A ± 0.19
Values in the same column with different letters are significantly different (A, B, C: p < 0.001).
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Lovallo, C.; Marchitelli, C.; Napolitano, F.; Claps, S.; Crisà, A. Sialyloligosaccharides Content in Mature Milk of Different Cow Breeds. Sustainability 2022, 14, 2805. https://doi.org/10.3390/su14052805

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Lovallo C, Marchitelli C, Napolitano F, Claps S, Crisà A. Sialyloligosaccharides Content in Mature Milk of Different Cow Breeds. Sustainability. 2022; 14(5):2805. https://doi.org/10.3390/su14052805

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Lovallo, Carmela, Cinzia Marchitelli, Francesco Napolitano, Salvatore Claps, and Alessandra Crisà. 2022. "Sialyloligosaccharides Content in Mature Milk of Different Cow Breeds" Sustainability 14, no. 5: 2805. https://doi.org/10.3390/su14052805

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