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Article

Milk Yield, Composition, and Fatty Acid Profile in Milk of Dairy Cows Supplemented with Microalgae Schizochytrium sp.: A Meta-Analysis

by
José Felipe Orzuna-Orzuna
1,
Juan Eduardo Godina-Rodríguez
2,
Jonathan Raúl Garay-Martínez
3,
Guillermo Reséndiz-González
4,
Santiago Joaquín-Cancino
5 and
Alejandro Lara-Bueno
1,*
1
Departamento de Zootecnia, Universidad Autónoma Chapingo, Chapingo C.P. 56230, State of Mexico, Mexico
2
Campo Experimental Uruapan, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Av. Latinoamérica 1001, Uruapan C.P. 60150, Michoacán, Mexico
3
Campo Experimental Las Huastecas, Instituto Nacional de Investigaciones Forestales, Agrícolas y Pecuarias, Altamira C.P. 89610, Tamaulipas, Mexico
4
Facultad de Estudios Superiores Cuautitlán, Universidad Nacional Autónoma de México, Cuautitlán C.P. 54740, State of Mexico, Mexico
5
Facultad de Ingeniería y Ciencias, Universidad Autónoma de Tamaulipas, Centro Universitario. Cd., Victoria C.P. 87000, Tamaulipas, Mexico
*
Author to whom correspondence should be addressed.
Agriculture 2024, 14(7), 1119; https://doi.org/10.3390/agriculture14071119
Submission received: 25 June 2024 / Revised: 9 July 2024 / Accepted: 9 July 2024 / Published: 11 July 2024
(This article belongs to the Special Issue Feeding Strategies and Nutritional Quality of Animal Products—Volume II)
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Abstract

:
This study aimed to evaluate the effects of the microalgae (MIAs) Schizochytrium sp. as a dietary supplement for dairy cows with respect to the yield, composition, and fatty acid profile of milk using a meta-analytical method. The data used in the statistical analyses were obtained from 11 peer-reviewed scientific publications. The effect size was assessed using the weighted mean differences (WMDs) between MIA-supplemented and control treatments. Dry matter intake, milk fat yield, and milk fat content decreased (p < 0.001) in response to the dietary inclusion of Schizochytrium sp. MIAs. However, Schizochytrium sp. MIAs supplementation increased (p = 0.029) milk yield. The dietary inclusion of Schizochytrium sp. MIAs decreased (p < 0.05) the content of the fatty acids (FAs) butyric, caproic, caprylic, capric, undecanoic, lauric, pentadecanoic, palmitic, heptadecanoic, stearic, arachidic, and total saturated FAs, and it resulted in a ω-6/ω-3 ratio in milk. In contrast, Schizochytrium sp. MIAs supplementation increased (p < 0.05) the content of linoleic, conjugated linoleic, eicosapentaenoic, behenic, docosahexaenoic, total monounsaturated FAs, total polyunsaturated FAs, and total omega-3 FAs in milk. The results showed that Schizochytrium sp. MIAs could be used as a dietary supplement to improve the milk yield and fatty acid profile of milk obtained from dairy cows.

1. Introduction

In recent years, the demand for high-quality milk has increased due to the growth in the world population and improvement of citizens’ quality of life [1]. According to Pereira [2], cow’s milk is the most consumed milk worldwide and contains several important nutrients for human nutrition and health, such as vitamins, minerals, proteins, fats, and sugars. However, Plata-Pérez et al. [3] and Samková and Kalač [4] mention that cow’s milk has a high content of total saturated fatty acids (SFAs), which have been reported to increase the risk of metabolic and cardiovascular diseases (CVDs) in humans [2]. On the other hand, previous studies [4,5] indicate that cow’s milk fat only has a low proportion of total polyunsaturated fatty acids (PUFAs), which decreases triglycerides and cholesterol in blood [6] have anti-inflammatory and antithrombotic properties [7], and benefit brain development and function in humans [8]. Consequently, in recent years, several studies have focused on the search for nutritional strategies that help improve the nutritional and nutraceutical quality of cow’s milk through an increase in the total PUFA content and a reduction in the proportion of total SFAs [4,9]. Among the currently available strategies, the inclusion of PUFA-rich products (e.g., protected fats and oilseeds) in cows’ diets has been successfully used to increase milk PUFA content [3,4].
Recent studies [1,10] indicate that the inclusion of microalgae (MIAs) in diets for dairy cows can also be used as a nutritional strategy to improve PUFA content and, at the same time, reduce the amount of SFAs in milk. MIAs are photosynthetic microorganisms [11], which contain a wide variety of vitamins, minerals, pigments, proteins (between 39 and 71%), carbohydrates (from 10 to 57%), and between 6 and 86% lipids, mainly long-chain PUFAs [9,11,12]. This variation in the chemical composition of MIAs depends on the cultivation and growth conditions, as well as their physical and chemical processing before being included in diets [11]. In dairy cows, large amounts (>100 g/kg DM) of MIAs have been successfully used as a protein ingredient in the diet [13]. Likewise, other studies have used MIAs to partially replace some ingredients, such as ground corn [14], soybean meal [15], and rapeseed and faba bean meals in the diets of dairy cows [13,16]. However, some recent reviews [17,18,19] have recommended not including high doses (>20 g/kg DM) of MIAs in dairy ruminant diets to avoid negative effects on fiber digestibility, feed intake, and milk fat content.
Particularly in dairy cows, few studies have evaluated the effects of the use of Schizochytrium sp. MIAs as a dietary supplement on milk yield [1,20], milk composition [6,21], and the profile of fatty acids in milk [22,23]. In addition, the results obtained in some of these studies are contradictory, which makes it difficult to draw reliable conclusions. For example, in some studies [10,21], Schizochytrium sp. MIAs have negatively affected milk yield and milk fat content. However, other authors have detected positive [24] or neutral [23] effects on milk yield, milk composition, and fatty acid profile in milk from dairy cows supplemented with Schizochytrium sp. MIAs. According to recent studies [17,19], the breed and lactation stage of the animals, the doses and species of MIAs, the duration of the experimental period, and the amount of forage in the diet are factors that influence the variability of the results observed between studies.
To date, some narrative reviews have been published [9,11,17] that suggest the use of MIAs as a dietary supplement to improve the productive performance and fatty acid profile of ruminant milk. However, none of these reviews focused only on dairy cows or Schizochytrium sp. MIAs, nor did they use a meta-analytic approach. According to Littell et al. [25], a meta-analysis is a set of statistical methods that allows for the quantitative results of multiple studies to be combined and statistically analyzed to obtain objective evidence on a given topic. The hypothesis of the present study states that the use of Schizochytrium sp. MIAs as a dietary supplement for dairy cows will positively impact the milk yield and profile of fatty acids in milk. Consequently, the present study aimed to evaluate, using a meta-analytical approach, the effects of the use of Schizochytrium sp. MIAs as a dietary supplement for dairy cows on the milk yield, milk composition, and milk fatty acid profile.

2. Materials and Methods

2.1. Literature Search

The research question was formulated using the PICO strategy proposed by Nishikawa-Pacher [26], in which P is the population, I is the intervention, C is the comparison, and O is the outcome. Therefore, in the current study, the population was dairy cows, the intervention was the dietary supplementation with Schizochytrium sp. MIAs, the comparison was between diets with and without the addition of Schizochytrium sp. MIAs, and the outcomes were the means of treatments obtained in the milk yield, milk composition, and milk fatty acid profile. Subsequently, the scientific documents that evaluated the effects of dietary supplementation with Schizochytrium sp. MIAs in dairy cows were identified, selected, chosen, and included in the database by following the guidelines of the PRISMA protocol [27], as shown in Figure 1. The identification of the literature was carried out through systematic searches using the search engines PubMed, ScienceDirect, Scopus, and Web of Science. The keywords used in all databases were: microalgae, dairy cows, dairy cattle, milk yield, milk composition, milk fatty acid profile, Schizochitrium sp., and Aurantiochytrium sp. Aurantiochytrium sp. MIAs were included in the keywords of the searches carried out because Schizochytrium sp. and Aurantiochytrium sp. are synonyms [28]. To obtain updated information, literature searches were restricted to studies published in the recent decade (January 2014 to May 2024).

2.2. Inclusion and Exclusion Criteria

Through the searches, 371 scientific documents were identified which, after eliminating duplicate documents, were reduced to 304. After this, documents that had any of the following traits were eliminated: (1) conference proceedings, books, theses, review articles, and simulations; (2) studies that did not use dairy cows or used experimentally infected, or cannulated dairy cows; and (3) studies that did not use MIAs Schizochytrium sp. or combined Schizochytrium sp. with another genus of microalgae. The remaining documents were evaluated, and only those that met all of the following inclusion criteria were used to form the meta-analysis database [19,29]: (1) full-text scientific articles published in English in peer-reviewed journals; (2) studies using dairy cows as experimental animals and randomized controlled study design; (3) studies that measured and reported data on milk yield, milk composition, or milk fatty acid profile; (4) studies that evaluated the impact of dietary supplementation with Schizochytrium sp. MIAs compared with the control using the same basal diet in all treatments; (5) studies that reported the amount (g/kg DM) of Schizochytrium sp. MIAs included in the diet or provided the information necessary to estimate it; and (6) studies that included data on the treatment means, number of experimental units (n), and standard error of means (SEM) from the control (diets without Schizochytrium sp. MIAs supplementation) and experimental (diets supplemented with Schizochytrium sp. MIAs) treatments.

2.3. Data Extraction

Table 1 shows the 11 scientific articles used to build the meta-analysis database. The following characteristics of each selected scientific article were extracted into an Excel spreadsheet: (1) name of the author; (2) year of publication; (3) breed of dairy cows; (4) doses (g/kg DM) of Schizochytrium sp. MIAs included in the experimental diets; (5) duration of the period of dietary supplementation with Schizochytrium sp. MIAs; (6) days in milk from dairy cows; and (7) amount of forage (g/kg DM) included in the diet. The final database only included response variables reported in at least three scientific articles, as recommended by other authors [25,29]. The final database included the following milk yield and milk composition variables: dry matter intake (DMI), milk yield (MY), milk fat yield (MFY), milk protein yield (MPY), milk lactose yield (MLY), milk fat content (MFC), milk protein content (MPC), milk lactose content (MLC), and somatic cell count (SCC). In addition, the database included the following milk fatty acids: butyric (C4:0), caproic (C6:0), caprylic (C8:0), capric (C10:0), undecanoic (C11:0), lauric (C12:0), myristic (C14:0), myristoleic (C14:1), pentadecanoic (C15:0), palmitic (C16:0), palmitoleic (C16:1), heptadecanoic (C17:0), margoleic (C17:1), stearic (C18:0), oleic (C18:1 n-9 cis), linoleic (C18:2 n-6 cis), conjugated linoleic (C18:2 cis-9, trans-11), α-linolenic (C18: 3 n-3), γ-linolenic (C18:3 n 6), arachidic (C20:0), eicosapentaenoic (C20:5 n-3), behenic (C22:0), docosahexaenoic (C22:6 n-3), total saturated fatty acids (SFAs), total monounsaturated fatty acids (MUFAs), total polyunsaturated fatty acids (PUFAs), total omega-3 (ω-3), total omega 6 (ω-6), and ω-6/ω-3 ratio. From the 11 scientific articles selected, the means of treatments, SEM, and n for each response variable were extracted.

2.4. Calculations, Statistical Analysis, Heterogeneity, and Publication Bias

The “meta” [33] and “metafor” [34] packages available in R statistical software (version 4.1.2) were used to analyze all data in the current study. The effect size (ES) of Schizochytrium sp. MIAs supplementation in dairy cow diets was assessed by examining the weighted mean differences (WMDs) between the experimental (diets with Schizochytrium sp. MIAs) and control (diets without Schizochytrium sp. MIAs) treatments. According to Takeshima et al. [35], WMDs have greater statistical power and are easier to interpret than other ES measures, which makes their use advisable. The methods and procedures previously proposed by Der-Simonian and Laird [36] for random effects models were used to weigh the treatment means by inverse variance.
Heterogeneity between studies was rigorously assessed using I2 and Cochran’s Q statistics, and significant heterogeneity was declared when Q had p ≤ 0.05 and I2 > 50% [25,37,38]. Furthermore, the statistical tests of Egger [39] and Begg [40] were used to detect the possible presence of publication bias considering a significance threshold of p ≤ 0.05.

2.5. Meta-Regression and Subgroup Analysis

Univariate meta-regression analyses were used to test the effects of Schizochytrium sp. MIAs doses, Schizochytrium sp. MIAs supplementation periods, days in milk from dairy cows, and amount of forage included in the diets in the heterogeneity detected in the response variables. Meta-regression analyses were performed using Der-Simonian and Laird’s [37] method of moments only on response variables that had the following traits: (1) reported in at least ten scientific articles [25]; (2) have p ≤ 0.05 for the Q test and I2 > 50% [38]; and (3) have no publication bias (i.e., p > 0.05 in Egger and Begg tests) [39,40]. The doses of Schizochytrium sp. MIAs added to the diets (≤10 and 11–18 g/kg DM), the supplementation period (experimental period) with Schizochytrium sp. MIAs (≤80 or >80), the days in milk (≤100 or >100), and the level of forage included in the diets (≤500 g/kg DM and >500 g/kg DM) were used as categorical covariates. The breed of dairy cows was not used as a covariate because all studies used Holstein cows (Table 1). The significant covariates (p ≤ 0.05) were evaluated through subgroup analysis, including only subgroups with at least three comparisons, as recommended by other authors [19,29,41].

3. Results

3.1. Milk Yield and Composition

Table 2 shows that DMI, MFY, and MFC decreased (p < 0.001) in response to Schizochytrium sp. MIAs supplementation. In contrast, MY increased in response to Schizochytrium sp. MIAs supplementation (p = 0.029). On the other hand, MPY, MLY, MPC, MLC, and SCC were not affected (p > 0.05) by Schizochytrium sp. MIAs supplementation.

3.2. Milk Fatty Acid Profile

Table 3 shows that the dietary inclusion of Schizochytrium sp. MIAs did not affect (p > 0.05) the content of C14:0, C14:1, C16:1, C17:1, C18:3 n-3, C18:3 n-6, and total ω-6 in milk. However, Schizochytrium sp. MIAs supplementation decreased (p < 0.05) the content of C4:0, C6:0, C8:0, C10:0, C11:0, C12:0, C15:0, C16:0, C17:0, C18:0, C18:1 n-9 cis, C20:0, and total SFAs and the ω-6/ω-3 ratio in milk. In contrast, dietary supplementation with Schizochytrium sp. MIAs increased (p < 0.05) the content of C18:2 n-6 cis, C18:2 cis-9, trans-11, C20:5 n-3, C22:0, C22:6 n-3, total MUFAs, total PUFAs, and total ω-3 in milk (Table 3).

3.3. Publication Bias and Meta-Regression

Table 2 and Table 3 show that Egger’s regression asymmetry test and Begg’s adjusted rank correlation were not significant (p > 0.05) for any of the response variables tested, indicating that publication bias was not detected.
Table 2 shows that there was significant heterogeneity (Q) (p ≤ 0.05) in DMI, MFY, MFC, MPC, MLC, and SCC. Likewise, Table 3 shows that there was significant Q (p ≤ 0.05) in the content of FAs C11:0, C18:0, C18:1n-9 cis, C18:2 cis-9, trans-11, C18:3 n-6, C20:0, C20:5 n-3, C22:0, C22:6 n-3, total SFAs, total MUFAs, total PUFAs, total ω-3, and total ω-6 and the ω-6/ω-3 ratio. In the current study, meta-regression analyses were only performed on DMI, MFC, MPC, MLC, total SFAs, total MUFAs, and total PUFAs. This is justified because the other response variables that had heterogeneity were reported in less than ten studies, and under these conditions, the power of the test is low [25].
Table 4 shows that the covariates’ days in milk and supplementation period did not have a significant relationship (p > 0.05) with any of the response variables evaluated. None of the covariates used had a significant relationship (p < 0.05) with MFC, MPC, total MUFAs, and total PUFAs. The Schizochytrium sp. MIAs dose covariate explained (p < 0.05) 68.72 and 18.32% of the observed heterogeneity for MLC and total SFAs, respectively. The level of forage in the diet explained (p < 0.05) 43.62 and 12.39% of the observed heterogeneity for DMI and MLC, respectively.

3.4. Subgroup Analysis

Figure 2a shows that MLC was decreased (p < 0.05) when low doses (≤10 g/kg DM) of Schizochytrium sp. MIAs were used. However, the inclusion of Schizochytrium sp. MIAs at doses ranging between 11 and 18 g/kg DM did not affect MLC (p > 0.05). On the other hand, the total SFAs content decreased (p < 0.001) regardless of the dose of Schizochytrium sp. MIAs used (Figure 2b).
Figure 3a shows that DMI decreased (p < 0.05) regardless of the level of forage included in the diets. On the other hand, MLC decreased (p < 0.05) in dairy cows consuming diets with a forage level ≤ 500 g/kg DM. However, MLC was not affected when the forage level in the diet of dairy cows was greater than 500 g/kg DM (Figure 3b).

4. Discussion

4.1. Milk Yield and Composition

In the present meta-analysis, supplementation with Schizochytrium sp. MIAs decreased DMI. This effect could be related to the unpleasant taste and smell that MIAs generally have [17]. Likewise, it has been hypothesized that the lower DMI observed in ruminants supplemented with Schizochytrium sp. MIAs may be related to possible toxic effects of the PUFAs contained in MIAs on ruminal microorganisms, which decreases fiber digestibility. This hypothesis is supported by recent studies [42,43], which indicate that the inclusion of Schizochytrium sp. MIAs as a supplement in ruminant diets decreases the relative abundance of fiber-degrading ruminal bacteria (e.g., Fibrobacter succinogenes and Ruminococcus albus). Likewise, the lower DMI observed in dairy cows supplemented with Schizochytrium sp. MIAs could be related to the PUFAs contained in the MIAs [21] as PUFAs stimulate the release of intestinal hormones in dairy cows, such as glucagon-like peptide-1 (GLP-1) and cholecystokinin (CKK), and DMI decreases when plasma levels of CKK and GLP-1 increase [44].
In the present meta-analysis, the dietary inclusion of Schizochytrium sp. MIAs increased MY; however, MFY and MFC decreased in response to Schizochytrium sp. MIAs supplementation. In a previous meta-analysis, Orzuna-Orzuna et al. [19] also detected higher MY and lower MFC in lactating small ruminants supplemented with MIAs as a dietary supplement. The higher MY and lower DMI observed suggest that Schizochytrium sp. MIAs improved feed efficiency (FE) in dairy cows; however, there was no necessary information in the database to assess FE directly. Some previous reviews [11,12,17] report that most Schizochytrium sp. MIAs contain folic acid, vitamin E, B-complex vitamins (B1, B6, and B12), and essential amino acids (e.g., methionine and lysine). The presence of these nutrients in the Schizochytrium sp. MIAs could explain the higher MY observed in the present meta-analysis as recent studies [45,46,47,48] have shown that these nutrients improve nutritional status and energy metabolism and lead to higher MY in dairy cows.
The lower MFC observed in the present meta-analysis could be negative as a positive correlation between MFC and cheese yield has been reported [49]. The exact mechanism of the lower MFC in dairy cows supplemented with Schizochytrium sp. MIAs has yet to be studied [6]. However, the lower MFC observed could be related to the high content of PUFAs in the Schizochytrium sp. MIAs [50], as Hussein et al. [51] suggest that dietary supplementation with products rich in PUFAs may inhibit circulating fatty acid uptake and de novo synthesis by the mammary gland. This hypothesis is supported by the results of Vahmani et al. [52] in dairy cows supplemented with Schizochytrium sp. MIAs. In that study, the authors detected lower hepatic expression of some genes (lipoprotein lipase, fatty acid synthase, stearoyl-CoA desaturase) involved in the uptake, de novo synthesis, and desaturation of fatty acids. In addition, according to Mavrommatis and Tsiplakou [53], MFC has a positive and negative correlation with the contents of C18:0 and C18:2 cis-9, trans-11 in milk, respectively. Therefore, the lower content of C18:0 and the higher proportion of C18:2 cis-9, trans-11 in milk detected in the present study partially explain the reduction in MFC. Likewise, the lower MFY observed could be directly related to the lower MFC because, in dairy cows, there is a positive correlation (r = 0.40) between MFY and MFC [54].

4.2. Milk Fatty Acid Profile

According to Hanuš et al. [55], making specific changes in the fatty acid profile of milk can improve the health of a large part of the human population. For example, it has been reported that a lower content of SFAs (C4:0-C20:0) in milk can decrease the risk of CVDs in humans [2]. In the present meta-analysis, MIAs supplementation decreased the content of most SFAs (C4:0, C6:0, C8:0, C10:0, C11:0, C12:0, C15:0, C16, C17:0, C18:0, and C20:0) in milk, which could benefit the health of consumers. In dairy cows or other lactating ruminants, the percentage transfer of C4:0, C6:0, and C8:0 to the blood has not been evaluated. However, in lactating ruminants, dietary supplementation with Schizochytrium sp. MIAs decreases between 21 and 76% of the blood levels of C10:0, C11:0, C12:0, C14:0, C15:0, C16:0, C17:0, C18:0, and C20:0 [1,23,53,56]. Therefore, similar effects of Schizochytrium sp. MIAs consumption in the present study could reduce the amount of C10:0, C11:0, C12:0, C14:0, C15:0, C16, C17:0, C18:0, and C20:0 reaching the mammary gland and reduce the percentage of these fatty acids in milk.
In dairy cows, vitamin B12 deficiency decreases the transformation of propionic acid to succinyl-CoA [47]. According to Pećina and Ivanković [57], this reduction leads to an accumulation of propionic acid and favors the formation of C15:0 and C17:0 FAs. Schizochytrium sp. MIAs contain vitamin B12, which partially explains the reduction observed in the current study in the contents of FAs C15:0 and C17:0 in milk. On the other hand, dietary supplementation with Schizochytrium sp. MIAs decreases the relative abundance of Butyrivibrio proteoclasticus bacteria in the ruminal fluid of dairy goats [58]. According to Costa et al. [18], B. proteoclasticus has a predominant role in the final step of the ruminal biohydrogenation (RBH) process, which is required for the saturation of 18-carbon unsaturated fatty acids and their conversion into C18:0 [59]. Therefore, a similar effect of consuming Schizochytrium sp. MIAs on the ruminal microbiota of dairy cows could explain the reduction observed in the current study in the concentration of C18:0 in milk. Mavrommatis and Tsiplakou [53] indicate that, in the ruminant mammary gland, C18:0 can be used as a substrate by the enzyme stearoyl-CoA desaturase (Δ9-desaturase) to synthesize C18:1 n-9 cis de novo. Therefore, the reduction of C18:1 n-9 cis in milk observed in the present meta-analysis could be related to the lower concentration of C18:0 observed in response to supplementation with Schizochytrium sp. MIAs.
In the present study, the use of Schizochytrium sp. MIAs as a dietary supplement for dairy cows increased the contents of C18:2 n-6 cis and C18:2 cis-9, trans-11 in milk. Similar results were reported by Orzuna-Orzuna et al. [19] in a meta-analysis of lactating small ruminants supplemented with MIAs. In dairy cows, it has been reported that supplementation with low doses (between 4.5 and 10.6 g/kg DM) of Schizochytrium sp. MIAs increases blood levels of vaccenic (C18:1 trans-11) acid to between 17.4 and 45.4% [1,23]. This effect could increase the amount of C18:1 trans-11 reaching the mammary gland and result in increased amounts of C18:2 cis-9, trans-11 in milk because, in the mammary gland, the enzyme Δ9-desaturase can convert C18:1 trans-11 to C18:2 cis-9, trans-11 [60]. In humans, the consumption of C18:2 n-6 cis decreases serum cholesterol levels, improves glucose metabolism, and is inversely correlated with the incidence of CVDs [61]. Likewise, the consumption of C18:2 cis-9, trans-11 has anti-inflammatory effects and decreases the risk of obesity, diabetes, atherosclerosis, and some types of cancer in humans [62].
The contents of C20:5 n-3, C22:0, and C22:6 n-3 in milk increased in response to the dietary inclusion of Schizochytrium sp. MIAs. A previously published meta-analysis [19] also detected a higher ratio of C20:5 n-3, C22:0, and C22:6 n-3 in milk from small ruminants supplemented with MIAs. It has been confirmed that MIAs contain C20:5 n-3 that are partially protected from the effects of the ruminal biohydrogenation (RBH) process [63]. This effect could increase the flow and duodenal absorption of C20:5 n-3 and subsequently increase the incorporation of this fatty acid in milk. Likewise, it has been reported that C22:6 n-3 can be saturated at C22:0 in the rumen [64]. Schizochytrium sp. MIAs contain a high concentration (up to 38% of total FAs) of C22:6 n-3 [12,28], and the saturation of a part of this C22:6 n-3 could be related to the higher C22:0 content observed in the current study. In addition, recent studies [1,31] have reported that C22:6 n-3 from Schizochytrium sp. MIAs consumed by dairy cows could be transferred to milk with an efficiency of up to 13.2%, which partially explains its increase in milk. Shahidi and Ambigaipalan [8] indicate that the consumption of foods rich in C20:5 n-3 and C22:6 n-3 decreases the risk of CVDs and improves cognitive function in humans. Likewise, a high consumption of C22:0 improves the intestinal absorption of C22:6 n-3 and reduces the incidence of fatty liver [65]. Therefore, including Schizochytrium sp. MIAs in diets for dairy cows could help produce milk that benefits consumers’ health.
In the present study, the dietary inclusion of Schizochytrium sp. MIAs increased the MUFAs, PUFAs, and total ω-3 contents in milk and, at the same time, decreased the total SFAs content and the ω-6/ω-3 ratio. These effects could be directly related to the changes observed in the proportions of individual FAs in the current study. A previous meta-analysis [66] found that MUFA consumption reduces the risk of stroke in humans by 17%. Maki et al. [67] reported that the consumption of PUFAs reduces the incidence of CVD problems and diabetes by 30 and 50%, respectively. Likewise, the consumption of ω-3 reduces mortality in patients with heart problems by up to 20% [7]. In contrast, previous studies [55,68] have indicated that the consumption of foods with a high SFA content and a high ω-6/ω-3 ratio increases the risk of obesity, atherosclerosis, CVDs, and Alzheimer’s in humans. Therefore, the changes detected in MUFAs, PUFAs, total ω-3, SFAs, and ω-6/ω-3 ratio in milk suggest that Schizochytrium sp. MIAs can be used as a dietary additive to produce healthier cow’s milk for humans.

5. Conclusions

The results of the present study suggest that the inclusion of Schizochytrium sp. microalgae in diets for dairy cows decreases dry matter intake, as well as milk fat content and yield. However, Schizochytrium sp. microalgae can be used as a dietary supplement to improve milk yield and fatty acid profile in milk from dairy cows. Furthermore, more studies are needed to evaluate the simultaneous use of Schizochytrium sp. microalgae and some other additives that prevent the reduction of milk fat content.

Author Contributions

Conceptualization, J.F.O.-O.; methodology, J.F.O.-O.; software, J.F.O.-O., J.E.G.-R. and G.R.-G.; validation, J.E.G.-R., J.R.G.-M., A.L.-B., G.R.-G. and S.J.-C.; formal analysis, J.F.O.-O.; investigation, J.E.G.-R., J.R.G.-M. and G.R.-G.; resources, J.E.G.-R., J.R.G.-M., A.L.-B., G.R.-G. and S.J.-C.; data curation, J.E.G.-R., J.R.G.-M. and S.J.-C.; writing—original draft preparation, J.F.O.-O.; writing—review and editing, J.E.G.-R., J.R.G.-M., A.L.-B., G.R.-G. and S.J.-C.; visualization, S.J.-C. and A.L.-B.; supervision, A.L.-B.; project administration, A.L.-B.; funding acquisition, A.L.-B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The datasets used and analyzed during the current study are available from the corresponding author upon reasonable request.

Conflicts of Interest

The authors declare no conflicts of interest.

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Agriculture 14 01119 g001
Figure 1. A PRISMA flow diagram detailing the literature search strategy and study selection for the meta-analysis.
Figure 1. A PRISMA flow diagram detailing the literature search strategy and study selection for the meta-analysis.
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Figure 2. Subgroup analysis (subgroup = doses of microalgae (g/kg DM)) of the effect of including Schizochytrium sp. microalgae in dairy cows’ diets, WMD = weighted mean differences between microalgae treatments and the control.
Figure 2. Subgroup analysis (subgroup = doses of microalgae (g/kg DM)) of the effect of including Schizochytrium sp. microalgae in dairy cows’ diets, WMD = weighted mean differences between microalgae treatments and the control.
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Figure 3. Subgroup analysis (subgroup = forage in diet (g/kg DM)) of the effect of Schizochytrium sp. microalgae supplementation in dairy cows’ diets; WMD = weighted mean differences between microalgae treatments and the control.
Figure 3. Subgroup analysis (subgroup = forage in diet (g/kg DM)) of the effect of Schizochytrium sp. microalgae supplementation in dairy cows’ diets; WMD = weighted mean differences between microalgae treatments and the control.
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Table 1. Description of the studies included in the meta-analysis database.
Table 1. Description of the studies included in the meta-analysis database.
ReferenceBreedDays in MilkSupplementation Period, dDose (g/kg DM)Forage, g/kg DM
Glover et al. [20]HolsteinNR1129.8557
Liu et al. [1]HolsteinNR606.8, 10.6523
Marques et al. [21]Holstein130842, 4, 6480
Moate et al. [30]Holstein163806, 12, 18700, 710, 730
Moran et al. [31]Holstein133844.1710
Moran et al. [22]Holstein164846.6, 6.6707
Till et al. [6]Holstein771122.1, 4.3, 6.4554
Till et al. [23]Holstein25984.5543
Vahmani et al. [24]Holstein01959.451
Vanbergue et al. [10]Holstein100707.3, 1875.5, 76.1
Vanbergue et al. [32]Holstein100707.3, 1875.5, 76.1
NR = not reported.
Table 2. Milk yield and milk composition of dairy cows supplemented with Schizochytrium sp. microalgae.
Table 2. Milk yield and milk composition of dairy cows supplemented with Schizochytrium sp. microalgae.
ItemN (NC) HeterogeneityEgger Test 1Begg Test 2
Control Means (SD)WMD (95% CI)p-Valuep-ValueI2 (%)p-Valuep-Value
DMI, kg/d10 (19)22.845 (1.341)−0.341 (−0.541; −0.141)<0.001<0.00168.640.2090.859
MY, kg/d10 (19)32.06 (5.37)0.458 (0.048; 0.868)0.0290.9670.000.4550.646
MFY, kg/d9 (18)1.251 (0.167)−0.128 (−0.182; −0.075)<0.001<0.00173.090.2820.467
MPY, kg/d9 (18)1.048 (0.173)0.005 (−0.01; 1 0.021)0.5230.9480.000.3410.502
MLY, kg/d7 (15)1.537 (0.266)0.015 (−0.006; 0.036)0.1630.9530.000.0820.130
MFC, g/kg10 (19)35.21 (5.86)−5.095 (−6.730; −3.461)<0.001<0.00172.030.3980.242
MPC, g/kg10 (19)32.68 (1.65)−0.248 (−0.929; 0.432)0.474<0.00191.490.3250.413
MLC, g/kg10 (19)49.12 (1.99)−0.054 (−0.359; 0.251)0.727<0.00168.390.2100.136
SCC, ×103 cell/mL7 (12)1.907 (0.709)0.208 (−0.102; 0.519)0.189<0.00195.460.9480.329
N = number of studies; NC = number of comparisons between Schizochytrium sp. microalgae treatment and control treatment; SD = standard deviation; WMD = weighted mean difference between control and treatments with Schizochytrium sp. microalgae; CI = confidence interval of WMD; p-value of the χ2 (Q) test of heterogeneity; I2 = proportion of total variation of size effect estimates that is due to heterogeneity; 1 = Egger’s regression asymmetry test; 2 = Begg’s adjusted rank correlation; DMI = dry matter intake; MY = milk yield; MFY = milk fat yield; MPY = milk protein yield; MLY = milk lactose yield; MFC = milk fat content; MPC = milk protein content; MLC = milk lactose content; SCC = somatic cell count.
Table 3. Fatty acids (FAs) (% of total FAs) in the milk of dairy cows supplemented with Schizochytrium sp. microalgae.
Table 3. Fatty acids (FAs) (% of total FAs) in the milk of dairy cows supplemented with Schizochytrium sp. microalgae.
ItemN (NC) HeterogeneityEgger Test 1Begg Test 2
Control Means (SD)WMD (95% CI)p-Valuep-ValueI2 (%)p-Valuep-Value
Butyric (C4:0)7 (13)2.703 (1.545)−0.025 (−0.047; −0.002)0.0290.7720.000.1390.217
Caproic (C6:0)7 (14)2.454 (1.518)−0.060 (−0.097; −0.023)0.0020.06343.090.2090.749
Caprylic (C8:0)7 (14)1.224 (0.326)−0.059 (−0.090; −0.029)<0.0010.08636.250.6360.855
Capric (C10:0)8 (15)2.846 (0.522)−0.217 (−0.293; −0.140)<0.0010.06139.950.3670.588
Undecanoic (C11:0)5 (11)0.665 (0.166)−0.183 (−0.228; −0.137)<0.001<0.00199.450.7570.465
Lauric (C12:0)7 (14)3.537 (0.352)−0.229 (−0.316; −0.142)<0.0010.07744.450.2700.966
Myristic (C14:0)8 (15)11.640 (0.910)−0.135 (−0.279; 0.010)0.0680.22221.360.3440.429
Myristoleic (C14:1)8 (15)1.189 (0.471)0.018 (−0.033; 0.069)0.4940.08842.770.4890.478
Pentadecanoic (C15:0)7 (13)1.291 (0.470)−0.038 (−0.056; −0.019)<0.0010.21922.230.1410.189
Palmitic (C16:0)8 (16)34.119 (3.957)−0.728 (−1.276; −0.181)0.0090.06341.310.1440.646
Palmitoleic (C16:1)5 (11)1.979 (0.538)0.031 (−0.084; 0.146)0.6020.07640.910.2300.384
Heptadecanoic (C17:0)8 (16)0.601 (0.185)−0.009 (−0.014; −0.003)0.0020.31212.330.6100.615
Margoleic (C17:1)5 (10)0.439 (0.342)0.002 (−0.003; 0.007)0.5010.12834.950.3130.117
Stearic (C18:0)8 (16)9.083 (2.046)−2.026 (−2.911; −1.142)<0.001<0.00196.050.9740.646
Oleic (C18:1 n-9 cis)7 (13)19.424 (2.830)−0.725 (−1.461; 0.012)0.049<0.00196.900.8300.228
Linoleic (C18:2 n-6 cis)6 (10)2.057 (0.718)0.173 (0.107; 0.238)<0.0010.5010.000.3620.428
Conjugated linoleic (C18:2 cis-9, trans-11)8 (16)0.489 (0.244)0.503 (0.350; 0.657)<0.001<0.00195.920.0990.128
α-linolenic (C18:3 n-3)9 (14)0.432 (0.201)−0.005 (−0.030; 0.020)0.7220.06439.470.1530.086
γ-linolenic (C18:3 n-6)4 (8)0.038 (0.019)0.028 (−0.020; 0.076)0.252<0.00199.550.6920.406
Arachidic (C20:0)7 (15)0.165 (0.042)−0.018 (−0.031; −0.005)0.006<0.00198.180.1740.129
Eicosapentaenoic (C20:5 n-3)9 (16)0.061 (0.032)0.022 (0.010; 0.034)<0.001<0.00198.650.2750.867
Behenic (C22:0)6 (12)0.079 (0.043)0.015 (0.003; 0.026)0.014<0.00192.250.1960.087
Docosahexaenoic (C22:6 n-3)19(16)0.042 (0.031)0.226 (0.187; 0.264)<0.001<0.00195.440.0620.321
Total SFA11 (21)69.345 (4.216)−2.419 (−3.225; −1.613)<0.001<0.00174.670.0820.305
Total MUFA11 (21)24.452 (3.395)0.842 (0.260; 1.424)0.005<0.00165.250.1250.087
Total PUFA11 (21)6.490 (9.110)2.001 (1.412; 2.591)<0.001<0.00198.830.3860.333
Total omega-3 (ω-3)8 (16)0.614 (0.274)0.183 (0.133; 0.233)<0.001<0.00197.470.1730.478
Total omega 6 (ω-6)8 (16)3.123 (1.270)0.253 (0.074; 0.431)0.006<0.00195.780.0680.227
ω-6/ω-3 ratio6 (12)6.35 (4.42)−0.611 (−0.820; −0.402)<0.001<0.00186.360.9930.998
N = number of studies; NC = number of comparisons between Schizochytrium sp. microalgae treatment and control treatment; SD = standard deviation; WMD = weighted mean difference between control and treatments with Schizochytrium sp. microalgae; CI = confidence interval of WMD; p-value of the χ2 (Q) test of heterogeneity; I2 = proportion of total variation of size effect estimates that is due to heterogeneity; 1 = Egger’s regression asymmetry test; 2 = Begg’s adjusted rank correlation; SFA = saturated fatty acid; MUFA = monounsaturated fatty acid; PUFA = polyunsaturated fatty acid.
Table 4. Meta-regression of the effects of dietary Schizochytrium sp. microalgae supplementation on the milk production and quality of dairy cows.
Table 4. Meta-regression of the effects of dietary Schizochytrium sp. microalgae supplementation on the milk production and quality of dairy cows.
Parameter Days in MilkSupplementation PeriodMicroalgae DoseForage Level
Dry matter intake (DMI)QM0.778 0.1500.08512.656
df1111
p-Value0.3780.6990.770<0.001
R2 (%)0.000.000.0043.62
Milk fat content (MFC)QM0.2200.2212.9960.444
df1111
p-Value0.1360.6380.0830.505
R2 (%)0.270.009.220.00
Milk protein content (MPC)QM0.4970.0690.3722.240
df1111
p-Value0.4810.7920.5420.134
R2 (%)4.440.000.003.89
Milk lactose content (MLC)QM1.3820.39724.5333.387
df1111
p-Value0.2400.529<0.0010.046
R2 (%)0.001.0268.7212.39
Total SFAsQM0.0542.3493.4250.880
df1111
p-Value0.8160.1250.0440.127
R2 (%)0.000.0018.320.00
Total MUFAsQM1.6201.3030.2922.546
df1111
p-Value0.2030.2540.5890.111
R2 (%)1.707.960.000.00
Total PUFAsQM0.6840.0793.0201.352
df1111
p-Value0.4080.7790.0820.301
R2 (%)3.973.102.740.00
QM = coefficient of moderators; QM is considered significant at p ≤ 0.05; df: degree of freedom; R2 = the amount of heterogeneity accounted for; SFAs = saturated fatty acids; MUFAs = monounsaturated fatty acids; PUFAs = polyunsaturated fatty acids.
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Orzuna-Orzuna, J.F.; Godina-Rodríguez, J.E.; Garay-Martínez, J.R.; Reséndiz-González, G.; Joaquín-Cancino, S.; Lara-Bueno, A. Milk Yield, Composition, and Fatty Acid Profile in Milk of Dairy Cows Supplemented with Microalgae Schizochytrium sp.: A Meta-Analysis. Agriculture 2024, 14, 1119. https://doi.org/10.3390/agriculture14071119

AMA Style

Orzuna-Orzuna JF, Godina-Rodríguez JE, Garay-Martínez JR, Reséndiz-González G, Joaquín-Cancino S, Lara-Bueno A. Milk Yield, Composition, and Fatty Acid Profile in Milk of Dairy Cows Supplemented with Microalgae Schizochytrium sp.: A Meta-Analysis. Agriculture. 2024; 14(7):1119. https://doi.org/10.3390/agriculture14071119

Chicago/Turabian Style

Orzuna-Orzuna, José Felipe, Juan Eduardo Godina-Rodríguez, Jonathan Raúl Garay-Martínez, Guillermo Reséndiz-González, Santiago Joaquín-Cancino, and Alejandro Lara-Bueno. 2024. "Milk Yield, Composition, and Fatty Acid Profile in Milk of Dairy Cows Supplemented with Microalgae Schizochytrium sp.: A Meta-Analysis" Agriculture 14, no. 7: 1119. https://doi.org/10.3390/agriculture14071119

APA Style

Orzuna-Orzuna, J. F., Godina-Rodríguez, J. E., Garay-Martínez, J. R., Reséndiz-González, G., Joaquín-Cancino, S., & Lara-Bueno, A. (2024). Milk Yield, Composition, and Fatty Acid Profile in Milk of Dairy Cows Supplemented with Microalgae Schizochytrium sp.: A Meta-Analysis. Agriculture, 14(7), 1119. https://doi.org/10.3390/agriculture14071119

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