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Article

Meta-Analysis of Dietary Supplementation with Seaweed in Dairy Cows: Milk Yield and Composition, Nutrient Digestibility, Rumen Fermentation, and Enteric Methane Emissions

by
José Felipe Orzuna-Orzuna
1,
Alejandro Lara-Bueno
1,
Germán David Mendoza-Martínez
2,
Luis Alberto Miranda-Romero
1,
Gabriela Vázquez Silva
3,
María Eugenia de la Torre-Hernández
4,
Nallely Sánchez-López
2 and
Pedro Abel Hernández-García
5,*
1
Departamento de Zootecnia, Universidad Autónoma Chapingo, Chapingo 56230, Mexico
2
Departamento de Producción Agrícola y Animal, Universidad Autónoma Metropolitana Xochimilco, Mexico City 04960, Mexico
3
Departamento El Hombre y su Ambiente, Universidad Autónoma Metropolitana—Xochimilco, Mexico City 04960, Mexico
4
Conahcyt-UAM Xochimilco, Universidad Autónoma Metropolitana Xochimilco, México City 04960, Mexico
5
Centro Universitario Amecameca, Universidad Autónoma del Estado de México, Amecameca 56900, Mexico
*
Author to whom correspondence should be addressed.
Dairy 2024, 5(3), 464-479; https://doi.org/10.3390/dairy5030036
Submission received: 2 July 2024 / Revised: 30 July 2024 / Accepted: 1 August 2024 / Published: 3 August 2024
(This article belongs to the Section Dairy Animal Nutrition and Welfare)
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Abstract

:
This study used a meta-analytic approach to evaluate the effects of dietary supplementation with seaweed on milk yield, milk composition, nutrient digestibility, ruminal fermentation, and enteric methane (CH4) emissions of dairy cows. Data used in statistical analyses were obtained from 23 peer-reviewed scientific articles. Effect size was assessed using weighted mean differences (WMD) between seaweed-supplemented and control treatments. Dietary supplementation with seaweed decreased (p < 0.05) dry matter intake, milk protein content, milk urea nitrogen, and somatic cell count. In contrast, milk fat content, milk lactose content, and milk iodine increased (p < 0.05) in response to dietary supplementation with seaweed. Dietary supplementation with seaweed did not affect (p > 0.05) nutrient digestibility, total volatile fatty acids, acetate, and propionate. Dietary supplementation with seaweeds increased (p < 0.05) ruminal pH and ruminal concentration of butyrate and valerate. In contrast, lower (p < 0.05) ruminal ammonia nitrogen concentration, acetate/propionate ratio, daily CH4 emission, CH4 yield, and CH4 intensity were observed in response to dietary supplementation with seaweeds. In conclusion, dietary supplementation with seaweed modifies milk composition, improves ruminal fermentation, and decreases enteric methane emissions without negatively affecting milk yield or feed efficiency.

1. Introduction

Dairy cow production systems are important, as cow’s milk is the most widely produced and consumed milk globally due to its high content of high-quality protein, bioavailable amino acids, vitamins, and minerals essential for humans [1]. However, enteric methane (CH4) is produced in the rumen of dairy cows due to microbial fermentation of ingested feed [2]. Bačėninaitė et al. [3] indicate that CH4 emitted by dairy cows contributes approximately 35–55% of total greenhouse gas (GHG) emissions from dairy farms worldwide. Consequently, in recent years, the interest of governments and researchers in finding solutions to reduce CH4 emissions has increased dramatically [4]. To date, a large number of dietary additives have been evaluated for mitigating enteric CH4 in dairy cows, such as essential oils, condensed tannins, saponins, flavonoids, ionophores, 3-nitrooxypropanol, and seaweed [3,4,5]. Among these additives, seaweed is one of the most effective in mitigating CH4 emissions in dairy cows without negatively affecting milk yield or feed efficiency [6,7].
Seaweeds (also known as macroalgae) are photosynthetic multicellular eukaryotic organisms that can have different sizes and morphologies [8]. According to some authors [6,9], seaweeds grow on the ocean bottom and are generally classified into three types: red seaweeds (Rhodophyta), brown seaweeds (Ochrophyta), and green seaweeds (Chlorophyta). Although their chemical profile may vary by seaweed type, seaweeds generally contain a wide variety of bioactive compounds, such as polysaccharides, phlorotannins, and halogenated alkanes (mainly bromoform) [6]. According to Glasson et al. [10], halogenated alkanes from seaweed can inhibit CH4 emission in ruminants by blocking the activity of coenzyme M methyltransferase and the enzyme methyl-coenzyme M reductase (MCR), which are required in ruminal CH4 formation [7]. On the other hand, seaweed polysaccharides have antimicrobial, antioxidant, antiviral, and anti-inflammatory properties in livestock [6]. Furthermore, seaweed phlorotannins improve ruminal protein metabolism and have antioxidant, anthelmintic, and anti-methanogenic activity in ruminants [7].
Specifically in dairy cows, a growing number of experiments have evaluated the effects of dietary seaweed supplementation on milk yield [11,12], milk composition [2,13], ruminal fermentation and nutrient digestibility [14,15], and enteric CH4 emissions [16,17]. However, no fully reliable conclusions have been obtained regarding the effect of seaweed treatment on dairy cows because the results reported across studies have been contradictory. For example, some studies reported an increase in milk yield [13], improved milk composition [18], and a decrease in enteric CH4 emissions [14] from dairy cows supplemented with seaweed. In contrast, other authors [2,17,19] show that seaweed negatively affects milk yield and milk composition of dairy cows. Likewise, other studies [11,15] reported that seaweed did not affect milk yield, milk composition, ruminal fermentation, nutrient digestibility, and CH4 methane emissions of dairy cows.
Previously reported results from two meta-analyses [20,21] suggest that seaweeds can mitigate enteric CH4 emissions in ruminants without negatively affecting productive performance. However, these two meta-analyses [20,21] only included a small number of studies (between six and 11) of dairy cows in their database. Furthermore, the meta-analysis by Lean et al. [21] only evaluated five response variables related to dairy cows. Likewise, in the meta-analysis by Sofyan et al. [20], the results for milk yield, milk composition, rumen parameters, and enteric CH4 emissions were obtained by combining data from small ruminants, dairy cows, and beef cattle (in some response variables such as CH4). According to Ioannidis [22], using databases with few studies or combining data from different animal species (e.g., small ruminants, dairy cows, and beef cattle) decreases the likelihood of obtaining robust and scientifically reliable results. On the other hand, Kebreab et al. [23] mention that periodically updating meta-analyses on a specific topic using larger databases can help obtain conclusive findings. In response to the increasing number of scientific articles published in recent years on the use of seaweed as a dietary additive for dairy cows, the current study aimed to evaluate the effects of dietary supplementation with seaweed on milk yield, milk composition, nutrient digestibility, ruminal fermentation, and enteric methane emissions of dairy cows through meta-analytical statistical procedures. The hypothesis of the present meta-analysis states that the inclusion of seaweed in diets for dairy cows will positively impact milk yield, milk composition, nutrient digestibility, and ruminal fermentation and will decrease methane emissions.

2. Materials and Methods

2.1. Literature Search

The research question was formulated using the PICO strategy proposed by Nishikawa-Pacher [24], in which P is the population, I is the intervention, C is the comparison, and O is the outcome. In the current study, the population was dairy cows, the intervention was the inclusion of seaweed in the diet, the comparison was between diets supplemented with seaweed and diets without seaweed, and the outcomes were the means of treatments obtained in milk yield and composition, nutrient digestibility, ruminal fermentation, and enteric CH4 emissions. Subsequently, the scientific documents that evaluated the effects of dietary supplementation with seaweed in dairy cows were identified, selected, chosen, and included in the database following the guidelines of the PRISMA protocol [25], as shown in Figure 1. The identification of literature was carried out through systematic searches using the search engines Scopus, ScienceDirect, PubMed, and Web of Science. The keywords used in the searches were the following: (1) seaweed, (2) macroalgae, (3) dairy cows, (4) dairy cattle, (5) milk yield, (6) milk production, (7) milk composition, (8) milk quality, (9) nutrient digestibility, (10) ruminal fermentation, and (11) methane emission. 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, 240 scientific documents were identified, which, after eliminating duplicate documents, were reduced to 213. 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 as experimental units; and (3) studies that did not use seaweed or combined seaweed with antibiotics, organic acids, or other products. The remaining documents were evaluated and only those that met all of the following inclusion criteria were used to form the meta-analysis database [26,27]: (1) scientific articles written in the English language and peer-reviewed; (2) studies that used dairy cows as experimental units and randomized experiments; (3) studies that compared the effect of dietary supplementation with seaweed against a control treatment (diets without the addition of seaweed) in dairy cows fed with the same basal diet; (4) studies reporting data on parameters related to milk yield and composition, nutrient digestibility, ruminal fermentation, and enteric CH4 emissions; (5) studies that indicated the duration of the seaweed supplementation period and the doses of seaweed added to diets; and (6) studies that included data on standard deviation (SD), standard error (SEM), number of replicates (n), and means of treatments supplemented with seaweed and control (diets without the addition of seaweed).

2.3. Data Extraction

Table 1 shows the 23 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) experimental design (continuous or rotative), (5) days in milk from dairy cows, (6) duration (days) of the period of dietary supplementation with seaweed, (7) dose (g/kg DM) of seaweed added to the diets, (8) seaweed species (i.e., Asparagopsis taxiformis, Ascophyllum nodosum, among others), (9) type of seaweed (red or brown), and (10) level of forage (g/kg DM) included in diets. The variables extracted from the scientific articles were grouped as follows: (1) dry matter intake (DMI), milk yield (MY); energy-corrected milk yield (ECMY); feed efficiency (FE), milk fat yield (MFY), milk protein yield (MPY), milk lactose yield (MLY), milk fat content (MFC), milk protein content (MPC), milk lactose content (MLC), total solids (TC), milk urea nitrogen (MUN), somatic cell count (SCC), iodine and bromoform in milk; (2) dry matter digestibility (DMD), organic matter digestibility (OMD), crude protein digestibility (CPD), neutral detergent fiber digestibility (NDFD), acid detergent fiber digestibility (ADFD), ruminal pH, ammonia nitrogen (NH3-N), total volatile fatty acids (TVFA), acetate, propionate, butyrate, valerate, acetate/propionate ratio, daily CH4 emission (g/d), CH4 yield (g/kg DMI), CH4 intensity (g/kg ECMY). The SEM, number of replicates, and treatment means were obtained for each response variable. The WebPlotDigitizer software version 4.4 was used to extract the data reported in graphs, following the procedures described by Drevon et al. [28].

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

The “meta” [42] and “metafor” [43] packages available in the R statistical software (version 4.1.2) were used to analyze all data in the current study. The effect size (ES) of seaweed supplementation in dairy cow diets was assessed by examining the weighted mean differences (WMD) between the experimental (diets with seaweed) and control (diets without seaweed) treatments. According to Takeshima et al. [44], WMD 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 [45] for random effects models were used to weight 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% [46,47]. Furthermore, publication bias was assessed with Rosenberg’s fail-safe number (NFS) using a significance level of p ≤ 0.05 [48]. Although publication bias was detected in one response variable, the result was considered valid and robust when NFS > [5 (n) + 10], where n is the number of comparisons included in the analysis [49].

2.5. Meta-Regression and Subgroup Analysis

Univariate meta-regression analyses were used to test the effects of experimental design, days in milk, level of forage in the diet, seaweed dose, supplementation period, seaweed type, and seaweed species on the observed heterogeneity in response variables. Meta-regression analyses were performed using Der-Simonian and Laird’s [45] method of moments only on response variables that had the following traits: (1) being reported in at least ten different scientific articles [26,27,46]; (2) have Cochran’s Q statistic with p ≤ 0.05 and I2 statistic > 50% [46,47]; and (3) have p > 0.05 in the Rosenberg’s fail-safe number [48]. The covariates evaluated were divided as follows: (1) experimental design (continuous and rotative); (2) days in milk (≤100 and >100 days); (3) level of forage in the diet (≤600 and >600 g/kg DM); (4) doses of seaweed added to diets 0.23–5.0, 5.1–10.0, and >10.0 g/kg DM; (5) dietary supplementation period with seaweed ≤ 30 and >30 days; (6) type of seaweed (red seaweed and brown seaweed); and (7) species of seaweed (i.e., Asparagopsis taxiformis, Ascophyllum nodosum, among others). The significant covariates (p ≤ 0.05) were evaluated through subgroup analysis, including only subgroups with at least three comparisons, as recommended by other authors [27,50].

3. Results

3.1. Milk Yield and Composition

Table 2 shows that dietary supplementation with seaweeds decreased (p < 0.05) DMI, MPC, MUN, and SCC. In contrast, MFC, MLC, and milk iodine increased (p < 0.05) in response to dietary seaweeds supplementation. On the other hand, MY, ECMY, FE, MFY, MPY, MLY, TS, and bromoform content in milk were not affected (p > 0.05) by dietary supplementation with seaweeds. Table 2 shows that there was significant heterogeneity (Q ≤ 0.05 and I2 > 50%) in DMI, MY, ECMY, and iodine.

3.2. Nutrient Digestibility, Ruminal Fermentation, and Enteric Methane Emissions

Dietary supplementation with seaweeds did not affect (p > 0.05) DMD, OMD, CPD, NDFD, ADFD, TVFA, acetate, and propionate (Table 3). Dietary supplementation with seaweeds increased (p < 0.05) ruminal pH and ruminal concentration of butyrate and valerate. In contrast, lower (p < 0.05) ruminal NH3-N concentration, acetate/propionate ratio, daily CH4 emission, CH4 yield, and CH4 intensity were observed in response to dietary supplementation with seaweeds. Likewise, Table 3 shows that significant heterogeneity (Q ≤ 0.05 and I2 > 50%) was observed in NH3-N, TVFA, acetate, propionate, butyrate, acetate/propionate ratio, daily CH4 emission, CH4 yield, and CH4 intensity. In the current study, meta-regression analyses were only performed on DMI, MY, ECMY, and daily CH4 emissions. This is justified because the other response variables that had significant heterogeneity were reported in fewer than ten studies, and under these conditions, the power of the test is low [46].

3.3. Publication Bias and Meta-Regression

Table 4 shows that the Rosenberg fail-safe number was only significant (p < 0.05) for MFC, MPC, MUN, SCC, iodine, daily CH4 emission, and CH4 yield, which suggests that there was publication bias in these response variables. However, the results obtained can be considered solid because NFS > [5 (n) + 10] was observed in all these variables [49].
Table 5 shows that the covariate of experimental design, days in milk, level of forage in the diet, seaweed dose, and supplementation period did not have a significant relationship (p > 0.05) with any of the response variables evaluated. The seaweed type covariate explained (p < 0.001) 61.18, 66.68, 72.40, and 58.26% of the heterogeneity observed in DMI, MY, ECMY, and daily CH4 emission, respectively. The seaweed species covariate explained (p < 0.001) 75.97, 66.10, 83.08, and 39.68% of the heterogeneity observed in DMI, MY, ECMY, and daily CH4 emission, respectively.

3.4. Subgroup Analysis

Figure 2a shows that DMI decreased (WMD = −1.507 kg/d; p = 0.010) when red seaweeds were used. However, when brown seaweeds were used, DMI was not affected (WMD = 0.059 kg/d; p = 0.501). Figure 2b shows that MY decreased when red seaweed was used (WMD = −1.542 kg/d; p = 0.006). In contrast, when brown seaweeds were used, MY increased (WMD = 0.595 kg/d; p = 0.003). Figure 2c shows that ECMY decreased (WMD = −2.780 kg/d; p < 0.001) when red seaweeds were used. However, when brown seaweeds were used, ECMY was not affected (WMD = 0.489 kg/d; p = 0.125). Daily CH4 emissions decreased (p < 0.01) regardless of the type of seaweed used (Figure 2d). However, the effect was greater when studies used red seaweed (WMD = −104.020 g/d) than when they used brown seaweed (WMD = −13.755 g/d).
Figure 3a shows that DMI was not affected (WMD = 0.198 kg/d; p = 0.561) when the seaweed used was Saccharina latissima. However, DMI decreased (WMD = −1.812 kg/d; p = 0.003) when seaweed Asparagopsis taxiformis was included in the diets. In contrast, DMI increased (WMD = 0.277 kg/d; p = 0.049) when seaweed Ascophyllum nodosum was added to the diets. Figure 3b shows that MY increased (WMD = 1.004 kg/d; p = 0.038) when the seaweed used was Saccharina latissima. However, MY decreased (WMD = −2.215 kg/d; p < 0.001) when seaweed Asparagopsis taxiformis was included in the diets. In contrast, MY increased (WMD = 0.823 kg/d; p < 0.001) when seaweed Ascophyllum nodosum was added to the diets. Figure 3c shows that ECMY was not affected (WMD = 0.054 kg/d; p = 0.958) when the seaweed used was Saccharina latissima. However, ECMY decreased (WMD = −3.402 kg/d; p < 0.001) when seaweed Asparagopsis taxiformis was included in the diets. In contrast, ECMY increased (WMD = 0.734 kg/d; p = 0.050) when seaweed Ascophyllum nodosum was added to the diets. Daily CH4 emissions decreased (p < 0.01) regardless of the seaweed type used (Figure 3d). However, the effect was greater when studies used seaweed Asparagopsis taxiformis (WMD = −105.673 g/d) than when they used seaweed Ascophyllum nodosum (WMD = −24.451 g/d).

4. Discussion

4.1. Milk Yield and Composition

Dietary supplementation with seaweed did not affect DMI, suggesting that seaweed does not negatively affect dietary palatability or nutrient intake in dairy cows. However, subgroup analyses revealed that DMI decreased when red seaweed Asparagopsis taxiformis was used and increased when brown seaweed Ascophyllum nodosum was used. An in vitro study [51] reported that several brown seaweeds (Undaria pinnatifida, Sargassum fusiforme, and A. nodosum) can increase the relative abundance of bacteria Fibrobacter succinogenes (+19.4 to +58.4%), Ruminococcus albus (+7.4 to +11.1%), Ruminococcus flavefaciens (+4.8 to +14.9%), and rumen fungi (+86.8 to +100%) in ruminal fluid of beef cattle fed high forage diets (600 g/kg DM). Similar effects of brown seaweed consumption on dairy cows could explain the higher DMI observed since, according to Comtet-Marre et al. [52], a high abundance of F. succinogenes, R. albus, R. flavefaciens, and rumen fungi can decrease the residence time of feed particles in the rumen and lead to higher DMI. On the other hand, under in vitro conditions [53], A. taxiformis decreases (−41.1 to −64.2%) the relative abundance of the microbial genera Fibrobacter and Ruminococcus in the ruminal fluid of steers fed high forage diets (500 g/kg DM). Similar effects of A. taxiformis on dairy cows could reduce fiber digestibility and passage rate and result in low DMI.
MY, ECMY, FE, MFY, MPY, MLY, and TS were not affected by seaweed supplementation. However, subgroup analyses showed that MY and ECMY decreased when red seaweed A. taxiformis was used and increased when brown seaweed A. nodosum was added to the diets. These differences could be related to the effects of A. taxiformis and A. nodosum on DMI. Likewise, under in vitro conditions, A. taxiformis and other red seaweed decrease the relative abundance of bacteria related to the degradation of fiber, carbohydrates, and proteins [53]. A similar effect of A. taxiformis in dairy cows would decrease nutrient digestibility and rumen production of volatile fatty acids, which could decrease the metabolic availability of nutrients and energy and negatively affect MY. In contrast, several brown seaweeds, including A. nodosum, improve (+12.7 to +22.5%) serum levels of antioxidant enzymes (glutathione peroxidase and catalase) and total antioxidant capacity (TAC) in the blood serum of dairy ruminants [40,54]. These effects of the brown seaweed A. taxiformis partially explain the higher MY detected in the present study since, according to Dong et al. [55], the serum concentration of catalase, superoxide dismutase, and TAC have a positive correlation (r of 0.38 to 0.64) with MY in dairy cows.
Dietary supplementation with seaweed increased MFC and MLC but decreased MPC. Although an increase in MFC is not considered a nutritional benefit in humans, it plays an essential role in milk quality because it directly influences its visual attributes and flavor [56]. For example, high MFC is positively associated with milk creaminess and flavor [57]. On the other hand, an increase in MLC could negatively affect the quality of some dairy products. For example, Portnoy and Barbano [58] indicate that high MLC can induce the excessive formation of lactose and lactate crystals, negatively affecting ice cream’s texture and consumers’ acceptability of cheddar cheese. Likewise, Osorio et al. [56] mention that a low MPC decreases the quality and value of cow’s milk and derived dairy products.
The higher MFC observed in the current study could be related to the effects of seaweed on lipid metabolism. For example, a recent study [18] shows that dietary supplementation with seaweed increases serum triglyceride (TG) concentration by up to 61.5% in dairy cows. Likewise, another study [11] reported that the dietary inclusion of seaweed decreases serum levels of non-esterified fatty acids (NEFA) between 12.0 and 19.5% in dairy cows. According to Andjelić et al. [59], in dairy cows, MFC has a significant positive (r = 0.304) and negative correlation (r = −0.324) with serum levels of TG and NEFA, respectively. On the other hand, recent studies [18,40] reported that seaweed increases (4.2 to 13.4%) the serum glucose concentration in dairy cows. This seaweed effect could explain the increased MLC because lactose synthesis in the mammary gland is carried out mainly from plasma glucose [60]. Furthermore, the lower MPC observed in the current study could be explained by the reduction in DMI of cows supplemented with seaweed. This hypothesis is justified because a low DMI decreases crude protein intake (CPI) and lactation net energy intake (NELI) and, according to Hristov et al. [61], DMI, CPI, and NELI are positively correlated (r of 0.57 to 0.62) with MPC in dairy cows. Likewise, a recent study [40] reported that seaweed supplementation decreases dairy cows’ serum insulin levels by up to 22.5%. A low serum insulin concentration can decrease the absorption of amino acids in the mammary gland [56], which could result in low MPC.
Hossein-Zadeh [62] mentions that MUN is a normal component in ruminant milk, which varies from 20 to 75% of the non-protein nitrogen of milk, and its values can be used as indicators of the efficiency of utilization of protein ingested in dairy cows. In the present study, lower MUN was observed in response to dietary supplementation with seaweed, suggesting that seaweed improves the utilization efficiency of dietary protein. Recent studies [29,40] reported that dietary supplementation with seaweed decreases blood urea nitrogen (BUN) levels in dairy cows by up to 16.4%. This effect of seaweed could explain the lower MUN observed in the current meta-analysis since, according to a recent study [62], BUN has a high positive correlation with MUN in dairy cows. On the other hand, SCC values are a simple and helpful tool to periodically evaluate ruminants’ udder health and milk quality [63]. Although somatic cells are a naturally present component in milk, an increase in SCC values is generally associated with a health problem in the udder and negatively affects MY and milk quality [64]. In the current study, dietary supplementation with seaweed decreased SCC, suggesting that seaweed could reduce SCC in milk from dairy cows. Lopez et al. [33] reported that seaweed supplementation decreases the abundance of Staphylococcus spp. bacteria (including Staphylococcus aureus) in the milk of dairy cows. This effect could explain the lower SCC observed in the current study since, according to Kaskous et al. [64], S. aureus has a positive correlation with SCC in ruminants.
Dietary supplementation with seaweed increased milk iodine content but did not affect milk bromoform content. These effects were expected since, in dairy cows supplemented with seaweed, the transfer efficiency of dietary iodine to milk is high (37.5 to 41.8%) [13,34], while the transfer efficiency of dietary bromoform to milk is low (4.44%) [65]. A high iodine content in milk could be positive for human health since, according to Han et al. [66], more than 2 billion people are at risk of consuming amounts of iodine below their requirements worldwide. According to Newton et al. [13], the high iodine content in milk could affect consumers’ health in human populations without iodine deficiencies. However, the maximum dose of iodine allowed in milk for human consumption is 500 mg/L [6], which is higher than the range iodine content (1.0 to 29.6 mg/L) observed in the milk of dairy cows supplemented with seaweed in the current study. On the other hand, the lack of significant changes in bromoform content in milk suggests that the inclusion of seaweed in diets for dairy cows does not represent any apparent risk of bromoform contamination [10].

4.2. Nutrient Digestibility, Ruminal Fermentation and Enteric Methane Emissions

In the current study, dietary supplementation with seaweed did not affect DMD, OMD, CPD, NDFD, and ADFD. Similarly, Maheswari et al. [54] also did not detect significant changes in DMD, OMD, CPD, NDFD, and ADFD of lactating buffaloes supplemented with high doses (25 g/kg DM for 90 days) of combinations of red and brown seaweeds (Kappaphycus alvarezii, Gracilaria salicornia, Turbinaria conoids). Likewise, dietary supplementation with up to 300 g/kg DM of various seaweeds (Ruppia sp., Ulva sp., or Chaetomorpha sp.) does not affect DMD, OMD, CPD, NDFD, and ADFD in sheep fed high forage diets [67].
Ruminal pH increased, and ruminal NH3-N concentration decreased in response to dietary supplementation with seaweed. These effects could be positive since a low rumen pH is associated with rumen acidosis [68], while a high NH3-N concentration generally indicates a low absorption of ammonia in the rumen, excessive deamination of amino acids or slow utilization of ammonia by ruminal microorganisms [69]. Some authors [70,71] reported that seaweed increases (40.0 to 142.1%) the rumen relative abundance of Selenomonas ruminantium and Megasphera elsdenii bacteria. A higher concentration of these bacteria could increase the ruminal pH because they are lactate-consuming, and the ruminal pH decreases when lactic acid accumulates [68]. On the other hand, Rémond et al. [72] found that a high ruminal concentration of butyrate stimulates ruminal absorption of NH3-N. Therefore, the lower ruminal NH3-N concentration could be partially explained by the increased ruminal butyrate concentration of dairy cows supplemented with seaweed. Likewise, several studies [40,51,70] show that seaweed decreases (−23.1 to −54.0%) the population of rumen protozoa, which have a positive correlation (r = 0.609) with the rumen concentration of NH3-N in ruminants [73].
In the current study, dietary supplementation with seaweed increased the rumen concentration of butyrate and valerate but decreased the acetate/propionate ratio. The higher ruminal concentration of butyrate and valerate could be closely related to the reduction in CH4 emission of dairy cows supplemented with seaweed. This hypothesis is justified because when ruminal methanogenesis decreases, the ruminal concentration of butyrate and valerate increases since it acts as an alternative sink for H2 [74]. According to Min et al. [9], the acetate/propionate ratio changes when the individual rumen concentration of acetate and propionate is modified. These two volatile fatty acids did not change significantly in the present study. However, dietary supplementation with seaweed numerically modified the rumen concentration of acetate (−1.9%) and propionate (+4.7%), which could be related to the observed lower acetate/propionate ratio.
A recent study [3] shows that enteric CH4 emitted by dairy cows accounts for a high proportion (between 35 and 55%) of total GHG emissions from dairy farms worldwide. According to recent reviews [10,75], mitigation of enteric CH4 emissions in dairy cows is essential to improve environmental sustainability in dairy farms. In the present meta-analysis, dietary supplementation with seaweed decreased daily CH4 emission (−7.16%), CH4 yield (−8.74%), and CH4 intensity (−10.81%). The simultaneous reduction of these three types of enteric CH4 shows that seaweed has a consistent anti-methanogenic effect and could improve environmental sustainability in dairy farms. Similar to our results, Roque et al. [76] reported that dietary supplementation with low doses (2.5 and 5.0 g/kg DM for 147 days) of seaweed in beef cattle fed high forage diets (600 g/kg DM) decreased the daily emission of CH4 (−36.28 to −58.64), CH4 yield (−32.58 to 52.03%), and CH4 intensity (−36.93 to −54.46%). Likewise, Li et al. [77] observed lower daily CH4 emission (−14.92 to −81.34%) and CH4 yield (−15.33 to −80.66%) in sheep fed with 40% forage in the diet and supplemented with increasing doses (5.0 to 30.0 g/kg DM for 72 days) of seaweed. Wanapat et al. [75] mention that the anti-methanogenic effects of seaweeds are related to their bromoform and phlorotannin content. Bromoform is a halogenated alkane that competitively binds to coenzyme M methyltransferase, inhibiting methyl transfer in methanogenesis [10]. Likewise, bromoform blocks the enzyme methyl-coenzyme M reductase (MCR) [6], which plays an essential role because it catalyzes the last step in the formation of ruminal CH4 [10]. On the other hand, phlorotannins are compounds analogous to condensed tannins [5], which can inhibit the growth of methanogenic archaea in the rumen [78].
Although daily CH4 emission decreased regardless of seaweed type, subgroup analyses showed that daily CH4 emission decreased almost four times more when red seaweed A. taxiformis was used than when brown seaweed A. nodosum was added to the diets. Hutchings et al. [79] reported that A. taxiformis has a high bromoform content (10–50 g/kg DM), while A. nodosum has a low concentration of phlorotannins (34.9 mg/kg DM) but does not have bromoform [5]. This variation in the concentration of anti-methanogenic compounds in seaweed could explain the differences in their effects on daily CH4 emissions.

5. Conclusions

The overall results indicate that dietary supplementation with seaweed does not affect dry matter intake, milk yield, energy-corrected milk yield, or feed efficiency in dairy cows. However, the use of red seaweed, specifically Asparagopsis taxiformis, decreases dry matter intake, milk yield, and energy-corrected milk yield in dairy cows. Furthermore, brown seaweed Ascophyllum nodosum increases dry matter intake, milk yield, and energy-corrected milk yield in dairy cows. Likewise, dietary supplementation with seaweed increases milk’s fat, lactose, and iodine content while decreasing milk protein content, milk urea nitrogen, and somatic cell count. On the other hand, the inclusion of seaweed in dairy cow diets does not affect nutrient digestibility but improves ruminal fermentation through an increase in pH, butyrate, and valerate and a reduction in ruminal ammonia nitrogen concentration and acetate/propionate ratio. Furthermore, dietary supplementation with seaweed can be used as a nutritional strategy to reduce enteric methane emissions in dairy cows. The best enteric methane mitigation effect is achieved using red seaweed Asparagopsis taxiformis.

Author Contributions

Conceptualization, J.F.O.-O. and P.A.H.-G.; methodology, J.F.O.-O.; software, J.F.O.-O., M.E.d.l.T.-H., A.L.-B. and G.D.M.-M.; validation, A.L.-B., G.D.M.-M., L.A.M.-R., G.V.S. and P.A.H.-G.; formal analysis, J.F.O.-O. and G.D.M.-M.; investigation, J.F.O.-O. and G.V.S.; resources, A.L.-B., G.D.M.-M., G.V.S., M.E.d.l.T.-H., N.S.-L. and P.A.H.-G.; data curation, L.A.M.-R. and G.V.S.; writing—original draft preparation, J.F.O.-O.; writing—review and editing, A.L.-B., G.D.M.-M., L.A.M.-R., G.V.S., M.E.d.l.T.-H., N.S.-L. and P.A.H.-G.; visualization, L.A.M.-R. and G.V.S.; supervision, P.A.H.-G.; project administration, J.F.O.-O. and P.A.H.-G.; funding acquisition, A.L.-B., G.D.M.-M., L.A.M.-R., G.V.S., M.E.d.l.T.-H., N.S.-L. and P.A.H.-G. 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.

Informed Consent 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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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 = seaweed type) of the effect of including seaweed in dairy cows’ diets, WMD = weighted mean differences between seaweed treatments and control.
Figure 2. Subgroup analysis (subgroup = seaweed type) of the effect of including seaweed in dairy cows’ diets, WMD = weighted mean differences between seaweed treatments and control.
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Figure 3. Subgroup analysis (subgroup = seaweed species) of the effect of seaweed supplementation in dairy cows’ diets; WMD = weighted mean differences between seaweed treatments and control.
Figure 3. Subgroup analysis (subgroup = seaweed species) of the effect of seaweed supplementation in dairy cows’ diets; WMD = weighted mean differences between seaweed treatments and 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.
ReferenceBreedEDDIM, dSP, dSW Dose (g/kg DM)SW SpecieSW TypeForage, g/kg DM
Antaya et al. [11]JerseyRotative40213.2, 6.3, 9.7Ascophyllum nodosumBrown642
Antaya et al. [29]JerseyContinuous142285.8, 6.6, 6.8Ascophyllum nodosumBrown700
Bendary et al. [30]HolsteinContinuous71502.9Ascophyllum nodosumBrown600
Bošnjaković et al. [18]HolsteinRotative1742120, 40SL, SM, ANBrown611
Eikanger et al. [2]NorwegianContinuous95391.25, 2.50Asparagopsis taxiformisRed650
Hong et al. [12]HolsteinContinuous3036020, 40Blend-1Brown650
Katwal et al. [31]CrossbreedRotativeNR4580.00Sargassum johnsoniiBrown600
Kidane et al. [32]NorwegianRotative164288.9Ascophyllum nodosumBrown840
Krizsan et al. [14]Nordic RedRotative122215.0Asparagopsis taxiformisRed600
López et al. [33]HolsteinContinuous302384.8Ascophyllum nodosumBrown770
Muizelaar et al. [16]HolsteinRotative91636.6, 6.5, 6.7CHC, SL, Blend-2Red, Brown750
Newton et al. [13]IcelandContinuous168490.9, 3.5Blend-3Brown550
Newton et al. [34]HolsteinContinuous1686313.4Ascophyllum nodosumBrown710
Nyloy et al. [35]NorwegianContinuous95521.25, 2.5Asparagopsis taxiformisRed650
Qin et al. [36]HolsteinRotativeNR282.1SLBrown750
Reyes et al. [37]Holstein and JerseyContinuous1508460CHCRed670
Roque et al. [19]HolsteinRotative201215.0, 10.0Asparagopsis armataRedNR
Rey-Crespo et al. [38]HolsteinContinuous154705.3Blend-4Blend765
Sharma y Datt [39]CrossbreedContinuousNR15015, 30Laminaria digitataBrownNR
Silva et al. [40]JerseyRotative102282.7, 5.4, 8.1Ascophyllum nodosumBrown663
Singh et al. [41]SahiwalContinuous565620Sargassum wightiiBrown750
Stefenoni et al. [17]HolsteinRotative95282.5, 5.0Asparagopsis taxiformisRed603
Thorsteinsson et al. [15]HolsteinContinuous174210.23, 0.46Ascophyllum nodosumBrown534
ED: experimental design; DIM: days in milk; d: days; SP: supplementation period; SW: seaweed; NR: not reported; CHC: Chondrus crispus; SL: Saccharina latissima; SM: Sargassum muticum; AN: Ascophyllum nodosum; Blend-1: unreported species; Blend-2: SL and Fucus serratus; Blend-3: Ascophyllum nodosum and Laminaria digitata; Blend-4: SM, Ulva rígida, and Sacchorhiza polyschides.
Table 2. Milk yield and milk composition in dairy cows supplemented with seaweed.
Table 2. Milk yield and milk composition in dairy cows supplemented with seaweed.
OutcomesN (NC) Heterogeneity
Control Means (SD)WMD (95% CI)p-Valuep-Value 1I2 (%)
DMI, kg/d21 (41)19.85 (4.93)−0.218 (−0.488; 0.052)0.113<0.00167.99
MY, kg/d18 (35)26.17 (7.43)−0.100 (−0.718; 0.519)0.752<0.00178.85
ECMY, kg/d11 (21)25.59 (8.55)−0.525 (−1.823; 0.774)0.428<0.00191.92
FE, DMI/MY9 (17)1.164 (0.351)−0.010 (−0.028; 0.009)0.2960.30912.39
MFY, kg/d8 (18)1.06 (0.33)−0.004 (−0.037; 0.030)0.8290.7690.00
MPY, kg/d8 (18)0.87 (0.31)0.008 (−0.013; 0.029)0.4460.9780.00
MLY, kg/d7 (17)1.17 (0.46)0.016 (−0.018; 0.049)0.3560.9980.00
MFC, g/kg17 (33)4.13 (0.55)0.070 (0.046; 0.095)<0.0010.5060.00
MPC, g/kg17 (33)3.34 (0.30)−0.039 (−0.068; −0.009)0.0100.07140.93
MLC, g/kg15 (32)4.67 (0.15)0.015 (0.001; 0.029)0.0400.5060.00
TS, g/100 g6 (13)12.61 (1.38)0.122 (−0.038; 0.282)0.1350.9890.00
MUN, mg/dL10 (19)12.27 (2.58)−0.478 (−0.755; −0.201)<0.0010.06037.63
SCC, ×103 cell/mL9 (17)4.98 (2.55)−0.275 (−0.424; −0.125)<0.0010.07348.34
Iodine, mg/dL9 (15)0.32 (0.19)0.805 (0.574; 1.036)<0.001<0.00196.87
Bromoform, μL3 (4)0.20 (0.11)0.047 (−0.008; 0.102)0.0960.9170.00
N: number of studies; NC: number of comparisons between seaweed treatment and control treatment; SD: standard deviation; WMD: weighted mean differences between control and treatments with seaweed; CI: confidence interval of WMD; 1 p-Value to Cochran’s Q statistic; I2: proportion of total variation of size effect estimates that is due to heterogeneity; DMI: dry matter intake; MY: milk yield; ECMY: energy-corrected milk yield; FE: feed efficiency; MFY: milk fat yield; MPY: milk protein yield; MLY: milk lactose yield; MFC: milk fat content; MPC: milk protein content; MLC: milk lactose content; TS: total solids; MUN: milk urea nitrogen; SCC: somatic cell count.
Table 3. Nutrient digestibility, ruminal fermentation, and enteric methane emission in dairy cows supplemented with seaweed.
Table 3. Nutrient digestibility, ruminal fermentation, and enteric methane emission in dairy cows supplemented with seaweed.
OutcomesN (NC) Heterogeneity
Control Means (SD)WMD (95% CI)p-Valuep-Value 1I2 (%)
DMD, g/100 g5 (11)69.95 (3.56)−0.241 (−0.639; 0.156)0.2340.7240.00
OMD, g/100 g7 (15)72.63 (2.91)−0.113 (−0.498; 0.272)0.5650.6600.00
CPD, g/100 g7 (15)66.67 (5.37)−0.230 (−1.199; 0.740)0.6420.06543.97
NDFD, g/100 g6 (15)62.42 (5.75)0.308 (−0.366; 0.981)0.3710.32711.27
ADFD, g/100 g3 (9)62.02 (5.93)0.248 (−1.113; 1.609)0.7210.23623.29
Ruminal pH4 (9)6.21 (0.37)0.074 (0.014; 0.134)0.0160.24222.61
NH3-N, mg/dL4 (6)11.88 (4.98)−1.643 (−3.270; −0.016)0.048<0.00183.53
TVFA, Mm6 (12)122.73 (16.94)−4.427 (−11.877; 3.023)0.244<0.00190.85
Acetate, mol/100 mol5 (10)61.69 (5.02)−1.204 (−2.412; 0.003)0.061<0.00168.73
Propionate, mol/100 mol5 (10)21.00 (2.57)0.978 (−0.219; 2.175)0.109<0.00171.80
Butyrate, mol/100 mol5 (10)13.51 (2.22)1.073 (0.385; 1.761)0.002<0.00185.87
Valerate, mol/100 mol5 (10)1.59 (0.41)0.141 (0.025; 0.257)0.0170.06347.05
Acetate/propionate4 (8)3.25 (0.70)−0.321 (−0.550; −0.093)0.006<0.00182.42
CH4 production, g/d10 (22)411.00 (87.40)−29.422 (−41.565; −17.280)<0.001<0.00189.18
CH4 yield, g/kg DMI9 (20)18.06 (3.61)−1.578 (−2.204; −0.951)<0.001<0.00181.01
CH4 intensity, g/kg ECMY9 (19)15.82 (5.26)−1.710 (−2.344; −1.076)<0.001<0.00166.10
N: number of studies; NC: number of comparisons between seaweed treatment and control treatment; SD: standard deviation; WMD: weighted mean differences between control and treatments with seaweed; CI: confidence interval of WMD; 1 p-Value to Cochran’s Q statistic; I2: proportion of total variation of size effect estimates that is due to heterogeneity; DMD: dry matter digestibility; OMD: organic matter digestibility; CPD: crude protein digestibility; NDFD: neutral detergent fiber digestibility; ADFD: acid detergent fiber digestibility; NH3-N: ammonia nitrogen; TVFA: total volatile fatty acids; CH4: methane; DMI: dry matter intake; ECMY: energy-corrected milk yield.
Table 4. Analysis of publication bias.
Table 4. Analysis of publication bias.
OutcomesObserved SignificanceTarget SignificanceNFS NumberNumber of
Comparisons (n)		NFS > [5 (n) + 10]
DMI0.28780.05041NA
MY0.19150.05035NA
ECMY0.27080.05021NA
FE0.06920.05017NA
MFY0.85890.05018NA
MPY0.42460.05018NA
MLY0.33320.05017NA
MFC<0.0010.0528333175
MPC<0.0010.0524733175
MLC0.07750.05032NA
TS0.67460.05013NA
MUN0.00080.0525319105
SCC<0.0010.053241795
Iodine<0.0010.0510101585
Bromoform0.09620.0504NA
DMD0.26710.05011NA
OMD0.65110.05015NA
CPD0.18900.05015NA
NDFD0.45620.05015NA
ADFD0.65310.0509NA
Ruminal pH0.06480.0509NA
NH3-N0.07290.0506NA
TVFA0.33910.05012NA
Acetate0.12110.05010NA
Propionate0.06340.05010NA
Butyrate0.19410.05010NA
Valerate0.07400.05010NA
Acetate/propionate0.06470.0508NA
CH4 production <0.00010.0520122120
CH4 yield<0.00010.0518720110
CH4 intensity0.32760.05019NA
DMI: dry matter intake; MY: milk yield; ECMY: energy-corrected milk yield; FE: feed efficiency; MFY: milk fat yield; MPY: milk protein yield; MLY: milk lactose yield; MFC: milk fat content; MPC: milk protein content; MLC: milk lactose content; TS: total solids; MUN: milk urea nitrogen; SCC: somatic cell count; DMD: dry matter digestibility; OMD: organic matter digestibility; CPD: crude protein digestibility; NDFD: neutral detergent fiber digestibility; ADFD: acid detergent fiber digestibility; NH3-N: ammonia nitrogen; TVFA: total volatile fatty acids; CH4: methane; n: number of comparisons; NFS: fail-safe number; NA: Rosenberg’s test does not apply since the observed significance level was greater than 0.05.
Table 5. Meta-regression of the effects of dietary seaweed supplementation on growth performance of dairy cows.
Table 5. Meta-regression of the effects of dietary seaweed supplementation on growth performance of dairy cows.
Outcomes QMDfp-ValueR2 (%)
Experimental design2.87910.0903.53
Days in milk1.47010.4800.62
Forage level0.73810.6070.00
Dry matter intake (DMI)Seaweed dose2.13320.3444.27
Suplementation period0.03710.8480.00
Seaweed type19.6831<0.00161.18
Seaweed specie38.2668<0.00175.97
Experimental design0.84710.3570.00
Days in milk0.02810.9860.00
Forage level4.18410.1230.00
Milk yield (MY)Seaweed dose1.55120.4602.41
Suplementation period0.08010.7780.00
Seaweed type28.5411<0.00166.68
Seaweed specie44.45910<0.00166.10
Experimental design0.04110.8400.00
Days in milk1.54410.6421.74
Forage level0.00310.9550.00
Energy corrected milk yield (ECMY)Seaweed dose3.21220.2011.07
Suplementation period1.63110.2023.18
Seaweed type25.0741<0.00172.40
Seaweed specie44.1505<0.00183.08
Experimental design2.32710.1272.79
Days in milk0.53610.4640.00
Forage level0.03210.8580.00
Methane (CH4) production, g/dSeaweed dose2.83620.2423.17
Suplementation period0.26910.6040.00
Seaweed type12.1841<0.00139.68
Seaweed specie27.5267<0.00158.26
QM: coefficient of moderators; QM is considered significant at p ≤ 0.05; df: degree of freedom; R2: the amount of heterogeneity accounted for.
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Orzuna-Orzuna, J.F.; Lara-Bueno, A.; Mendoza-Martínez, G.D.; Miranda-Romero, L.A.; Vázquez Silva, G.; de la Torre-Hernández, M.E.; Sánchez-López, N.; Hernández-García, P.A. Meta-Analysis of Dietary Supplementation with Seaweed in Dairy Cows: Milk Yield and Composition, Nutrient Digestibility, Rumen Fermentation, and Enteric Methane Emissions. Dairy 2024, 5, 464-479. https://doi.org/10.3390/dairy5030036

AMA Style

Orzuna-Orzuna JF, Lara-Bueno A, Mendoza-Martínez GD, Miranda-Romero LA, Vázquez Silva G, de la Torre-Hernández ME, Sánchez-López N, Hernández-García PA. Meta-Analysis of Dietary Supplementation with Seaweed in Dairy Cows: Milk Yield and Composition, Nutrient Digestibility, Rumen Fermentation, and Enteric Methane Emissions. Dairy. 2024; 5(3):464-479. https://doi.org/10.3390/dairy5030036

Chicago/Turabian Style

Orzuna-Orzuna, José Felipe, Alejandro Lara-Bueno, Germán David Mendoza-Martínez, Luis Alberto Miranda-Romero, Gabriela Vázquez Silva, María Eugenia de la Torre-Hernández, Nallely Sánchez-López, and Pedro Abel Hernández-García. 2024. "Meta-Analysis of Dietary Supplementation with Seaweed in Dairy Cows: Milk Yield and Composition, Nutrient Digestibility, Rumen Fermentation, and Enteric Methane Emissions" Dairy 5, no. 3: 464-479. https://doi.org/10.3390/dairy5030036

APA Style

Orzuna-Orzuna, J. F., Lara-Bueno, A., Mendoza-Martínez, G. D., Miranda-Romero, L. A., Vázquez Silva, G., de la Torre-Hernández, M. E., Sánchez-López, N., & Hernández-García, P. A. (2024). Meta-Analysis of Dietary Supplementation with Seaweed in Dairy Cows: Milk Yield and Composition, Nutrient Digestibility, Rumen Fermentation, and Enteric Methane Emissions. Dairy, 5(3), 464-479. https://doi.org/10.3390/dairy5030036

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