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Journal of Animal Science logoLink to Journal of Animal Science
. 2021 Sep 24;99(10):skab267. doi: 10.1093/jas/skab267

Potential use of ground brown rice for weanling pigs

Jeong Jae Lee 1,4,#, Sheena Kim 2,4,#, Jin Ho Cho 3, Hyunjin Kyoung 4, Seonmin Lee 4, Jeehwan Choe 5, Yanhong Liu 6, Peng Ji 7, Xia Xiong 8, Younghoon Kim 9, Hyeun Bum Kim 2, Minho Song 4,
PMCID: PMC8525501  PMID: 34558617

Abstract

The purpose of the current study was to assess the effects of substituting corn with ground brown rice on growth performance, immune status, and gut microbiota in weanling pigs. Seventy-two weanling pigs (28 d old with 6.78 ± 0.94 kg body weight [BW]) were randomly allotted to two dietary treatments with six pens and six pigs (three barrows and gilts) per pen within a randomized complete block design. The control pigs were fed a typical diet for weanling pigs based on corn and soybean meal diet (control diet: CON), and the other pigs were fed a formulated diet with 100% replacement of corn with ground brown rice for 35d (treatment diet: GBR). Growth performance, immune status, and gut microbiota of weanling pigs were measured. The substitution of corn with GBR did not affect growth performance or diarrhea frequency. Additionally, there were no differences in white blood cell number, hematocrit, cortisol, C-reactive protein, and serum tumor necrosis factor-alpha levels between pigs fed CON or GBR for the first 2 wk after weaning. However, weanling pigs fed GBR had lower (P < 0.05) serum transforming growth factor-beta 1 level than those fed CON. Furthermore, weanling pigs fed GBR had increased (P < 0.05) relative abundance of phylum Firmicutes and genus Lactobacillus and Streptococcus and decreased (P < 0.05) relative abundance of phylum Bacteroidetes and genus Clostridium and Prevotella in the gut microbiota compared with those fed CON. In conclusion, there was no significant difference in growth performance when corn was replaced with ground brown rice in diets for weanling pigs. Furthermore, the substitution of corn with ground brown rice in weaning diet modulated immune status and gut microbiota of pigs by increasing beneficial microbial communities and reducing harmful microbial communities. Overall, ground brown rice-based diet is a potential alternative to corn-based diet without negative effects on growth performance, immune status, and gut microbiota changes of weanling pigs.

Keywords: ground brown rice, growth performance, gut microbiota, immune status, weanling pigs

Introduction

Rice is grown in many Asian countries and is consumed as a staple grain in human diets. Many studies have examined the starch properties of rice that are related to the variety or processing method (Arns et al., 2015; Chelliah et al., 2019; Kim et al., 2021a); polished white rice contains more than 75% starch and has low fiber content (Li et al., 2004). Paddy rice is processed in several steps to produce polished final products such as brown and white rice for human consumption (Kaur et al., 2016). However, rice byproducts generated during processing and stale rice that cannot be used for human consumption may be used in the feeding of animals (Farrell and Hutton, 2017). Replacing corn with rice in diets for weanling (Devi et al., 2015; Casas and Stein, 2016; Yagami and Takada, 2017) or growing pigs (Casas et al., 2018; Fan et al., 2020; Kim et al., 2021b) improved growth performance and nutrient digestibility without negative effects. It has also been reported that rice feeding prevents diarrhea in weanling pigs (Pluske et al., 2003). In particular, brown rice is more nutritious than corn, containing 3,801 kcal/kg of gross energy and 8.0% crude protein (Piao et al., 2002), with higher starch content and more essential amino acids, minerals, and fatty acids than corn (Li et al., 2006). In addition, brown rice is cheaper to process than white rice (Saleh et al., 2019), and brown rice byproducts are also relatively cheaper in price than corn (Piao et al., 2002). The bioactive compounds such as phenolic acids, flavonoids, aminobutyric acid, γ-oryzanol, α-tocopherol, and γ-tocotrienol in brown rice have beneficial effects on immune functions and gut health (Pluske et al., 2003; Wu et al., 2013a; Saleh et al., 2019; Liang et al., 2020). Due to these properties, brown rice can potentially replace corn in swine diets without negatively affecting growth performance, nutrient digestibility, and gut health.

The nutritional quality and functionality of brown rice have beneficial effects on human health in food nutrition (Wu et al., 2013b; Lin et al., 2019; Saleh et al., 2019). Most studies examining the replacement of corn with brown rice in pig diets have focused on nutrient utilization and growth performance. However, information about corn replacement with brown rice on growth performance, immune status, and gut microbiota of weanling pigs is limited. Thus, it was hypothesized that when ground brown rice completely replace corn in diets for weanling pigs, there would be alters in the gut microbiota without negative effects on growth performance and immune responses. Therefore, the purpose of this study was to investigate the effects of substituting corn with ground brown rice in weaning diets on growth performance, immune status, and gut microbiota of weanling pigs.

Materials and Methods

All animal protocols of this experiment were reviewed and approved by the Institutional Animal Care and Use Committee of the Chungnam National University, Daejeon, Korea (approval no. CNU-00780). The animal study was conducted based on the guidelines of the Declaration of Helsinki.

Experimental animals and design

Pigs (Duroc × Landrace × Yorkshire) were weaned at 28 d old with an initial average body weight (BW) of 6.78 ± 0.94 kg. Seventy-two weanling pigs were randomly allotted to two dietary treatments of CON- and GBR-based diets with six pens and six pigs (three barrows and gilts) per pen in a randomized complete block design with BW as blocking criteria.

Diets

Pigs in the control group were fed a typical diet for weanling pigs based on corn–soybean meal (CON), and pigs in the treatment group were fed a formulated diet with 100% replacement of corn with ground brown rice for 35d (GBR). Experimental diets were made from the same base mix and formulated to meet nutrient requirements for weanling pigs (NRC, 2012) with both diets having comparable concentrations of crude protein, calcium, and phosphorus contents (Table 1). All diets were provided in mash form and did not contain animal plasma, antibiotics, or zinc oxide to prevent the antibacterial and the physiological effects. Experimental diets were fed to weanling pigs for 5 wk. All pigs were housed in an environmentally controlled room and had free access to diets and water during the entire period.

Table 1.

Composition of experimental diet of weanling pigs

Items Diets1
CON GBR4
Ingredient, %
 Corn 49.86
 Ground brown rice 49.86
 Whey powder 12.50 12.50
 Soybean meal (44%) 25.00 25.00
 Soy protein concentrate 6.25 6.25
 Soybean oil 3.00 3.00
 Limestone 1.14 1.14
 Monocalcium phosphate 1.05 1.05
 Vitamin premix2 0.20 0.20
 Mineral premix3 0.20 0.20
l-lysine-HCl (78.8%) 0.45 0.45
dl-methionine 0.16 0.16
l-threonine 0.13 0.13
l-valine 0.06 0.06
 Total 100.00 100.00
Analyzed value
 Dry matter, % 95.93 95.42
 Crude protein, % 22.04 22.53
 Gross energy, kcal/kg 3,988 4,112
Calculated energy and nutrients
 Metabolizable energy, kcal/kg 3,465 3,574
 Crude protein, % 21.26 21.52
 Calcium, % 0.81 0.81
 Phosphorus, % 0.65 0.67
 Lysine, % 1.53 1.57
 Methionine, % 0.47 0.48
 Total sulfur amino acid, % 0.83 0.82
 Threonine, % 0.95 0.97
 Tryptophan, % 0.25 0.31

1CON, weanling diet based on corn and soybean meal; GBR, diet with 100% replacement of corn with ground brown rice.

2Vitamin premix provided the following quantities of vitamin per kilogram of complete diet: vitamin A, 12,000 IU; vitamin D3, 2,500 IU; vitamin E, 30 IU; vitamin K3, 3 mg; d-pantothenic acid, 15 mg; nicotinic acid, 40 mg; choline, 400 mg; and vitamin B12, 12 μg.

3Mineral premix provided the following quantities of mineral per kilogram of complete diet: Fe, 90 mg from iron sulfate; Cu, 8.8 mg from copper sulfate; Zn, 100 mg from zinc oxide; Mn, 54 mg from manganese oxide; I, 0.35 mg from potassium iodide; and Se, 0.30 mg from sodium selenite.

4Analyzed value of ground brown rice: dry matter, 85.5%; crude protein, 9.13%; crude fat, 2.71%; ash, 1.38%; crude fiber, 6.68%; and calcium, 0.03%.

Experimental process and sample collection

Pigs and feeder were weighted at days 1, 14 and 35, in order to obtain the average daily gain (ADG), average daily feed intake (ADFI), and gain to feed ratio (G:F). Because postweaning diarrhea affects weanling pigs during the first 2 wk after weaning, each pig was monitored daily for 20 d after weaning, and its feces visually assessed and assigned a diarrhea score ranging from 1 to 5 by two independent evaluators (1 = well-formed feces, 2 = damp feces, 3 = shapeless feces, 4 = runny feces, and 5 = watery severe diarrhea). Diarrhea frequency was calculated by counting pig days with a pen average diarrhea score of 3 or higher (Lee et al., 2020a). Blood samples were collected at days 1, 3, 7, and 14 after weaning through the jugular vein of one selected pig (average BW of 7.8 ± 0.59 kg; a barrow) in each pen within a treatment via vacuum tubes (BD, Franklin Lakes, NJ, USA) with or without an anticoagulant (ethylenediaminetetraacetic acid). The serum samples were obtained after centrifuging the coagulated blood for 15 min at 3,000 × g at room temperature and then stored at −80 °C. Feces samples for verifying microbiota changes were obtained from randomly selected three pigs per dietary treatment on the last day (day 35 after weaning) and then stored at −80 °C. Evaluation of gut microbiota was conducted using the metagenome analysis (Guevarra et al., 2018) and designed according to previous studies (Lin and Yu, 2020; Park et al., 2020; Xu et al., 2020; Kim et al., 2021b).

Sample analysis

White blood cells and hematocrit counts were measured using a hematology analyzer (scil Vet abc hematology analyzer, scil animal care company, F-67120 Altorf, France) calibrated with porcine blood (Lee et al., 2020b). The enzyme-linked immunosorbent assay (ELISA) kits were used to determine concentrations of serum cortisol (Cusabio, Wuhan, China), C-reactive protein (Abnova Corp., Taipei City, Taiwan), transforming growth factor-β1 (TGF-β1; R&D Systems, Inc., Minneapolis, MN, USA), and tumor necrosis factor-α (TNF-α; R&D Systems, Inc., Minneapolis, MN, USA) following the manufacturer’s protocol.

16S rRNA sequencing for gut microbiota

Genomic DNA was extracted from fecal samples by QIAamp DNA Stool Mini Kit (Qiagen, Hilden, Germany) according to their protocol. The concentration and quality of genomic DNA were evaluated using NanoDrop ND-1000 spectrophotometer (NanoDrop Technologies, DE, USA). Genomic DNA was stored for analysis at −20 °C. The V4 region of the 16S rRNA gene was amplified by the polymerase chain reaction (PCA) step using featured primers as listed previously (Kozich et al., 2013). The amplicons were sequenced by the Illumina MiSeq platform based on the directions of the manufacturer. All sequencing was conducted at Macrogen Inc. (Seoul, Korea). Raw sequence data were processed by the Mothur software and low-quality sequences were eliminated (Schloss et al., 2009). Sequencing errors and chimeras were eliminated using the UCHIME during Mothur processing (Kozich et al., 2013). The remaining high-quality sequences were categorized into operational taxonomic units (OTUs) clustering according to an identity cutoff of 97% (Caporaso et al., 2010). The sequence number was normalized by random subsampling for downstream analyses of microbial alpha diversity such as phylogenetic information; observed OTUs; Chao1, Shannon, and Simpson indices; and beta diversity (principal coordinates analysis [PCoA]).

Statistical analysis

Analyses of data were performed using the MIXED procedure of SAS statistical software (Version 9.4, 2013, SAS Inc., Cary, NC, USA; Gonçalves et al., 2016). The statistical model for growth performance, white blood cell and hematocrit counts, C-reactive protein, serum cytokines (TNF-α and TGF-β1), and cortisol included effects of dietary treatments as a fixed effect, initial BW as a random effect, and pen as the experimental unit. The χ 2 test was used to analyze data for diarrhea frequency. Alpha and beta diversities of taxonomic classification and microbial populations were analyzed using the STAMP and Prism software (Prism 5.00, GraphPad Software, La Jolla, CA, USA) as well as MicrobiomeAnalyst (https://www.microbiomeanalyst.ca/). Alpha diversity data were presented as mean ± SE. Significant differences and tendency were considered based on P < 0.05 and 0.05 ≤ P < 0.10, respectively.

Results

Growth performance

No differences in growth performance and final BW of pigs were observed between dietary treatments throughout the experiment (Table 2). During the first 20 d after weaning, no treatment effects were observed in the diarrhea frequency between CON and GBR groups (Table 2).

Table 2.

Growth performance of weanling pigs fed corn- or ground brown rice-based diets1

Items Diets2 SEM P-value
CON GBR
 Initial BW3, kg 6.77 6.78 0.40 0.980
 Final BW, kg 22.45 23.56 0.72 0.267
Day 1 to 14
 ADG3, g/d 175.00 228.00 26.16 0.182
 ADFI3, g/d 315.00 335.00 25.37 0.587
 G:F3, g/g 0.54 0.68 0.06 0.108
Day 15 to 35
 ADG, g/d 630.00 647.00 17.63 0.527
 ADFI, g/d 925.00 950.00 29.76 0.566
 G:F, g/g 0.68 0.68 0.01 0.932
Day 1 to 35
 ADG, g/d 448.00 479.00 15.40 0.183
 ADFI, g/d 681.00 704.00 21.08 0.457
 G:F, g/g 0.66 0.68 0.01 0.277
Diarrhea frequency4,% 3.84 3.87 0.43 0.674

1Data are least squares means of six replicates (six pigs per pen).

2CON, weanling diet based on corn and soybean meal; GBR, diet with 100% replacement of corn with ground brown rice.

3ADFI, average daily feed intake; ADG, average daily gain; BW, body weight; G:F, gain to feed ratio.

4Diarrhea frequency during the 20 d after weaning = (diarrhea number/days) × 100. The χ 2 test was used to analyze data for diarrhea frequency.

Blood profiles, cortisol, C-reactive protein, and serum cytokines

No differences were observed between dietary treatments in the number of white blood cells, hematocrit, C-reactive protein, and serum TNF-α of weanling pigs in the first 2 wk after weaning (Table 3). However, 3 d after weaning, the concentration of serum TGF-β1 decreased (P < 0.05) in the weanling pigs fed GBR diet compared with those fed CON diet.

Table 3.

Immune status of weanling pigs fed corn- or ground brown rice-based diets1

Items Diets2 SEM P-value
CON GBR
White blood cells, × 103/µL
 Day 1 14.07 13.07 1.46 0.232
 Day 3 12.27 11.63 1.12 0.836
 Day 7 15.97 15.77 1.27 0.229
 Day 14 23.50 19.53 1.88 0.486
Hematocrit, %
 Day 1 33.07 32.93 1.87 0.965
 Day 3 32.30 35.07 2.03 0.721
 Day 7 34.92 37.02 1.34 0.615
 Day 14 33.25 33.65 0.77 0.624
Cortisol, ng/mL
 Day 1 25.72 10.23 5.42 0.071
 Day 3 36.35 11.81 16.71 0.324
 Day 7 61.43 13.00 26.30 0.222
 Day14 10.18 10.88 4.20 0.908
C-reactive protein, ng/mL
 Day 1 70.13 85.58 19.76 0.593
 Day 3 92.29 97.96 19.98 0.845
 Day 7 123.22 98.70 26.45 0.527
 Day 14 102.64 51.53 29.78 0.253
Serum TGF-β13, pg/mL
 Day 1 1,473 1,470 5.36 0.732
 Day 3 1,458 881 182.00 0.049
 Day 7 654 267 257.00 0.305
 Day 14 992 450 350.00 0.583
Serum TNF-α3, pg/mL
 Day 1 113 115 7.74 0.870
 Day 3 134 132 8.44 0.825
 Day 7 121 118 10.16 0.872
 Day 14 102 106 7.60 0.710

1Data are least squares means of six replicates (one pig per pen).

2CON, weanling diet based on corn and soybean meal; GBR, diet with 100% replacement of corn with ground brown rice.

3TGF-β1, transforming growth factor-beta 1; TNF-α, tumor necrosis factor-alpha.

Diversity of gut microbiota

The fecal microbiota community diversity results are presented in Table 4. The mean total sequence numbers were 238,515 ± 62,593 reads in the CON group and 225,497 ± 117,166 reads in the GBR group. In addition, the mean of observed OTUs was 257.33 ± 27.21 in the CON group and 239.33 ± 24.70 in the GBR group. No differences in Chao, Shannon, and Simpson diversity indices were observed between the GBR and CON groups.

Table 4.

Alpha diversity analysis for gut microbiota of weanling pigs by 16S rRNA sequencing1

Diversity index Diets2 P-value
CON GBR
Total number of sequence reads 238,515 ± 62,593 225,497 ± 117,166
Observed OTUs3 257.33 ± 27.21 239.33 ± 24.70 0.444
Chao1 281.83 ±18.83 251.03 ± 20.98 0.132
Shannon 4.93 ± 0.53 4.50 ± 0.42 0.335
Simpson 0.905 ± 0.05 0.868 ± 0.06 0.447

1Data are least squares means of three replicates (one pig per pen) and presented as mean ± standard deviation.

2CON, weanling diet based on corn and soybean meal; GBR, diet with 100% replacement of corn with ground brown rice.

3OTUs, operational taxonomic units.

The PCoA plot illustrates the composition of microbial communities between the CON and GBR groups (Figure 1). During the weaning period, the distinct separation of microbial communities was not visually found between CON and GBR groups.

Figure 1.

Figure 1.

Biplot of principal coordinates analysis (PCoA) weighted UniFrac distances in gut microbiota communities from piglets’ feces. Weanling pigs were regarded as the experimental units, n = 3 for each treatment group. CON, weanling diet based on corn and soybean meal (█, red); GBR, diet with 100% replacement of corn with ground brown rice (blue, ● ).

A comparison of the relative abundance of taxonomic groups at the phylum and genus levels between CON and GBR is shown in Figure 2. The relative abundance of Firmicutes increased (P < 0.05) at the phylum level in GBR pigs compared with CON pigs (Figure 2A). However, weanling pigs fed GBR diet had a lower (P < 0.05) relative abundance of Bacteroidetes at the phylum level than those fed CON diet (Figure 2A). At the genus level, the GBR group had an increased (P < 0.05) relative abundance of Lactobacillus and Streptococcus compared with the CON group (Figure 2B). However, weanling pigs fed GBR diet had a lower (P < 0.05) relative abundance of Clostridium and Prevotella at the genus level than those fed CON diet (Figure 2B).

Figure 2.

Figure 2.

Taxonomic composition shows the relative abundance of fecal microbiota in each treatment group at the phylum level (A) and genus level (B). Weanling pigs were regarded as the experimental units, n = 3 for each treatment group. CON, weanling diet based on corn and soybean meal; GBR, diet with 100% replacement of corn with ground brown rice.

Discussion

During the paddy rice milling process, brown rice is obtained when only the husk layer is removed and the outer bran layers, which contain a large amount of nutrients, remain on the grain (Kaur et al., 2016). Brown rice contains more protein, lipids, minerals, and vitamins than white rice and is not significantly different from corn nutritionally (Li et al., 2006; Amagliani et al., 2017; Saleh et al., 2019). In addition, brown rice has higher starch content and well-balanced amino acid composition compared with corn (Li et al., 2004). The starch in brown rice is stored within the inner endosperm of rice kernel, existing as glucose polymers composed of amylose and amylopectin (Takeda et al., 1993). After starch, protein is the main component of brown rice, found in albumin, globulin, and glutelin in the outer bran layers (Amagliani et al., 2017). These nutritional properties of brown rice provide a good substitute to completely replace corn in the swine diets.

The present study showed the effects of completely replacing corn with ground brown rice in weaner diets. The BW, ADG, ADFI, and G:F ratio of weanling pigs were not different between dietary treatments during the experimental period. These observations are consistent with previously published results (Mateos et al., 2006; Li et al., 2019), showing that the replacement of corn with GBR in the weaning diets does not disrupt pig performance. Additionally, some studies have reported that pigs fed rice-based diets had better or no difference in growth performance than those fed the corn-based diets due to the type, the dietary composition, and the processing method of rice and rice byproducts (Vicente et al., 2008; Gekara et al., 2014). Generally, the fiber content of brown rice is less than that of corn (1.87% vs. 2.86%); fiber inhibits starch hydrolysis by forming a physical barrier that limits amylase access to starch granules (Li et al., 2004). High-fiber diets reportedly had negative effects on growth performance and nutrient digestibility of weanling pigs (Berrocoso et al., 2015). Moreover, starch is a major component of brown rice and corn, and the differences in starch content, composition, and structure are related to growth performance and nutrient digestibility. The digestibility of starch is inversely proportional to the amylose content and granule size, which are associated with digestive enzymes activity on the surface area (Li et al., 2019). Brown rice has less amylose content (15% to 19% vs. 25% to 35%) and smaller granule size (2 to 8 μm vs. 5 to 20 μm) than corn (Riaz, 2006). Despite these nutritional advantages of brown rice, the reason that there was no difference in growth performance in the current study might be due to the relatively poorer palatability of brown rice compared with corn during weaning period, which was mentioned in previous study (Li et al., 2002). Based on previous and present studies, it is possible to use brown rice without negative effects as a complete substitute for corn in weaner diets.

During the weaning period, piglets often suffer the stress during diet changes due to immature intestinal function. Changes in the immune status resulting from intestinal inflammation have been reported in pigs after weaning (Rhouma et al., 2017; Lee et al., 2020b). Therefore, we tested the blood profiles, cortisol, and serum cytokines of weanling pigs in two dietary treatments. Postweaning diarrhea can be considered the early symptom by the pathogenic Escherichia coli infection, which can stimulate the immune system, and we observed no difference in the diarrhea frequency between dietary treatments; however, the cortisol level in the CON group tended to be higher at the beginning of the study, which might be related to the weaning event. The functional ingredients such as phenolic acids, flavonoids, aminobutyric acid, γ-oryzanol, α-tocopherol, and γ-tocotrienol in brown rice ameliorated the inflammatory response (Saleh et al., 2019). Inflammatory cytokines provide indicators for immune and inflammatory status and are closely associated with intestinal disease caused by weaning stress. In particular, TGF-β1 has both pro- and anti-inflammatory properties and thus can enhance and repress immunities (Kany et al., 2019; Lee et al., 2019). Regulation of pro-inflammatory cytokines in the intestinal mucosa may alleviate gut dysfunction due to weaning stress (Liu et al., 2008). The outer bran layers in brown rice contain bioactive compounds, including phenolic compounds such as isoferulic, p-coumaric, vanillic, and ferulic acid (Pang et al., 2018), which enhance antioxidant activity and immune status (Wu et al., 2013a; Liang et al., 2020). In another study, a brown rice and rice bran-supplemented diet reduced liver inflammation and fibrosis in rats (Wunjuntuk et al., 2016). As an antioxidant plant extract, brown rice-derived extracts also have anti-inflammatory effects. A previous study reported that brown rice extract contains a natural anti-inflammatory agent, which inhibits gene expression and interleukin production of colon cancer cells (Quagliariello et al., 2016). The results of a recent study have shown that the combinations of brown rice and probiotics such as Lactobacilli strains in a rat model inhibited colorectal carcinogenesis by regulating antioxidant activity (Lin et al., 2019). This symbiotic produces exopolysaccharides, which have antioxidative properties via upregulating the expression of antiangiogenic genes and inactivating the inflammatory pathway (Deepak et al., 2016). Therefore, the reduced serum TGF-β1 resulting from the complete replacement of corn with ground brown rice in the weaning diets suggests effects on autoimmunity and inflammation responses.

Brown rice supplementation can modulate intestinal microbiota and enhance innate immunity, which in turn improves gut health in nursery piglets (Yang et al., 2015). We used Illumina sequencing to perform 16S rRNA gene analysis on the fecal microbiota of piglets. Intestinal microbiota is directly or indirectly involved in the gut disease by affecting digestion and absorption of nutrients as well as resistance to infection and supporting animal health. It has been reported that fermentable carbohydrates such as dietary fiber, resistant starch, and oligosaccharide within whole grain rice may improve gut health by regulating the microbial fermentation pathway in the intestine (Han et al., 2018). Dietary rice bran increased beneficial microbial communities such as Lactobacillus and Bifidobacterium in the gut microbiota of pigs (Yang et al., 2015). Fermentation of indigestible carbohydrates in brown rice by native intestinal probiotics such as Lactobacillus and Bifidobacterium generates short-chain fatty acids (SCFAs), including acetic acids, propionic acids, and butyric acids (Lin et al., 2019). SCFAs reduce intestinal pH, thereby inhibiting the growth of pathogens to maintaining intestinal health and play an important role in the prevention of intestinal inflammation and diseases and served as a primary energy source for the colonic mucosa (Han et al., 2018). It is possible that ground brown rice supplementation attributes fermentation and SCFAs production in the colon, and thus improves the formation of mucins and gut health. Ground brown rice supplementation decreased the relative abundance of genera Clostridium and Prevotella caused by increased genera Lactobacillus in the current study, which is in agreement with results of previous data (So et al., 2016; Han et al., 2018), suggesting that brown rice supplementation suppresses pathogenic bacteria that cause intestinal diseases and promotes beneficial probiotic bacteria (So et al., 2016). Therefore, ground brown rice supplementation may improve immune status and gut health of weanling pigs by increasing the relative abundance of Lactobacillus.

Conclusions

There was no significant difference in growth performance when corn was replaced with ground brown rice in diets for weanling pigs. Furthermore, the substitution of corn with ground brown rice in weaning diet modulated immune status and gut microbiota of pigs by increasing beneficial microbial communities and reducing harmful microbial communities. Overall, ground brown rice is a potential alternative to traditional feed ingredients such as corn without negative effects on pigs, as demonstrated by the growth performance, immune status, and gut microbiota changes of weanling pigs on a ground brown rice-based diet. To our knowledge, the present study is the first to demonstrate that a complete replacement of corn with ground brown rice in nursery diets correlates with growth performance, immune status, and gut microbiota of weanling pigs during the weaning period. However, more research is needed to understand the benefits and biological effects of ground brown rice as an alternative feed ingredient.

Acknowledgment

This work was supported by the National Research Foundation of Korea (NRF) grant funded by the Korean government (MSIT) (NRF-2021R1I1A3046876).

Glossary

Abbreviations

ADFI

average daily feed intake

ADG

average daily gain

BW

body weight

G:F

gain to feed ratio

OTUs

operational taxonomic units

PCoA

principal coordinates analysis

SCFAs

short-chain fatty acids

TGF-β1

transforming growth factor-beta 1

TNF-α

tumor necrosis factor-alpha

Conflict of interest statement

The authors declare that there are no competing interests.

Literature Cited

  1. Amagliani, L., O′Regan J., Kelly A. L., and O′Mahony J. A.. . 2017. The composition, extraction, functionality and applications of rice proteins: a review. Trends Food Sci. Technol. 64:1–12. doi: 10.1016/j.jpgs.2017.01.008 [DOI] [Google Scholar]
  2. Arns, B., Bartz J., Radunz M., do Evangelho J. A., Pinto V. Z., Zavareze E. d. R., and Dias A. R. G.. . 2015. Impact of heat-moisture treatment on rice starch, applied directly in grain paddy rice or in isolated starch. LWT. 60:708–713. doi: 10.1016/j.lwt.2014.10.059 [DOI] [Google Scholar]
  3. Berrocoso, J. D., Menoyo D., Guzmán P., Saldaña B., Cámara L., and Mateos G. G.. . 2015. Effects of fiber inclusion on growth performance and nutrient digestibility of piglets reared under optimal or poor hygienic conditions. J. Anim. Sci. 93:3919–3931. doi: 10.2527/jas.2015-9137 [DOI] [PubMed] [Google Scholar]
  4. Caporaso, J. G., Kuczynski J., Stombaugh J., Bittinger K., Bushman F. D., Costello E. K., Fierer N., Peña A. G., Goodrich J. K., Gordon J. I., . et al. 2010. QIIME allows analysis of high-throughput community sequencing data. Nat. Methods 7:335–336. doi: 10.1038/nmeth.f.303 [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Casas, G. A., Overholt M. F., Dilger A. C., Boler D. D., and Stein H. H.. . 2018. Effects of full fat rice bran and defatted rice bran on growth performance and carcass characteristics of growing-finishing pigs. J. Anim. Sci. 96:2293–2309. doi: 10.1093/jas/sky145 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Casas, G. A., and Stein H. H.. . 2016. Effects of full fat or defatted rice bran on growth performance and blood characteristics of weanling pigs1. J. Anim. Sci. 94:4179–4187. doi: 10.2527/jas.2016-0565 [DOI] [PubMed] [Google Scholar]
  7. Chelliah, R., Chandrashekar S., Saravanakumar K., Ramakrishnan S. R., Rubab M., Daliri E. B.-M., Barathikannan K., Tyagi A., Kwame Ofosu F., Chen X., . et al. 2019. Effect of rice processing towards lower rapidly available glucose (RAG) favors idli, a South Indian fermented food suitable for diabetic patients. Nutrients 11:1497. doi: 10.3390/nu11071497 [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Deepak, V., Ramachandran S., Balahmar R. M., Pandian S. R., Sivasubramaniam S. D., Nellaiah H., and Sundar K.. . 2016. In vitro evaluation of anticancer properties of exopolysaccharides from Lactobacillus acidophilus in colon cancer cell lines. In Vitro Cell. Dev. Biol. Anim. 52:163–173. doi: 10.1007/s11626-015-9970-3 [DOI] [PubMed] [Google Scholar]
  9. Devi, S. M., Kim S., and Kim I.. . 2015. Evaluation of effect of supplementation of extruded rice as a substitute for dried whey in the diet of weanling pigs. Vet. Med. 60:675–682. doi: 10.17221/8581-VETMED [DOI] [Google Scholar]
  10. Fan, L., Huang R., Wu C., Cao Y., Du T., Pu G., Wang H., Zhou W., Li P., and Kim S. W.. . 2020. Defatted rice bran supplementation in diets of finishing pigs: effects on physiological, intestinal barrier, and oxidative stress parameters. Animals 10:449. doi: 10.3390/ani10030449 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Farrell, D. J., and Hutton K.. . 2017. Rice and rice milling by-products. In: Thacker, P. A., and Kirkwood R. N., editors. Non-traditional feeds for use in swine production (1992). Boca Raton (FL): CRC press; p. 339–353. [Google Scholar]
  12. Gekara, O., Dokes T., and Marshall R.. . 2014. Effect of replacing corn and soybean meal with brewers rice and dried distillers brewers yeast on performance of growing-finishing pigs. Am. J. Anim. Vet. Sci. 9:110–115. doi: 10.3844/ajavsp.2014.110.115 [DOI] [Google Scholar]
  13. Gonçalves, M. A. D., Bello N. M., Dritz S. S., Tokach M. D., DeRouchey J. M., Woodworth J. C., and Goodband R. D.. . 2016. An update on modeling dose–response relationships: accounting for correlated data structure and heterogeneous error variance in linear and nonlinear mixed models1,2. J. Anim. Sci. 94:1940–1950. doi: 10.2527/jas.2015-0106 [DOI] [PubMed] [Google Scholar]
  14. Guevarra, R. B., Hong S. H., Cho J. H., Kim B. R., Shin J., Lee J. H., Kang B. N., Kim Y. H., Wattanaphansak S., Isaacson R. E., . et al. 2018. The dynamics of the piglet gut microbiome during the weaning transition in association with health and nutrition. J. Anim. Sci. Biotechnol. 9:54. doi: 10.1186/s40104-018-0269-6 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Han, F., Wang Y., Han Y., Zhao J., Han F., Song G., Jiang P., and Miao H.. . 2018. Effects of whole grain rice and wheat on composition of gut microbiota and short-chain fatty acids in rats. J. Agric. Food Chem. 66:6326–6335. doi: 10.1021/acs.jafc.8b01891 [DOI] [PubMed] [Google Scholar]
  16. Kany, S., Vollrath J. T., and Relja B.. . 2019. Cytokines in inflammatory disease. Int. J. Mol. Sci. 20:6008. doi: 10.3390/ijms20236008 [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Kaur, B., Ranawana V., and Henry J.. . 2016. The glycemic index of rice and rice products: a review, and table of GI values. Crit. Rev. Food Sci. Nutr. 56:215–236. doi: 10.1080/10408398.2012.717976 [DOI] [PubMed] [Google Scholar]
  18. Kim, S., Cho J. H., Kim Y., Kim H. B., and Song M.. . 2021b. Effects of substitution of corn with ground brown rice on growth performance, nutrient digestibility, and gut microbiota of growing-finishing pigs. Animals 11:375. doi: 10.3390/ani11020375 [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Kim, S., Cho J. H., Kim H. B., and Song M.. . 2021a. Rice as an alternative feed ingredient in swine diets. J. Anim. Sci. Technol. 63:465–474. doi: 10.5187/jast.2021.e5 [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Kozich, J. J., Westcott S. L., Baxter N. T., Highlander S. K., and Schloss P. D.. . 2013. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl. Environ. Microbiol. 79:5112–5120. doi: 10.1128/AEM.01043-13 [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Lee, J. J., Choe J., Kang J., Cho J. H., Park S., Perez-Maldonado R., Cho J. Y., Park I. H., Kim H. B., and Song M.. . 2020a. Dietary protease improves growth rate and protein digestibility of growing-finishing pigs. J. Anim. Sci. Technol. 62:313–320. doi: 10.5187/jast.2020.62.3.313 [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Lee, J. J., Choi S. H., Cho J. H., Choe J., Kang J., Kim S., Park S., Kyoung H., Seo D., Cho J. Y., . et al. 2019. Effects of dietary carbohydrases on productive performance and immune responses of lactating sows and their piglets. J. Anim. Sci. Technol. 61:359–365. doi: 10.5187/jast.2019.61.6.359 [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Lee, J. J., Kang J., Park S., Cho J. H., Oh S., Park D. J., Perez-Maldonado R., Cho J. Y., Park I. H., Kim H. B., . et al. 2020b. Effects of dietary protease on immune responses of weaned pigs. J. Anim. Sci. Technol. 62:174–179. doi: 10.5187/jast.2020.62.2.174 [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Li, J., Li D., Yin Y. L., Piao X. S., He J. H., Chen G. P., and Shu J. C.. . 2004. Performance, nutrient digestibility and intestinal disaccharidase activity of weaner/grower pigs given diets containing extruded Chinese stored brown rice with exogenous enzyme supplements. Anim. Sci. 79:429–438. doi: 10.1017/s1357729800090299 [DOI] [Google Scholar]
  25. Li, X. L., Yuan L., Piao X. S., Lai C. H., Zang J. J., Ding Y. H., Han L. J., and Han I. K.. . 2006. The nutritional value of brown rice and maize for growing pigs. Asian-Australas. J. Anim. Sci. 19:892–897. doi: 10.5713/ajas.2006.892 [DOI] [Google Scholar]
  26. Li, D. F., Zhang D. F., Piao X. S., Han I. K., Yang C. J., Li J. B., and Lee J. H.. . 2002. Effects of replacing corn with Chinese brown rice on growth performance and apparent fecal digestibility of nutrients in weanling pigs. Asian-Australas. J. Anim. Sci. 15:1191–1197. doi: 10.5713/ajas.2002.1191 [DOI] [Google Scholar]
  27. Li, E., Zhu T., Dong W., and Huang C.. . 2019. Effects of brown rice particle size on energy and nutrient digestibility in diets for young pigs and adult sows. Anim. Sci. J. 90:108–116. doi: 10.1111/asj.13127 [DOI] [PubMed] [Google Scholar]
  28. Liang, H. L., Cheng P. W., Lin H. L., Hao C. L., Ke L. Y., Chou H. Y., Tseng Y. H., Yen H. W., and Shen K. P.. . 2020. Extract of pre-germinated brown rice protects against cardiovascular dysfunction by reducing levels of inflammation and free radicals in a rat model of type II diabetes. J. Funct. Foods. 75:104218. doi: 10.1016/j.jff.2020.104218 [DOI] [Google Scholar]
  29. Lin, P. Y., Li S. C., Lin H. P., and Shih C. K.. . 2019. Germinated brown rice combined with Lactobacillus acidophilus and Bifidobacterium animalis subsp. lactis inhibits colorectal carcinogenesis in rats. Food Sci. Nutr. 7:216–224. doi: 10.1002/fsn3.864 [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Lin, K.-H., and Yu Y.-H.. . 2020. Evaluation of Bacillus iicheniformis-fermented feed additive as an antibiotic substitute: effect on the growth performance, diarrhea incidence, and cecal microbiota in weaning piglets. Animals 10:1649. doi: 10.3390/ani10091649 [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. Liu, Y., Huang J., Hou Y., Zhu H., Zhao S., Ding B., Yin Y., Yi G., Shi J., and Fan W.. . 2008. Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs. Br. J. Nutr. 100:552–560. doi: 10.1017/S0007114508911612 [DOI] [PubMed] [Google Scholar]
  32. Mateos, G. G., Martín F., Latorre M. A., Vicente B., and Lázaro R.. . 2006. Inclusion of oat hulls in diets for young pigs based on cooked maize or cooked rice. Anim. Sci. 82:57–63. doi: 10.1079/asc20053 [DOI] [Google Scholar]
  33. NRC . 2012. Nutrient requirements of swine. 11th rev. ed. Washington (DC): National Academies Press. [Google Scholar]
  34. Pang, Y., Ahmed S., Xu Y., Beta T., Zhu Z., Shao Y., and Bao J.. . 2018. Bound phenolic compounds and antioxidant properties of whole grain and bran of white, red and black rice. Food Chem. 240:212–221. doi: 10.1016/j.foodchem.2017.07.095 [DOI] [PubMed] [Google Scholar]
  35. Park, S., Lee J. J., Yang B. M., Cho J. H., Kim S., Kang J., Oh S., Park D. J., Perez-Maldonado R., Cho J. Y., . et al. 2020. Dietary protease improves growth performance, nutrient digestibility, and intestinal morphology of weaned pigs. J. Anim. Sci. Technol. 62:21–30. doi: 10.5187/jast.2020.62.1.21 [DOI] [PMC free article] [PubMed] [Google Scholar]
  36. Piao, X. S., Li D. F., Han I. K., Chen Y., Lee J. H., Wang D. Y., Li J. B., and Zhang D. F.. . 2002. Evaluation of Chinese brown rice as an alternative energy source in pig diets. Asian-Australas J. Anim. Sci. 15:89–93. doi: 10.5713/ajas.2002.89 [DOI] [Google Scholar]
  37. Pluske, J. R., Black B., Pethick D. W., Mullan B. P., and Hampson D. J.. . 2003. Effects of different sources and levels of dietary fibre in diets on performance, digesta characteristics and antibiotic treatment of pigs after weaning. Anim. Feed Sci. Technol. 107:129–142. doi: 10.1016/S0377-8401(03)00072-5 [DOI] [Google Scholar]
  38. Quagliariello, V., Iaffaioli R. V., Falcone M., Ferrari G., Pataro G., and Donsì F.. . 2016. Effect of pulsed electric fields—assisted extraction on anti-inflammatory and cytotoxic activity of brown rice bioactive compounds. Food Res. Int. 87:115–124. doi: 10.1016/j.foodres.2016.07.005 [DOI] [PubMed] [Google Scholar]
  39. Rhouma, M., Fairbrother J. M., Beaudry F., and Letellier A.. . 2017. Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Vet. Scand. 59:31. doi: 10.1186/s13028-017-0299-7 [DOI] [PMC free article] [PubMed] [Google Scholar]
  40. Riaz, M. N. 2006. Extruded snacks. In: Hui, Y. H., editor. Handbook of food science, technology, and engineering. Vol. 4. Boca Raton (FL): Taylor & Francis; p. 168. [Google Scholar]
  41. Saleh, A. S. M., Wang P., Wang N., Yang L., and Xiao Z.. . 2019. Brown rice versus white rice: nutritional quality, potential health benefits, development of food products, and preservation technologies. Compr. Rev. Food Sci. Food Saf. 18:1070–1096. doi: 10.1111/1541-4337.12449 [DOI] [PubMed] [Google Scholar]
  42. Schloss, P. D., Westcott S. L., Ryabin T., Hall J. R., Hartmann M., Hollister E. B., Lesniewski R. A., Oakley B. B., Parks D. H., Robinson C. J., . et al. 2009. Introducing mothur: open-source, platform-independent, community-supported software for describing and comparing microbial communities. Appl. Environ. Microbiol. 75:7537–7541. doi: 10.1128/AEM.01541-09 [DOI] [PMC free article] [PubMed] [Google Scholar]
  43. So, W. K. W., Law B. M. H., Law P. T. W., Chan C. W. H., and Chair S. Y.. . 2016. Current hypothesis for the relationship between dietary rice bran intake, the intestinal microbiota and colorectal cancer prevention. Nutrients. 8:569. doi: 10.3390/nu8090569 [DOI] [PMC free article] [PubMed] [Google Scholar]
  44. Takeda, Y., Tomooka S., and Hizukuri S.. . 1993. Structures of branched and linear molecules of rice amylose. Carbohydr. Res. 246:267–272. doi: 10.1016/0008-6215(93)84038-8 [DOI] [Google Scholar]
  45. Vicente, B., Valencia D. G., Pérez-Serrano M., Lázaro R., and Mateos G. G.. . 2008. The effects of feeding rice in substitution of corn and the degree of starch gelatinization of rice on the digestibility of dietary components and productive performance of young pigs. J. Anim. Sci. 86:119–126. doi: 10.2527/jas.2006-697 [DOI] [PubMed] [Google Scholar]
  46. Wu, F., Chen H., Yang N., Duan X., Jin Z., and Xu X.. . 2013a. Germinated brown rice enhances antioxidant activities and immune functions in aged mice. Cereal Chem. 90:601–607. doi: 10.1094/cchem-02-13-0039-r [DOI] [Google Scholar]
  47. Wu, F., Yang N., Touré A., Jin Z., and Xu X.. . 2013b. Germinated brown rice and its role in human health. Crit. Rev. Food Sci. Nutr. 53:451–463. doi: 10.1080/10408398.2010.542259 [DOI] [PubMed] [Google Scholar]
  48. Wunjuntuk, K., Kettawan A., Rungruang T., and Charoenkiatkul S.. . 2016. Anti-fibrotic and anti-inflammatory effects of parboiled germinated brown rice (Oryza sativa ‘KDML 105’) in rats with induced liver fibrosis. J. Funct. Foods. 26:363–372. doi: 10.1016/j.jff.2016.08.009 [DOI] [Google Scholar]
  49. Xu, X., Yang C., Chang J., Wang P., Yin Q., Liu C., Gao T., Dang X., and Lu F.. . 2020. Dietary supplementation with compound probiotics and berberine alters piglet production performance and fecal microbiota. Animals. 10:511. doi: 10.3390/ani10030511 [DOI] [PMC free article] [PubMed] [Google Scholar]
  50. Yagami, K., and Takada R.. . 2017. Dietary rice improves growth performance, mucosal enzyme activities and plasma urea nitrogen in weaning piglets. Anim. Sci. J. 88:2010–2015. doi: 10.1111/asj.12874 [DOI] [PubMed] [Google Scholar]
  51. Yang, X., Twitchell E., Li G., Wen K., Weiss M., Kocher J., Lei S., Ramesh A., Ryan E. P., and Yuan L.. . 2015. High protective efficacy of rice bran against human rotavirus diarrhea via enhancing probiotic growth, gut barrier function, and innate immunity. Sci. Rep. 5:15004. doi: 10.1038/srep15004 [DOI] [PMC free article] [PubMed] [Google Scholar]

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