Insights into sub-chronic toxicity effects of enzymatic hydrolysate of peony seed meal derived Maillard reaction products in SD rats

Abstract

Despite the use of Maillard reaction products (MRPs) as food flavoring and coloring agents, they are also known to constitute acrylamide, heterocyclic amines, advanced glycosylation end products, and precursors of low molecular weight compounds. The very little is known about the toxicology of peony seed meal-derived MRPs. In this study, sub-chronic toxicity of peony seed meal derived MRPs was evaluated in Sprage-Dawley (SD) rats. Results showed that the body weight, hematology and serum biochemistry, organ coefficient and histopathology of SD rats with daily intake of peony seed meal-derived MRPs lower than 0.45 g/kg were not affected. After feeding with peony seed meal-derived MRPs for 13-weeks, there were no significant toxic effect on either male or female rats. This study provides a theoretical basis for the safety of MRPs derived from the reactants of enzymatic hydrolysis of peony seed meal.

Keywords:
peony seed meal; Maillard reaction products; sub-chronic toxicity; safety

1 Introduction

Maillard reaction (MR) is a covalent grafting reaction between amino groups and carbonyl groups, also known as "non-enzymatic Browning reaction" (Shakoor et al., 2022). On the one hand, the MR is known to contribute flavor and color during food processing, leading to better taste and improved nutritional value (Bai et al., 2022; Kul et al., 2021). On the other hand, external sugars and amino acids are introduced into food through MR (Cao et al., 2022; Xiao et al., 2021).

MPRs also have antioxidant properties and can be used as oxidants in the food industry (Wei et al., 2022; Chen et al., 2022). The antioxidants of MPRs are derived from the interactions between sugars, essential amino acids, and peptides in foods (Han et al., 2021; Fu et al., 2020). Recently, it has been reported that a variety of bacteria can be inhibited by MRPs derivatives, which have significant antimicrobial activity (Chen et al., 2021; Hafsa et al., 2021). Despite their positive effects and potential application in food industry, studies have also highlighted their negative effects on food quality and safety when the reaction is not properly controlled. Under abnormal MR conditions, certain hzaradous and toxic substances such as acrylamide and heterocyclic amines are produced (Wei et al., 2019a; Quan et al., 2021). In addition, MR also produces advanced glycosylation end products, which can produce toxic substances. At present, the study of MRP in food toxicology only focuses on the amino acid - reducing sugar model (Shang et al., 2020; Lu et al., 2022).

Peony is widely planted in China, and peony seeds contain high omega-3 fatty acids (Qu et al., 2017; Wang et al., 2022). The polysaccharides extracted from peony seed dreg displayed high anti-oxidant (Shi et al., 2016a; Shi et al., 2016b; Zhang et al., 2022), and anti-cancerous properties (Zhang et al., 2017). After chemical modifications, the antioxidant activities (Li et al., 2018b; Li et al., 2021) and antibacterial activities (Li et al., 2018a; Liu et al., 2022) were increased significantly. A novel peptide SMRKPPG was identified from peony seed dregs, and exhibited remarkable antioxidant activities, especially, radical scavenging capacities and reducing power (Zhang et al., 2019). The phospholipids prepared from peony seed dregs are enriched in polyunsaturated fatty acids, and can be used as emulsifiers with improved antioxidant properties (Xia et al., 2022). In our previous research, sugar, PSH and L-cysteine were used to evaluate the effect of sugar types on MRPs from peony seed dregs, and the free amino acids, and volatile compounds of the products were determined (Shang et al., 2020). Furthermore, we investigated the effects of oxidized chicken fats produced in different ways on peony seed meal-derived MRPs, and results demonstrated that the meat flavor and Maillard reaction could be promoted by chicken fat (Xia et al., 2021). However, the very little is known about the toxicology of peony seed meal-derived MRPs.

Therefore, the main purpose of this study was to analyze and evaluate the safety of MRP obtained from enzymatic hydrolysates of peony seed meal, xylose, and L-cysteine. Therefore, this study provides a sub-chronic safety assessment of MPRs for evaluating its subsequent product development.

2 Materials and methods

2.1 Preparation of MRPs

Peony seed meal was purchased from Beijing Tongrentang Anhui Traditional Chinese Medicine Co., LTD. According to the previous studies (Zheng et al., 2022; Wei et al., 2019b; Shang et al., 2020), peony seed enzymatic hydrolysates were prepared and mixed with xylose and L-cysteine in a substrate solution with a concentration of 10% according to the mass ratio of w/w/w = 10:3:1.5 and pH 7.5 followed by heating at 120 °C for 2 h. After the reaction, the supernatant was centrifuged and freeze-dried to obtain MRPs samples, which were crushed and sieved through 80 mesh and stored at -20 °C until next use (Ni et al., 2022).

2.2 Experimental animals and treatments

Five-week-old SPF rats (Anhui Medical University) were used in the experiment, according to the regulations of Animal Care institutions and committees of Hefei University of Technology, China. The experimental environment was maintained at controlled humidity (60 ± 10%), light (12 h day/night), and temperature (22 ± 2 °C) in animal room provided by Hefei University of Technology. The general signs and mortality of each SD rat were recorded daily, and the body weight and food intake were recorded weekly. Sub-chronic toxicity tests were carried out according to the method of (Wei et al., 2019a). The daily intake of MRPs in the control (CG), the low dose (LDG), the medium dose (MDG), and the high dose (HDG) groups was 0.00, 0.15, 0.45, and 1.35 g/kg BW, respectively (Figure 1). The general signs and mortality of each SD rat were recorded daily. The body weight and food intake of SD rats were recorded weekly (Gao et al., 2022). Blood samples were obtained according to the method of (Wei et al., 2019a), and histopathology was performed at the end of the experiment (Wu et al., 2020).

Figure 1
Experimental design. The SD rat in the control (CG), the low dose (LDG), the medium dose (MDG), and the high dose (HDG) groups were administrated with peony seed meal-derived MRPs at 0.00, 0.15, 0.45, and 1.35 g/kg BW, respectively. After 13 weeks, the SD rats were euthanized and used for further experiments.

2.3 Hematology and serum biochemistry

The animal blood counter (BC-2800VET, Mindray, China) was used for hematological assessment based on hematological parameter: White blood cell (WBC), lymphocyte (LYM), monocyte (Mon), neutrophil (Gran), red blood cell (RBC), hemoglobin (HGB), hematocrit (HCT), mean corpuscular volume (MCV), mean corpuscular hemoglobin content (MCH), mean corpuscular hemoglobin concentration (MCHC), RBC volume distribution width (RDW), platelet count (PLT), mean platelet volume (MPV), platelet distribution width (PDW) and platelet hematocrit (PCT).

Serum biochemical parameters were analyzed by automatic biochemical analyzer (Chemray 240, Rayto, China). The serum biochemical parameters such as alanine aminotransferase (ALT), aspartate aminotransferase (AST), urea nitrogen (BUN), creatinine (Cr), glucose (Glu), total protein (TP), albumin (Alb), total cholesterol (TC), triglyceride (TG), chlorine (Cl), potassium (K), and sodium (Na).

2.4 Viscera coefficient

The test animals were dissected and weighed for the following organs: liver, kidney, spleen, testis, and ovaries. The paired organs (testes, kidneys, and ovaries) were weighed against each other. Absolute organ weight was the weight of the organ itself, and relative organ weight was the percentage of organ weight to body weight.

2.5 Histopathology

By paraffin embedding machine (EG1150C, Germany); Tissue microtome (NVSLM1, WPI); Histopathology was performed with light microscopy (CX41, OLYMPUS, Japan). SD rats in CG and HDG groups were taken for liver and kidney examination, and organs corresponding to LDG and MDG were retained. If HDG pathology was abnormal, LDG and MDG pathology studies were performed. The sectioned tissue was soaked and fixed in 10% formaldehyde buffer, cut into thin sections, dehydrated, and embedded in paraffin, stained with standard hematoxylin and eosin, and examined under light microscope (Manzoor et al., 2022).

2.6 Statistical analysis

All the experiments were repeated three times and data were analyzed by ANOVA with SPSS Statistics 20.0 and expressed as mean ± standard deviation (n = 3), (p < 0.05).

3 Results and discussion

3.1 Body weight and food consumption

In sub-chronic toxicity studies, no weight loss associated with MRPs intake was observed in SD rats fed a single dose of 0.00, 0.15, 0.45, and 1.35 g MRPs/kg BW for 90 days (p > 0.05) (Figure 2). During the first five weeks of the experiment, there was little difference in body weight between the different groups of male rats, and after the fifth week, there was an increasing difference in body weight between SD rats compared to the first five weeks. The body weight of female rats in LDG group became larger than that in other groups from the 9th week, and the body weight difference gradually decreased after the 11th week. On the other hand, except HDG (p < 0.05), no difference in food consumption was detected in CG, LDG, and MDG (p > 0.05) (Figure 3). During sub-chronic toxicity tests, no associated clinicopathological symptoms or death were observed in SD rats ingested with MRPs. There was significant difference in feed consumption between male HDG group and CG group (p < 0.05) (Figure 3).

Figure 2
Changes in body weight of Sprague-Dawley rats during sub-chronic toxicity tests. (a) male; (b) female.

Figure 3
Feed consumption in Sprague-Dawley rats during sub-chronic toxicity tests. Compared with the control group of the same sex (CG), *p < 0.05.

3.2 Hematological and serum biochemical analysis

Table 1 shows a summary of the hematological data of MRPs feeding. There were significant differences in erythrocytes in HDG group (p < 0.05). The chronic toxicity of feeding experiments, rats of WBC, LYM, Mon, Gran, RBC, HGB, HCT, MCH, MCHC, RDW, MCH, MCHC, RDW, PDW had no obvious change (p > 0.05). The blood biochemical parameters in the sub-chronic feeding toxicity study are summarized in Table 1. In the trial there was no significant effect on hematological indexes (p > 0.05).

Table 1
Blood routine parameters and serum biochemical parameters of Sprague-Dawley rats fed MRPs. Comparison between different dose groups and the same sex control group, the different superscript letters represent significant differences at p < 0.05.

Hematological parameters	Male							Female
	CG		LDG		MDG		HDG	CG		LDG		MDG	HDG
White blood cells (109/L)	6.24 ± 1.19a		5.72 ± 1.35a		6.14 ± 1.11a		6.46 ± 1.44a	6.68 ± 1.15a		5.94 ± 1.44a		6.36 ± 1.31a	5.68 ± 1.29a
Lymphocytes (109/L)	4.02 ± 1.52a		3.92 ± 1.47a		4.28 ± 1.41a		4.42 ± 1.49a	4.62 ± 1.06a		4.14 ± 1.29a		4.32 ± 1.43a	3.94 ± 1.19a
Monocytes (109/L)	0.48 ± 0.08a		0.42 ± 0.15a		0.44 ± 0.21a		0.36 ± 0.15a	0.44 ± 0.13a		0.38 ± 0.19a		0.48 ± 0.19a	0.42 ± 0.18a
Neutrophils (109/L)	1.74 ± 0.53a		1.38 ± 0.59a		1.42 ± 0.39a		1.68 ± 0.51a	1.62 ± 0.39a		1.41 ± 0.58a		1.56 ± 0.38a	1.34 ± 0.44a
Red blood cells (1012/L)	8.36 ± 0.20a		8.40 ± 0.51a		7.70 ± 0.58ab		7.41 ± 0.82b	7.48 ± 0.68a		7.21 ± 0.72ab		7.08 ± 0.53ab	6.56 ± 0.37b
Hemoglobin (g/L)	138.5 ± 10.7a		139.6 ± 11.1a		131.6 ± 14.2a		127.5 ± 16.1a	131.8 ± 12.1a		125.4 ± 14.9a		122.6 ± 11.1a	117.6 ± 5.0a
Hematocrit (%)	44.6 ± 3.2a		44.7 ± 3.5a		42.5 ± 4.1a		41.5 ± 5.1a	42.6 ± 3.6a		40.6 ± 3.4a		40.4 ± 3.4a	38.4 ± 2.1a
Mean corpuscular volume (fl)	53.4 ± 2.8a		53.3 ± 1.9a		55.2 ± 1.6a		55.9 ± 1.3a	57.1 ± 1.8a		56.4 ± 1.6a		57.1 ± 0.6a	58.6 ± 1.8a
Mean corpuscular hemoglobin (pg)	16.5 ± 1.0a		16.6 ± 0.7a		17.0 ± 0.7a		17.2 ± 0.8a	17.6 ± 0.4a		17.3 ± 0.9a		17.2 ± 0.3a	17.9 ± 0.6a
Mean corpuscular hemoglobin concentration (g/L)	309.8 ± 6.4a		311.6 ± 3.8a		308.8 ± 7.0a		307.0 ± 8.0a	308.8 ± 4.5a		308.0 ± 15.0a		303.2 ± 3.6a	306.2 ± 5.9a
Red cell distribution width (%)	14.6 ± 0.9a		14.1 ± 0.6a		14.0 ± 0.8a		13.7 ± 1.6a	13.0 ± 0.8a		13.2 ± 0.8a		12.1 ± 0.9a	12.0 ± 1.4a
Platelets (109/L)	742 ± 169a		727 ± 168a		773 ± 147a		806 ± 193a	714 ± 153a		761 ± 142a		816 ± 146a	791 ± 157a
Hematological parameters	Male							Female
	CG	LDG		MDG		HDG		CG	LDG		MDG		HDG
Mean platelet volume (fl)	5.08 ± 0.60a	5.24 ± 0.76a		5.42 ± 0.53a		5.28 ± 0.67a		5.38 ± 0.69a	5.52 ± 0.46a		5.24 ± 0.59a		5.44 ± 0.77a
Platelet distribution width (%)	16.9 ± 0.2a	16.8 ± 0.2a		16.8 ± 0.3a		17.0 ± 0.2a		17.1 ± 0.5a	17.4 ± 0.6a		17.2 ± 0.4a		17.2 ± 0.6a
	0.373 ± 0.070a	0.387 ± 0.125a		0.423 ± 0.110a		0.431 ± 0.141a		0.389 ± 0.112a	0.417 ± 0.064a		0.431 ± 0.122a		0.423 ± 0.068a
Serum biochemistry parameters
Alanine aminotransferase (U/L)	55.78 ± 7.53a	52.14 ± 8.19a		59.46 ± 10.41a		64.34 ± 10.56a		51.81 ± 8.86a	50.51 ± 10.24a		49.18 ± 8.02a		54.55 ± 12.16a
Aspartate aminotransferase (U/L)	129.32 ± 12.31a	124.15 ± 12.42a		127.45 ± 9.43a		132.06 ± 12.01a		135.92 ± 13.88a	133.27 ± 12.76a		130.74 ± 14.94a		128.14 ± 10.69a
Blood urea nitrogen (mg/dL)	19.65 ± 2.65a	19.09 ± 2.92a		20.48 ± 3.16a		21.32 ± 3.79a		21.86 ± 3.05a	20.54 ± 3.11a		22.72 ± 3.86a		21.43 ± 3.17a
Total protein (g/L)	76.67 ± 3.91a	76.28 ± 4.21a		73.62 ± 4.04a		74.12 ± 3.83a		83.96 ± 6.43a	80.74 ± 5.86a		79.29 ± 3.11a		84.58 ± 4.25a
Creatinine (μmol/L)	32.52 ± 5.63a	31.68 ± 4.18a		34.61 ± 6.52a		36.48 ± 8.35a		29.83 ± 4.01a	30.88 ± 2.78a		35.46 ± 6.36a		33.76 ± 5.63a
Glucose (mmol/L)	5.69 ± 0.46a	5.81 ± 0.54a		5.73 ± 0.61a		5.62 ± 0.41a		5.47 ± 0.53a	5.41 ± 0.49a		5.56 ± 0.42a		5.35 ± 0.47a
Albumin (g/L)	34.22 ± 3.29a	35.34 ± 3.58a		34.68 ± 3.02a		35.92 ± 3.71a		37.03 ± 3.69a	36.17 ± 2.75a		37.46 ± 2.96a		35.62 ± 3.18a
Total cholesterol (mmol/L)	2.17 ± 0.34a	2.04 ± 0.29a		1.96 ± 0.20a		2.29 ± 0.37a		1.98 ± 0.24a	2.13 ± 0.34a		2.35 ± 0.41a		2.18 ± 0.26a
Triglyceride (mmol/L)	0.74 ± 0.16a	0.69 ± 0.11a		0.61 ± 0.13a		0.72 ± 0.14a		0.68 ± 0.12a	0.63 ± 0.11a		0.71 ± 0.15a		0.59 ± 0.09a
Cl (mmol/L)	106.24 ± 4.95a	108.48 ± 5.81a		110.51 ± 7.42a		107.72 ± 6.39a		103.83 ± 4.56a	107.19 ± 6.07a		105.67 ± 5.18a		110.75 ± 8.23a
K (mmol/L)	6.45 ± 0.74a	5.92 ± 0.57a		6.91 ± 0.83a		5.67 ± 0.62a		5.83 ± 0.49a	6.24 ± 0.64a		6.05 ± 0.62a		6.12 ± 0.51a
Na (mmol/L)	143.42 ± 6.04a	147.51 ± 7.38a		141.38 ± 5.86a		145.64 ± 5.29a		140.85 ± 5.85a	145.61 ± 6.07a		142.96 ± 6.23a		148.57 ± 7.64a

3.3 Hematological and serum biochemical analysis

As shown in Table 2, the relative weight difference of liver organs between the MDG group and the HDG group (p < 0.05). The other organs, absolute organs and relative organs of SD rats ingested with MRPs had no effect (p > 0.05).

Table 2
Absolute and relative organ weights in Sprague-Dawley Rats administered with MRPs for 13 weeks comparison between different dose groups and the same sex control group, the different superscript letters represent significant differences at p < 0.05.

Parameters	CG	LDG	MDG	HDG
Male
Body weight (g)	555.76 ± 69.86a	511.96 ± 25.13a	519.24 ± 32.14a	507.74 ± 62.41a
Absolute organ weight (g)
Liver	13.80 ± 1.41a	12.83 ± 0.78a	13.99 ± 1.30a	13.06 ± 1.39a
Kidney	3.44 ± 0.49a	3.12 ± 0.18a	3.06 ± 0.17a	3.29 ± 0.34a
Spleen	1.27 ± 0.10a	1.33 ± 0.18a	1.26 ± 0.27a	1.03 ± 0.23a
Testis	3.51 ± 0.13a	3.42 ± 0.13a	3.41 ± 0.20a	3.29 ± 0.33a
Relative organ weight (%)
Liver	2.43 ± 0.10c	2.51 ± 0.04cb	2.69 ± 0.10a	2.61 ± 0.08ab
Kidney	0.60 ± 0.02ab	0.61 ± 0.06ab	0.59 ± 0.04b	0.66 ± 0.03a
Spleen	0.22 ± 0.01a	0.26 ± 0.02a	0.24 ± 0.04a	0.20 ± 0.02a
Testis	0.62 ± 0.05a	0.67 ± 0.01a	0.66 ± 0.00a	0.66 ± 0.03a
Female
Body weight (g)	335.34 ± 35.35a	345.54 ± 29.56a	334.8 ± 41.73a	341.04 ± 11.00a
Absolute organ weight (g)
Liver	8.60 ± 0.65a	8.87 ± 0.77a	8.59 ± 0.79a	8.66 ± 0.56a
Kidney	2.11 ± 0.29a	2.26 ± 0.24a	2.06 ± 0.19a	2.08 ± 0.15a
Spleen	0.98 ± 0.33a	0.85 ± 0.09a	0.80 ± 0.10a	0.88 ± 0.13a
Ovary	0.26 ± 0.04a	0.29 ± 0.03a	0.27 ± 0.05a	0.28 ± 0.02a
Relative organ weight (%)
Liver	2.57 ± 0.12a	2.57 ± 0.07a	2.58 ± 0.16a	2.57 ± 0.08
Kidney	0.63 ± 0.06a	0.66 ± 0.04a	0.62 ± 0.08a	0.62 ± 0.03a
Spleen	0.29 ± 0.07a	0.25 ± 0.01a	0.24 ± 0.03a	0.26 ± 0.03a
Ovary	0.078 ± 0.007a	0.082 ± 0.001a	0.080 ± 0.005a	0.083 ± 0.003a

3.4 Macroscopic and histopathological examination

As shown in Figures 4-5, no macroscopic pathological manifestations related to MPRs were found during autopsy of SD rats. Over the course of the 13-week sub-chronic toxicity test, feeding MRPs had no significant toxic effect on either male or female rats. Compared with the CG group, no macroscopic lesions related to MRPs ingestion were found in the organs of the HDG group during the anatomical process.

Figure 4
Liver sections of Sprague-Dawley rats in control and high-dose groups (HE, ×400).

Figure 5
Kidney sections of Sprague-Dawley rats in control and high-dose groups (HE, ×400).

4 Discussion

The MRP of the enzymatic hydrolysate of peony seed meal has excellent meat flavor characteristics. According to in vivo toxicology reports, there are limited data on this meat-taste additive. Therefore, sub-chronic toxicity tests of MRP were performed to assess the safety of MRP as a meat additive or food ingredient.

During sub-chronic toxicity tests, no associated clinicopathological symptoms or death were observed in SD rats ingested with MRPs. There was significant difference in feed consumption between male HDG group and CG group (p < 0.05) (Figure 2). No adverse reactions were observed in rats ingested with MRPs. On the one hand, the MRP produced by the condensation of the carbonyl group oand the amino group in the MR produces indigestion components (Martinez-Saez et al., 2019; Arihara et al., 2021). On the other hand, reactions containing proteins or amino acids form acrylamide when subjected to high temperatures during frying and baking, acrylamide is formed (Alam et al., 2018; Knight et al., 2021).

Hematological and serum biochemical parameters can intuitively reveal whether MRP is toxic to induce hemolysis (Guefack et al., 2022). Our results showed that LDG and MDG of MRP were not significantly different in terms of hematological and serum biochemical parameters (p > 0.05); compared with the control group, the difference of red blood cells in HDG group was significant (p < 0.05). Excessive glucose in rats causes abnormal erythrocyte protein (Gilliéron et al., 2020). In toxicological tests, serum biochemical parameters and organ histopathology are the widely used (Abebe et al., 2021). Our data show that MDG and HDG groups of MRPs are not toxic tao organs, but HDG can some effects on liver function. On the other hand, as shown in Figure 3 and Figure 4, tissue sections were taken from SD rats in CG and HDG groups, as well as organ mass changes in SD rats (Table 2). Our research data showed that MRPs did not produce toxicity to most of the vital organs of SD rats.

At present, reports on MPR tend to focus on its functional research and exploration of flavor substances (Habinshuti et al., 2019). It has been reported that the MR, in the initial stage, uses sugars to rearrange ketosugars in the primary reaction of amino acids to produce active dicarbonyl compounds, which can be used as acrylamide, heterocyclic amines and advanced glycosylation end products, and can also provide food color and flavor (Liu et al., 2020). A previous study reported that 9.0% of flaxseed MPR in SD rats did not show toxicity in a 90-day chronic toxicity test (Wei et al., 2019a). SD rats fed with 9.0% flaxseed MPR for 90 days had no effect on intestinal health (Zheng et al., 2022).

In another study, the coexistence of acrylamide and acrylamide and arginine and glucose-derived MRPs effectively reduced the toxicity of acrylamide to mice (Wu et al., 2021). In this study, SD rats in the three different dose groups did not show adverse symptoms such as inflammation. The kidneys of male SD rats in MDG and HDG groups were significantly different (p < 0.05). To summarize, when the daily intake of MRPs was lower than 0.45 g/kg BW/day, there was no toxicological effect on SD rats.

5 Conclusion

In this study, the MPRs of peony seed meal were fed to SD rats, and the toxicological test showed that there were no significant differences in body weight, absolute organ weight and serum biochemical indexes of SD rats. Histopathological examination revealed no pathological symptoms associated with MRPs ingestion. When the daily intake of MRPs was lower than 0.45 g/kg BW/day, the body weight, feed consumption, histopathology, blood routine and serum biochemical indexes of SD rats were not affected.

Acknowledgements

This study was supported by the Major Projects of Science and Technology in Anhui Province (202203a06020009), and the Key Research and Development Projects of Anhui Province (202104f06020026, 202004a06020042, 202004a06020052).

• Practical Application: The main purpose of this study was to analyze and evaluate the safety of MRP obtained from enzymatic hydrolysates of peony seed meal, xylose, and L-cysteine. Therefore, the results provided a sub-chronic safety assessment of MPRs for evaluating its subsequent product development.

References

• Abebe, M. S., Asres, K., Bekuretsion, Y., Abebe, A., Bikila, D., & Seyoum, G. (2021). Sub-chronic toxicity of ethanol leaf extract of Syzygium guineense on the biochemical parameters and histopathology of liver and kidney in the rats. Toxicology Reports, 8, 822-828. http://dx.doi.org/10.1016/j.toxrep.2021.03.032 PMid:33868962.
  » http://dx.doi.org/10.1016/j.toxrep.2021.03.032
• Alam, S., Ahmad, R., Pranaw, K., Mishra, P., & Khare, S. K. (2018). Asparaginase conjugated magnetic nanoparticles used for reducing acrylamide formation in food model system. Bioresource Technology, 269, 121-126. http://dx.doi.org/10.1016/j.biortech.2018.08.095 PMid:30157443.
  » http://dx.doi.org/10.1016/j.biortech.2018.08.095
• Arihara, K., Yokoyama, I., & Ohata, M. (2021). Bioactivities generated from meat proteins by enzymatic hydrolysis and the Maillard reaction. Meat Science, 180, 108561. http://dx.doi.org/10.1016/j.meatsci.2021.108561 PMid:34034035.
  » http://dx.doi.org/10.1016/j.meatsci.2021.108561
• Bai, S., You, L., Ji, C., Zhang, T., Wang, Y., Geng, D., Gao, S., Bi, Y. Z., & Luo, R. (2022). Formation of volatile flavor compounds, maillard reaction products and potentially hazard substance in China stir-frying beef sao zi. Food Research International, 159, 111545. http://dx.doi.org/10.1016/j.foodres.2022.111545 PMid:35940754.
  » http://dx.doi.org/10.1016/j.foodres.2022.111545
• Cao, J. R., Yan, H., & Liu, L. (2022). Optimized preparation and antioxidant activity of glucose-lysine Maillard reaction products. LWT, 161, 113343. http://dx.doi.org/10.1016/j.lwt.2022.113343
  » http://dx.doi.org/10.1016/j.lwt.2022.113343
• Chen, P., Cheng, F., Wei, L., Wang, S., Zhang, Z. M., Hang, F. X., Li, K., & Xie, C. F. (2022). Effect of Maillard reaction browning factors on color of membrane clarification non-centrifugal cane sugar during storage. Food Science and Technology, 42, e43722. http://dx.doi.org/10.1590/fst.43722
  » http://dx.doi.org/10.1590/fst.43722
• Chen, X., Jiang, D., Xu, P. P., Geng, Z. M., Xiong, G. Y., Zou, Y., Wang, D. Y., & Xu, W. M. (2021). Structural and antimicrobial properties of Maillard reaction products in chicken liver protein hydrolysate after sonication. Food Chemistry, 343, 128417. http://dx.doi.org/10.1016/j.foodchem.2020.128417 PMid:33406574.
  » http://dx.doi.org/10.1016/j.foodchem.2020.128417
• Fu, Y., Zhang, Y. H., Soladoye, O. P., & Aluko, R. E. (2020). Maillard reaction products derived from food protein-derived peptides: insights into flavor and bioactivity. Critical Reviews in Food Science and Nutrition, 60(20), 3429-3442. http://dx.doi.org/10.1080/10408398.2019.1691500 PMid:31738577.
  » http://dx.doi.org/10.1080/10408398.2019.1691500
• Gao, J., Zhang, C., Qin, X., Cao, W., Chen, J., Li, Y., Zheng, H., Lin, H., & Chen, Z. (2022). Hepatoprotective effect of clam (Corbicula fluminea) protein hydrolysate on alcohol-induced liver injury in mice and partial identification of a hepatoprotective peptide from the hydrolysate. Food Science and Technology, 42, e61522. http://dx.doi.org/10.1590/fst.61522
  » http://dx.doi.org/10.1590/fst.61522
• Gilliéron, N., Hemmerle, A., Lung, T., Sakem, B., Risch, L., Risch, M., & Nydegger, U. E. (2020). Oral glucose tolerance test does not affect degree of hemoglobin glycation as measured by routine assay. Annales d’Endocrinologie, 81(6), 545-550. http://dx.doi.org/10.1016/j.ando.2020.11.003 PMid:33278381.
  » http://dx.doi.org/10.1016/j.ando.2020.11.003
• Guefack, M.-G. F., Damen, F., Ngaffo, C. M. N., & Kuete, V. (2022). Acute and sub-chronic toxicities assessment of methanol bark extract of Hypericum roeperianum in rats. South African Journal of Botany, 150, 691-701. http://dx.doi.org/10.1016/j.sajb.2022.08.006
  » http://dx.doi.org/10.1016/j.sajb.2022.08.006
• Habinshuti, I., Chen, X., Yu, J., Mukeshimana, O., Duhoranimana, E., Karangwa, E., Muhoza, B., Zhang, M., Xia, S., & Zhang, X. (2019). Antimicrobial, antioxidant and sensory properties of Maillard reaction products (MRPs) derived from sunflower, soybean and corn meal hydrolysates. LWT, 101, 694-702. http://dx.doi.org/10.1016/j.lwt.2018.11.083
  » http://dx.doi.org/10.1016/j.lwt.2018.11.083
• Hafsa, J., Smach, M. A., Mrid, R. B., Sobeh, M., Majdoub, H., & Yasri, A. (2021). Functional properties of chitosan derivatives obtained through Maillard reaction: a novel promising food preservative. Food Chemistry, 349, 129072. http://dx.doi.org/10.1016/j.foodchem.2021.129072 PMid:33556729.
  » http://dx.doi.org/10.1016/j.foodchem.2021.129072
• Han, J. R., Han, Y. T., Li, X. W., Gu, Q., Li, P., & Zhu, B. W. (2021). Antioxidant activity of Yesso scallop (Patinopecten yessoensis) female gonad hydrolysates-ribose Maillard reaction products extracted with organic reagents, before and after in vitro digestion. Food Bioscience, 43, 101262. http://dx.doi.org/10.1016/j.fbio.2021.101262
  » http://dx.doi.org/10.1016/j.fbio.2021.101262
• Knight, M., McWilliam, S., Peck, S., Koutsidis, G., Chope, G., Puddephat, I., & Wedzicha, B. (2021). Kinetic modelling of acrylamide formation during the frying of potato chips. Food Chemistry, 352, 129305. http://dx.doi.org/10.1016/j.foodchem.2021.129305 PMid:33691208.
  » http://dx.doi.org/10.1016/j.foodchem.2021.129305
• Kul, D. B., Anlar, P., Oral, Z. F. Y., Kaya, M., & Kaban, G. (2021). Furosine and Nε-carboxymethyl-lysine in cooked meat product (kavurma): effects of salt and fat levels during storage. Journal of Stored Products Research, 93, 101856. http://dx.doi.org/10.1016/j.jspr.2021.101856
  » http://dx.doi.org/10.1016/j.jspr.2021.101856
• Li, Q., Li, X. J., Ren, Z. Y., Wang, R. J., Zhang, Y., Li, J., Ma, F. Y., & Liu, X. H. (2021). Physicochemical properties and antioxidant activity of Maillard reaction products derived from Dioscorea opposita polysaccharides. LWT, 149, 111833. http://dx.doi.org/10.1016/j.lwt.2021.111833
  » http://dx.doi.org/10.1016/j.lwt.2021.111833
• Li, X. L., Thakur, K., Zhang, Y. Y., Tu, X. F., Zhang, Y. S., Zhu, D. Y., Zhang, J. G., & Wei, Z. J. (2018a). Effects of different chemical modifications on the antibacterial activities of polysaccharides sequentially extracted from peony seed dreg. International Journal of Biological Macromolecules, 116, 664-675. http://dx.doi.org/10.1016/j.ijbiomac.2018.05.082 PMid:29775705.
  » http://dx.doi.org/10.1016/j.ijbiomac.2018.05.082
• Li, X. L., Tu, X. F., Thakur, K., Zhang, Y. S., Zhu, D. Y., Zhang, J. G., & Wei, Z. J. (2018b). Effects of different chemical modifications on the antioxidant activities of polysaccharides sequentially extracted from peony seed dreg. International Journal of Biological Macromolecules, 112, 675-685. http://dx.doi.org/10.1016/j.ijbiomac.2018.01.216 PMid:29425872.
  » http://dx.doi.org/10.1016/j.ijbiomac.2018.01.216
• Liu, X., Xia, B., Hu, L. T., Ni, Z. J., Thakur, K., & Wei, Z. J. (2020). Maillard conjugates and their potential in food and nutritional industries: a review. Food Frontiers, 1(4), 382-397. http://dx.doi.org/10.1002/fft2.43
  » http://dx.doi.org/10.1002/fft2.43
• Liu, Y., Zhu, Y. L., Yang, Y., Hu, S. W., & Jiang, W. (2022). Quality improvement of shrimp (Litopenaeus vannamei) during refrigerated storage by application of Maillard peptides/water-soluble chitosan coating. Food Science & Nutrition, 10(9), 2980-2988. http://dx.doi.org/10.1002/fsn3.2894 PMid:36171773.
  » http://dx.doi.org/10.1002/fsn3.2894
• Lu, J., Li, M., Huang, Y., Xie, J., Shen, M., & Xie, M. (2022). A comprehensive review of advanced glycosylation end products and N- Nitrosamines in thermally processed meat products. Food Control, 131, 108449. http://dx.doi.org/10.1016/j.foodcont.2021.108449
  » http://dx.doi.org/10.1016/j.foodcont.2021.108449
• Manzoor, F., Nisa, M. U., Hussain, A. H., Anwar, H., Ahmad, N., & Umbreen, H. (2022). Therapeutic potential of hydrolysable tannin on weight management oxidative stress and reproductive health in polycystic rats. Food Science and Technology, 42, e63720. http://dx.doi.org/10.1590/fst.63720
  » http://dx.doi.org/10.1590/fst.63720
• Martinez-Saez, N., Fernandez-Gomez, B., Cai, W., Uribarri, J., & Castillo, M. D. (2019). In vitro formation of Maillard reaction products during simulated digestion of meal-resembling systems. Food Research International, 118, 72-80. http://dx.doi.org/10.1016/j.foodres.2017.09.056 PMid:30898355.
  » http://dx.doi.org/10.1016/j.foodres.2017.09.056
• Ni, Z. J., Wei, C. K., Zheng, A. R., Thakur, K., Zhang, J. G., & Wei, Z. J. (2022). Analysis of key precursor peptides and flavor components of flaxseed derived Maillard reaction products based on iBAQ mass spectrometry and molecular sensory science. Food Chemistry: X, 13, 100224. http://dx.doi.org/10.1016/j.fochx.2022.100224 PMid:35146413.
  » http://dx.doi.org/10.1016/j.fochx.2022.100224
• Qu, J., Zhang, F., Thakur, K., Shia, J. J., Zhang, J. G., Faisal, S., & Wei, Z. J. (2017). The effects of process technology on the physicochemical properties of peony seed oil. Grasas y Aceites, 68(2), e192. http://dx.doi.org/10.3989/gya.1058162
  » http://dx.doi.org/10.3989/gya.1058162
• Quan, W., Wu, Z., Jiao, Y., Liu, G. P., Wang, Z. J., He, Z. Y., Tao, G. J., Qin, F., Zeng, M. M., & Chen, J. (2021). Exploring the relationship between potato components and Maillard reaction derivative harmful products using multivariate statistical analysis. Food Chemistry, 339, 127853. http://dx.doi.org/10.1016/j.foodchem.2020.127853 PMid:32829247.
  » http://dx.doi.org/10.1016/j.foodchem.2020.127853
• Shakoor, A., Zhang, C., Xie, J., & Yang, X. (2022). Maillard reaction chemistry in formation of critical intermediates and flavour compounds and their antioxidant properties. Food Chemistry, 393, 133416. http://dx.doi.org/10.1016/j.foodchem.2022.133416 PMid:35696950.
  » http://dx.doi.org/10.1016/j.foodchem.2022.133416
• Shang, Y. F., Cao, H., Wei, C. K., Thakur, K., Liao, A. M., Huang, J. H., & Wei, J. Z. (2020). Effect of sugar types on structural and flavor properties of peony seed derived Maillard reaction products. Journal of Food Processing and Preservation, 44(3), e14341. http://dx.doi.org/10.1111/jfpp.14341
  » http://dx.doi.org/10.1111/jfpp.14341
• Shi, J. J., Zhang, J. G., Sun, Y. H., Qu, J., Li, L., Prasad, C., & Wei, Z. J. (2016a). Physicochemical properties and antioxidant activities of polysaccharides sequentially extracted from peony seed dreg. International Journal of Biological Macromolecules, 91, 23-30. http://dx.doi.org/10.1016/j.ijbiomac.2016.05.082 PMid:27234494.
  » http://dx.doi.org/10.1016/j.ijbiomac.2016.05.082
• Shi, J. J., Zhang, J. G., Sun, Y. H., Xu, Q. X., Li, L., Prasad, C., & Wei, Z. J. (2016b). The rheological properties of polysaccharides sequentially extracted from peony seed dreg. International Journal of Biological Macromolecules, 91, 760-767. http://dx.doi.org/10.1016/j.ijbiomac.2016.06.038 PMid:27311505.
  » http://dx.doi.org/10.1016/j.ijbiomac.2016.06.038
• Wang, C., Li, N., Wu, L., Xia, L., Hu, Z., Li, X., Qu, Z., & Yang, J. (2022). Optimization of ultrasound-homogenization combined extraction of phenolics in peony roots and leaves. Food Science and Technology, 42, e108621. http://dx.doi.org/10.1590/fst.108621
  » http://dx.doi.org/10.1590/fst.108621
• Wei, C. K., Ni, Z. J., Thakur, K., Liao, A. M., Hu, F., Huang, J. H., & Wei, Z. J. (2019a). Acute, genetic and sub-chronic toxicities of flaxseed derived Maillard reaction products. Food and Chemical Toxicology, 131, 110580. http://dx.doi.org/10.1016/j.fct.2019.110580 PMid:31202938.
  » http://dx.doi.org/10.1016/j.fct.2019.110580
• Wei, C. K., Ni, Z. J., Thakur, K., Liao, A. M., Huang, J. H., & Wei, Z. J. (2019b). Color and flavor of flaxseed protein hydrolysates Maillard reaction products: effect of cysteine, initial pH, and thermal treatment. International Journal of Food Properties, 22(1), 84-99. http://dx.doi.org/10.1080/10942912.2019.1573830
  » http://dx.doi.org/10.1080/10942912.2019.1573830
• Wei, Q.-J., Nie, P., Gong, J.-T., Wei, C.-K., Thakur, K., Hu, F., & Wei, Z.-J. (2022). Antibacterial and food preservative attributes of maillard reaction products of shrimp shell chitosan. Current Topics in Nutraceutical Research, 20(1), 64-69. http://dx.doi.org/10.37290/ctnr2641-452X.20:64-69
  » http://dx.doi.org/10.37290/ctnr2641-452X.20:64-69
• Wu, B., Chai, X., He, A., Huang, Z., Chen, S., Rao, P., Ke, L., & Xiang, L. (2021). Inhibition of acrylamide toxicity in vivo by arginine-glucose maillard reaction products. Food and Chemical Toxicology, 154, 112315. http://dx.doi.org/10.1016/j.fct.2021.112315 PMid:34082049.
  » http://dx.doi.org/10.1016/j.fct.2021.112315
• Wu, L., Weng, M., Zheng, H., Lai, P., Tang, B., Chen, J., & Li, Y. (2020). Hypoglycemic effect of okra aqueous extract on streptozotocin-induced diabetic rats. Food Science and Technology, 40(4), 972-978. http://dx.doi.org/10.1590/fst.28619
  » http://dx.doi.org/10.1590/fst.28619
• Xia, B., Ni, Z. J., Hu, L. T., Elam, E., Thakur, K., Zhang, J. G., & Wei, Z. J. (2021). Development of meat flavors in peony seed derived Maillard reaction products with the addition of chicken fat prepared under different conditions. Food Chemistry, 363, 130276. http://dx.doi.org/10.1016/j.foodchem.2021.130276 PMid:34144426.
  » http://dx.doi.org/10.1016/j.foodchem.2021.130276
• Xia, Z. W., Zhang, J. G., Ni, Z. J., Zhang, F., Thakur, K., Hu, F., & Wei, Z. J. (2022). Functional and emulsification characteristics of phospholipids and derived o/w emulsions from peony seed meal. Food Chemistry, 389, 133112. http://dx.doi.org/10.1016/j.foodchem.2022.133112 PMid:35504077.
  » http://dx.doi.org/10.1016/j.foodchem.2022.133112
• Xiao, Q., Woo, W. M., Hu, J., Xiong, H., & Zhao, Q. (2021). The role of heating time on the characteristics, functional properties and antioxidant activity of enzyme-hydrolyzed rice proteins-glucose Maillard reaction products. Food Bioscience, 43, 101225. http://dx.doi.org/10.1016/j.fbio.2021.101225
  » http://dx.doi.org/10.1016/j.fbio.2021.101225
• Zhang, F., Qu, J., Thakur, K., Zhang, J. G., Mocan, A., & Wei, Z. J. (2019). Purification and identification of an antioxidative peptide from peony (Paeonia suffruticosa Andr.) seed dreg. Food Chemistry, 285, 266-274. http://dx.doi.org/10.1016/j.foodchem.2019.01.168 PMid:30797344.
  » http://dx.doi.org/10.1016/j.foodchem.2019.01.168
• Zhang, F., Shi, J. J., Thakur, K., Hu, F., Zhang, J. G., & Wei, Z. J. (2017). Anti-cancerous potential of polysaccharide fractions extracted from peony seed dreg on various human cancer cell lines via cell cycle arrest and apoptosis. Frontiers in Pharmacology, 8, 102. http://dx.doi.org/10.3389/fphar.2017.00102 PMid:28316571.
  » http://dx.doi.org/10.3389/fphar.2017.00102
• Zhang, X. X., Ni, Z. J., Zhang, F., Thakur, K., Zhang, J. G., Khan, M. R., Busquets, R., & Wei, Z. J. (2022). Physicochemical and antioxidant properties of Lycium barbarum seed dreg polysaccharides prepared by continuous extraction. Food Chemistry: X, 14, 100282. http://dx.doi.org/10.1016/j.fochx.2022.100282 PMid:35299725.
  » http://dx.doi.org/10.1016/j.fochx.2022.100282
• Zheng, A. R., Wei, C. K., Ni, Z. J., Thakur, K., Zhang, J. G., & Wei, Z. J. (2022). Gut modulatory effects of flaxseed derived Maillard reaction products in Sprague-Dawley rats during sub-chronic toxicity. Food and Chemical Toxicology, 165, 113115. http://dx.doi.org/10.1016/j.fct.2022.113115 PMid:35537647.
  » http://dx.doi.org/10.1016/j.fct.2022.113115

Publication Dates

• Publication in this collection
  21 Nov 2022
• Date of issue
  2023

History

• Received
  25 Aug 2022
• Accepted
  23 Oct 2022