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2023 Volume 3
Article Contents
Abstract
INTRODUCTION
MATERIALS AND METHODS
Plant culture and treatments
Plant growth and visual quality
Water use and substrate moisture
Gas exchange measurements
Strawberry fruit harvest
Experimental design and data analyses
RESULTS
Plant vegetative growth
Timing of fruit harvest
Yield
Fruit quality
Water use and substrate moisture
Gas exchange
DISCUSSION
CONCLUSIONS
ACKNOWLEDGMENTS
Conflict of interest
Supplementary information
Rights and permissions
References
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Effect of natural plant extracts on the quality of meat products: a meta-analysis

  • State key Laboratory of Meat Quality Control and Cultured Meat Development,Ministry of Science and Technology; Key Laboratory of Meat Processing, Ministry of Agriculture and Rural Affairs; Jiangsu Provincial Collaborative Innovative Center of Meat Production, Processing and Quality Control; College of Food Science and Technology, Nanjing Agricultural University, Nanjing, 210095, PR China

More Information
  • Natural plant extracts (NPE) from some organs of plants are rich in bioactive substances. They have special nutritional characteristics with strong antioxidant and antimicrobial activities. The potential of NPEs to maintain and improve the quality of meat products has attracted attention due to concerns about the safety hazards of synthetic food additives. This paper extensively reviewed the application of NPE in meat processing, and systematically analyzed the comprehensive effects of different NPE using meta-analysis. Fourty-eight articles from 23 countries were studied with standard mean deviation (SMD) using random effect model, and 28 indexes were isolated. Results showed that NPE can reduce the pH value of meat products, improve antioxidant capacity, reduce the degree of oxidation and inhibit microbial growth. In addition, it was found that NPE had a significant impact on the quality of meat products. This meta-analysis provides quantitative evidence to explain how NPE affects meat quality, and helps to better understand the role of NPE in meat processing.

  • INTRODUCTION

    The United States is the world's second largest producer of strawberries (Fragaria × ananassa Duch.)[1]. In 2017, the U.S. produced 1.6 billion pounds of strawberries, with an industry value of near $3.5 billion[2,3]. Strawberry is one of the most consumed fruits in the U.S., with per capita consumption of 7.12 lbs in 2018[4−6]. Strawberries are rich in basic nutritional components including sugars, mineral nutrients, and vitamins, and bioactive compounds that are known to have antioxidant capacity, scavenge free radicals, and introduce health benefits such as slowing down aging, preventing cardiovascular diseases, inflammation, and certain types of cancers[7, 8].

    Cultivated strawberry plants are classified into three types of cultivars based on their flowering response to photoperiod and temperature: June-bearing, everbearing, or day-neutral[9]. June-bearing strawberries initiate flowering in response to a short photoperiod of 14 h or less, or low temperatures below 15 °C, and typically produce one flush of fruit in spring[9,10]. Ever-bearing cultivars initiate flower buds with days of greater than 12 h, resulting in a fall harvest or two crops in one year[11]. Day-neutral strawberry plants can produce crowns and flower buds whenever the temperature is within a favorable range of 4 to 29 °C regardless of the day length[12]. This ability allows for potential year-round fruit harvest in areas where summer or fall temperatures stay in this range or where high tunnels or other protected cultivation methods can produce the favorable conditions[12,13]. Commercial production of strawberries uses mostly June-bearing cultivars or a combination of June-bearing and day-neutral cultivars, with ever-bearing cultivars rarely grown outside of home gardens. There has been increasing interest in using day-neutral cultivars for extended harvest season[3].

    The leading states for strawberry production in the U.S. are California and Florida, producing approximately 91% and 8% of the nation's strawberry crop[14]. Commercial strawberry production in the U.S. uses primarily an annual hill production system featuring plasticulture and raised beds. Strawberry production in all other states is mainly small-scale and aims for local market outlets[3]. Growers are seeking ways to improve competitiveness, including using protected culture with greenhouses, high and low tunnels, or soilless culture to achieve season extension, reduce pest pressure, and improve fruit yield and quality[3,15]. Besides using an annual hill system, strawberry plants can also be grown as hanging baskets and marketed to home gardeners for both the decorative and edible attributes. Best management practices including fertilization and irrigation of containerized strawberry plants using soilless substrate largely remain unknown and merits investigation.

    There has been strong consumer demand for locally, sustainably, or organically grown fruits and vegetables with increasing consumer health consciousness[16−18]. Organically grown strawberry fruit were found to have lower pesticide residues, better fruit quality, and greater antioxidant activity[17]. By comparison, Hargreaves et al.[19] found no significant differences in yield, total soluble solids content or antioxidant capacity in organically versus conventionally grown strawberries. Similar flavanol and phenolic acid contents were found in berries grown organically and conventionally by Häkkinen & Törrönen[20]. Fertilization management is an important aspect of growing strawberry plants in an alternative production system. There lacks information regarding effects of certain organic growing practices like fertilizer type on plant growth, fruit yield and quality of strawberry plants.

    An efficient irrigation program should be economically sound, and reduce excessive nutrient leaching to ground water. Deficit irrigation increased concentrations of taste- and health-related compounds including sugars and acids in strawberry fruit, but resulted in smaller fruit size[21]. Fare et al.[22] reported that splitting the irrigation volume into separate times reduced water runoff and nitrate leached from the substrate in container grown holly (Ilex crenata Thunb. 'Compacta'). Scagel et al.[23,24] reported that increased irrigation frequency decreased water stress, increased nitrogen use efficiency, and had varying effects on mineral nutrient uptake of three Rhododendron species. Irrigation applied in split intervals increased plant growth, carbon dioxide (CO2) assimilation, stomatal conductance, and water use efficiency of Cotoneaster dammeri 'Skogholm' compared with plants receiving water once in the morning[25]. Plant species varied in their response to altered irrigation frequency. Li et al.[26] found that increasing irrigation frequency from once to twice per day decreased plant growth index, root dry weight, length, surface area, and flower number per plant in Rhododendron sp. 'Chiffon'. Two irrigations per day increased plant size, substrate moisture, and N concentration in Hydrangea macrophylla 'Merritt Supreme' compared to one irrigation[27]. The effect of altering irrigation frequency on plant growth and fruit production of strawberry cultivars remains unclear.

    We hypothesized that fertilizer type and irrigation frequency may affect strawberry plant performance independently or interactively when grown in containers with soilless substrate. The objective of this study was to investigate plant vegetative growth, gas exchanges, fruit yield and quality of ten containerized strawberry cultivars, including seven June-bearing and three day-neutral, as affected by fertilizer type and irrigation frequency in USDA hardiness zone 8a.

    MATERIALS AND METHODS

    Plant culture and treatments

    Seven June-bearing cultivars 'Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour', and three day-neutral cultivars 'Evie 2', 'San Andreas', and 'Seascape' were evaluated in this study. Bare root liners of the ten selected cultivars were purchased from a commercial nursery (Nourse Farms, Whately, MA, U.S.) and transplanted into 2-gallon plastic containers (C900, top diameter 24.1 cm, height 23.2 cm, volume 7.33 L; Nursery Supplies® Inc., Chambersburg, PA, U.S.) on 28 Feb. 2018. Pine bark : peat moss : perlite in a volume ratio of 4:3:1 was used as growing substrate. The substrate was incorporated with 0.89 kg·m−3 micronutrient (Micromax®; ICL Specialty Fertilizers, Summerville, SC, U.S.) and 2.97 kg·m−3 lime (Soil Doctor Pelletized Lawn Lime; Oldcastle, Atlanta, GA, U.S.). Each containerized plant was fertilized with 60 g granular organic fertilizer 5N-1.3P-3.3K (5-3-4; McGeary Organics, Lancaster, PA, U.S.) or 20 g conventional controlled-release fertilizer 15N-2P-10K (Osmocote® 15-9-12 5−6 months; Scotts Miracle-Grow Co., Marysville, OH, U.S.). All strawberry plants were maintained outdoors in full sun at the R. R. Foil Plant Science Research Center of Mississippi State University in Starkville, MS, U.S. (lat. 33.45° N, long. 88.79° W; USDA hardiness zone 8a). Strawberry plants were drip irrigated at a flow rate of half gallon per hour with the same total daily irrigation volume through two irrigation frequencies: once per day at 0800HR or twice per day at 0800HR (half volume) and 1430HR (half volume). Plants were irrigated to replace daily water loss plus 10% to 15% leaching fraction. Irrigation volume was determined by randomly selecting ten plants and measuring their daily water use approximately once per month.

    Local outdoor air temperature in Starkville were obtained from the website of the USDA-Natural Resources Conservation Service[28]. Growing degree days (GDDs) were calculated daily by [(Daily maximum temperature + Daily minimum temperature)/2 – Base temperature]. Cumulative GDDs between certain time periods were estimated by summing daily GDDs. The base temperature used for strawberry was 3 °C[29].

    Plant growth and visual quality

    Plant height and widths (width 1, the widest point of canopy; width 2, perpendicular width of width 1) of each plant were measured on 22 June 2018. Plant growth index (PGI) was calculated as the average of the plant height and two widths to estimate plant size. On 20 June, relative leaf chlorophyll content was estimated by SPAD readings. Leaf SPAD readings were measured from the terminal leaflet of three fully expanded new leaves using a chlorophyll meter (SPAD 502 Plus; Konica Minolta, Inc., Osaka Japan). An average of the three readings were calculated to represent relative leaf chlorophyll content of an individual plant. Plant visual quality was evaluated by a five-point scale, where 1 = poor quality with severe leaf damage over 70%; 2 = leaf damage of 50% to 70%, 3 = moderate quality with 20% to 50% leaf damage; 4 = good quality with minor leaf damage of less than 20%; 5 = excellent quality without any leaf damage. A dead plant was rated 0 for the visual score.

    One plant from each treatment combination was destructively harvested with three replications. For each individual plant, shoots were separated from roots, and roots were then cleaned free of substrate. Roots and shoots samples were oven dried at 60 °C to constant weight. The number of crowns from each harvested plant and the dry weight of each sample were recorded.

    Water use and substrate moisture

    Daily water use (DWU) was determined in plants irrigated once per day using a gravimetric method by subtracting pot weight (plant included) 24 h after irrigation from pot weight at container capacity (about half an hour after irrigation). Daily water use was measured twice on 19 June and 27 June, respectively. Substrate moisture at 6-cm depth was measured using a soil moisture sensor (ML2x; Delta-T Devices, Cambridge, England) with two readings collected from each container. The moisture sensor was connected to a soil sensor reader (HH2; Delta-T Devices) for instant moisture readings. Substrate moisture was measured on 27 June before scheduled daily irrigation in the morning.

    Gas exchange measurements

    To evaluate physiological activities of plants affected by fertilizer type and irrigation frequency, leaf net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of strawberry plants were measured between 1100HR and 1500HR on 27 June and 28 June using a portable photosynthesis system (LI-6400XT; LI-COR, Lincoln, NE, U.S.). Three plants were randomly selected from three different blocks for gas exchange measurements for each treatment combination. One recent fully expanded leaf, not shaded by other leaves, was selected for the measurement. The selected leaf was enclosed into a 2-cm2 leaf chamber with a fluorometer (6400-40; LI-COR) as the light source. A reference CO2 concentration of 400 µmol·mol−1 and photosynthetically active radiation (PAR) of 1500 µmol·m−2·s−1 were maintained inside the leaf chamber during gas exchange measurements. Block temperature was maintained according to outdoor air temperature on the measurement date.

    Strawberry fruit harvest

    Strawberry fruit was harvested once per week. The date of first fruit harvest was recorded for each plant. Strawberries were culled for misshaped, disease- or insect-damaged fruits. Fruit yield and the number of fruit at each harvest were recorded. Yield from each harvest was summed up for a season total. Soluble solids content of strawberry fruit from each plant were measured using a digital refractometer (PR-32α; Atago U.S.A., Inc., Bellevue, WA, U.S.). Fruit firmness was measured with a fruit hardness tester (FR-5120; Lutron Electronic Enterprise CO., LTD, Taipei, Taiwan, ROC). One marketable fruit was used to measure soluble solids content and fruit firmness from each plant, respectively.

    Experimental design and data analyses

    The experiment was designed in a factorial randomized complete block design with five replications. Three mains factors are strawberry cultivar (10), fertilizer type (2), and irrigation frequency (2), resulting in 40 treatment combinations. Each replication contained two single-plant subsamples. Due to the large number of treatment combinations, data of plant dry weights and gas exchange were measured with three replications, where the three plants were randomly selected from different blocks. Data were analyzed by analysis of variance (ANOVA) using the PROC GLIMMIX procedure in SAS (version 9.4; SAS Institute, Cary, NC, U.S.). Where indicated by ANOVA, means were separated using Tukey's Honest Significant Difference (HSD) test at P ≤ 0.05.

    RESULTS

    Plant vegetative growth

    Plant vegetative growth variables including plant growth index (PGI) (P < 0.0001), leaf relative chlorophyll content measured as leaf SPAD (P < 0.0001), number of crowns per plant (P = 0.040), visual score (P < 0.0001), and root dry weight (P < 0.0001) varied among cultivars (Table 1), with PGI (P = 0.0003), SPAD (P < 0.0001), and plant visual score (P < 0.0001) also affected by the main effect of fertilizer type without interactions (Table 2).

    Table 1.  Vegetative growth of seven June-bearing ('Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour') and three day-neutral ('Evie 2', 'San Andreas', and 'Seascape') strawberry cultivars grown in Starkville, Mississippi in 2018.
    CultivarPGI1, 2 (cm)SPADNumber of crowns
    (per plant)    		Visual score
    (1-5)3    		Shoot dry wt.
    (g per plant)    		Root dry wt.
    (g per plant)
    Allstar41.2 ab31.9 def4.1 ab3.0 bcde71.413.5 abcd
    Chandler37.4 c30.1 f4.3 ab2.9 bcde65.810.1 d
    Darselect39.5 abc31.0 ef3.8 ab2.6 e65.114.6 abc
    Earlyglow38.3 bc32.9 de4.0 ab2.8 cde63.711.9 cd
    Evie 237.0 c36.3 ab3.8 ab3.0 bcde58.89.6 d
    Honeoye40.9 ab35.3 bc4.2 ab3.8 a81.516.5 ab
    Jewel41.6 a30.4 f3.5 b2.7 de67.512.9 abcd
    L'Amour38.5 abc33.5 cd4.4 ab3.2 bc75.917.3 a
    San Andreas37.6 c37.5 a4.2 ab2.9 cde64.412.3 bcd
    Seascape38.7 abc35.7 abc5.2 a3.3 b63.211.5 cd
    P-value<.0001<.00010.040<.00010.13<.0001
    1 Plant growth index (PGI) = [plant height + widest width 1 + width 2 (width at the perpendicular direction to width 1]/3.
    2 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
    3 Plant visual quality was evaluated by a five-point scale, where 1 = poor quality with severe leaf damage over 70%; 2 = leaf damage of 50% to 70%; 3 = moderate quality with 20% to 50% leaf damage; 4 = good quality with minor leaf damage of less than 20%; 5 = excellent quality without any leaf damage. A dead plant was rated 0 for the visual score.
     | Show Table
    DownLoad: CSV
    Table 2.  Effect of fertilizer type on plant growth index (PGI), leaf SPAD, visual score, yield in May, daily water use, substrate moisture, and net photosynthetic rate (Pn) of container-grown strawberries grown in Starkville, Mississippi.
    Fertilizer1PGI2 (cm)SPADVisual score
    (1−5)    		Yield in May
    (g per plant)    		Daily water use (L per day)Substrate moisture (%)Pn
    (µmol·m−2·s−1)
    19 June26 June
    Organic38.3 b32.3 b2.8 b57.9 b0.54 b0.62 b27.2 a10.7 b
    Conventional39.9 a34.6 a3.2 a67.9 a0.65 a0.73 a24.6 b12.0 a
    P-value0.0003< 0.0001< 0.00010.044< 0.00010.0003< 0.00010.0059
    1 Strawberry plants were fertilized with a conventional controlled release fertilizer or an organic fertilizer at comparable rates.
    2 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
     | Show Table
    DownLoad: CSV

    'Allstar', 'Jewel', and 'Honeoye' had comparable highest PGIs ranging from 40.9 to 41.6 cm, higher than 'Chandler', 'Evie 2', or 'San Andreas' with the lowest PGIs of 37.0 to 37.6 cm (Table 1). The other four cultivars 'Darselect', 'Earlyglow', 'L'Amour', and 'Seascape' had similar PGIs of 38.3 to 39.5 cm. The three day-neutral cultivars 'Evie 2', 'San Andreas', and 'Seascape' had the comparable highest leaf SPAD ranging from 35.7 to 37.5, with 'Allstar', 'Chandler', 'Darselect', and 'Jewel' having the lowest SPAD ranging from 30.4 to 31.9. Ten tested cultivars generally produced similar number of crowns per plant averaged 3.5 to 5.2 per plant. 'Honeoye' had the highest visual scores averaged 3.8 with minor leaf diseases. 'L'Amour' and 'Seascape' had intermediate visual scores of 3.2 and 3.3, respectively. 'Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Evie 2', 'Jewel', and 'San Andreas' had comparable visual scores ranging from 2.6 to 3.0 out of 5.

    Shoot dry weight ranged from 58.8 to 81.5 g per plant, similar among all tested cultivars. 'Allstar', 'Darselect', 'Honeoye', 'Jewel' and 'L'Amour' had comparable root dry weights of 12.9 to 17.3 g per plant, with 'Chanlder', 'Earlyglow', 'Evie 2', 'San Andreas', and 'Seascape' having comparable root dry weights of 9.6 to 12.3 g per plant (Table 1).

    When affected by the main effect of fertilizer type, the conventional fertilizer increased PGI, SPAD, and visual score by 4.2%, 7.1%, and 14.3% compared to the organic fertilizer, respectively (Table 2). Fertilizer type did not affect other vegetative growth variables including number of crowns, shoot, and root dry weight.

    Affected by the interaction between fertilizer type and irrigation frequency (P = 0.049), strawberry plants fertilized with the conventional fertilizer and irrigated twice per day produced higher shoot dry weight of 81.8 g per plant than plants fertilized with organic fertilizer and irrigated twice per day, or plants irrigated once per day fertilized with the conventional or the organic fertilizer (Table 3). Irrigation frequency did not affect plant vegetative growth variables including PGI, SPAD, number of crowns, visual score, and root dry weight.

    Table 3.  Shoot dry weight affected by the interaction between irrigation frequency and fertilizer type and substrate moisture affected by the main effect of irrigation frequency of container-grown strawberries.
    Irrigation frequency1FertilizerShoot dry wt
    (g per plant)2    		Substrate moisture (%)
    OnceOrganic60.3 b21.21 b
    Conventional68.1 b
    TwiceOrganic60.7 b30.55 a
    Conventional81.8 a
    P-value0.049< 0.0001
    1 Seven June-bearing ('Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour') and three day-neutral ('Evie 2', 'San Andreas', and 'Seascape') strawberry cultivars were grown in 2-gal containers irrigated once or twice per day with the same total irrigation volume, and fertilized with a conventional controlled release fertilizer or an organic fertilizer at comparable rates.
    2 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
     | Show Table
    DownLoad: CSV

    Timing of fruit harvest

    When transplanted on 28 Feb, 2018, fruit harvest of tested strawberry cultivars started 49.4 days after transplanting (DAT) in 'Honeoye' to 65.7 DAT in 'Chandler' in the 2018 growing season (Table 4), with correspondent cumulative GDDs of 536 and 783 (Fig. 1a), respectively. The day-neutral cultivar 'Evie 2' was the second latest-fruiting cultivar with the first harvest being 60.9 DAT. Local average daily air temperature was in between 12.8 to 23.6 °C during the first fruit harvest of tested cultivars (Fig. 1b). Fertilizer type or irrigation frequency did not affect the fruit production timing of any tested cultivar. The first fruit harvest was on 19 Apr and the last fruit harvest was on 13 June 2018 with a total of ten harvests.

    Table 4.  Fruiting characteristics including first harvest date, number of fruit per plant, berry size, soluble solids content, and fruit firmness of seven June-bearing ('Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour') and three day-neutral ('Evie 2', 'San Andreas', and 'Seascape') strawberry cultivars grown in Starkville, Mississippi in 2018.
    CultivarFirst harvest date1 (DAT)Number
    of fruit
    (per plant)    		Berry size (g per berry)Soluble
    solids content
    (°Brix)    		Fruit firmness (N)
    Allstar58.6 bc6.9 c8.8 e10.5 a1.89 abc
    Chandler65.7 a4.6 cd11.7 d10.4 a1.32 e
    Darselect54.0 def4.7 cd14.0 bc11.5 a1.48 de
    Earlyglow51.3 fg3.9 cd9.3 e11.5 a1.49 de
    Evie 260.9 b16.5 a14.8 b8.4 c1.53 de
    Honeoye49.4 g4.4 cd10.1 de10.4 ab1.60 cde
    Jewel58.4 bcd6.0 cd10.2 de10.3 ab1.73 bcd
    L'Amour57.3 bcde3.1 d12.2 cd11.1 a2.00 ab
    San Andreas53.7 efg5.0 cd17.8 a8.7 bc2.17 a
    Seascape54.4 cdef12.3 b14.2 bc10.9 a1.65 cd
    P-value< 0.0001< 0.0001< 0.0001< 0.0001< 0.0001
    1 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
     | Show Table
    DownLoad: CSV
    Figure 1.  (a) Cumulative growing degree days (GDDs) and (b) outdoor daily air temperatures from 1 Mar to 15 June 2018 in Starkville, Mississippi, U.S. GDDs = (Tdaily max + Tdaily min)/2– Tbase. Tbase = 3 °C for strawberries. GDDs was calculated on a daily basis, and cumulative GDDs during certain time periods were estimated by summing up daily GDDs; Local outdoor air temperature data was obtained from the USDA Natural Resources Conservation Service website.
    DownLoad: Full-Size Img PowerPoint

    Yield

    In April, five cultivars 'Darselect', 'Earlyglow', 'Honeoye', 'San Andreas', and 'Seascape' produced similar yield ranging from 17.9 to 24.4 g fruit per plant, higher than 'Allstar', 'Chandler', or 'Jewel' (Table 5). In May, the two day-neutral cultivars 'Evie 2' and 'Seascape' produced the highest and second highest yield of 170.6 and 135.7 g fruit per plant, with 'Chandler', 'Darselect','Earlyglow', 'Honeoye', and 'L'Amour' producing the lowest yield of 16.6 and 50.2 g fruit per plant. The cultivars 'Allstar', 'Jewel', and 'San Andreas' produced similar intermediate yields of 52.0 to 61.1 g fruit per plant in May. The conventional fertilizer increased yield in May by 17.3% compared with the organic fertilizer (Table 2). In June, 'Evie 2' produced the highest yield of 56.8 g fruit per plant, with all other cultivars producing similar yield below 10 g fruit per plant. 'Darselect' and 'Jewel' did not produce any fruit in June. Except for the two early ripening cultivars 'Earlyglow' and 'Honeoye' producing peak harvest in April, the other eight cultivars produced peak harvest in May, which was 68% to 92% of total yield.

    Table 5.  Monthly and total yield of seven June-bearing ('Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour') and three day-neutral ('Evie 2', 'San Andreas', and 'Seascape') strawberry cultivars grown in Starkville, Mississippi in 2018.
    CultivarStrawberry yield in 2018 (g per plant)1
    AprilMayJuneTotal
    Allstar5.0 c52.0 cd1.5 b58.4 cd
    Chandler3.5 c50.2 cde1.9 b55.7 cd
    Darselect18.6 ab47.3 cde0 b65.8 cd
    Earlyglow17.9 ab16.7 e0.6 b35.2 d
    Evie 28.9 bc170.6 a56.8 a236.3 a
    Honeoye24.4 a16.6 e0.5 b41.5 d
    Jewel4.6 c53.8 cd0 b58.5 cd
    L’Amour10.0 bc25.3 de0.5 b35.8 d
    San Andreas23.4 a61.1 c5.3 b89.8 c
    Seascape22.5 a135.7 b9.4 b167.6 b
    P-value< 0.0001< 0.0001< 0.0001< 0.0001
    1 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
     | Show Table
    DownLoad: CSV

    For total yield, the two day-neutral cultivars 'Evie 2' and 'Seascape' ranked first and second producing yield of 236.3 and 167.6 g per plant, respectively (Table 5). 'Evie 2' and 'Seascape' also produced the highest and the second highest fruit number of 16.5 and 12.3 per plant among all tested cultivars (Table 4). The seven June-bearing cultivars Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour' generally produced similar total yield and number of fruit per plant ranging from 35.2 to 65.8 g per plant and 3.1 to 6.9 fruits per plant, respectively.

    Fruit quality

    The day-neutral cultivar 'San Andreas' produced the largest berry size averaged 17.8 g per berry, higher than 'Darselect', 'Evie 2', or 'Seascape' producing berry size of 14.0 to 14.8 g per berry. 'Allstar', 'Earlyglow', 'Honeoye', and 'Jewel' produced comparable lowest berry sizes of 8.8 to 10.1 g per berry (Table 4).

    'Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', 'L'Amour', and 'Seascape' had comparable soluble solids content ranging from 10.3 to 11.1 °Brix, with 'Evie 2' and 'San Andreas' producing fruit with the lowest soluble solids content of 8.4 and 8.7 °Brix, respectively. 'San Andreas', 'L'Amour', and 'Allstar' produced the firmest strawberry fruit of 1.89 to 2.17 N, higher than 'Chandler', 'Darselect', 'Earlyglow', or 'Evie 2' producing the least firm fruit of 1.32 to 1.53 N (Table 4).

    Fruiting characteristics including time of fruit harvest, strawberry yield, berry size, number of fruit per plant, fruit soluble solids content and firmness were not affected by fertilizer type or irrigation frequency.

    Water use and substrate moisture

    Daily water use was significantly different among cultivars on June 19 but similar among cultivars on June 26 ranging from 0.57 to 0.78 L per day (Table 6). On June 19, eight cultivars had similar daily water use ranging from 0.54 L ('San Andreas') to 0.67 L ('Allstar'), with 'L'Amour' and 'Seascape' having the highest and lowest daily water use of 0.71 and 0.53 L per day, respectively. Substrate moisture at 6-cm depth was generally similar among cultivars ranging from 23.1% in 'Darselect' to 28.0% in 'Allstar'. Organic fertilizer resulted in increased substrate moisture by 10.6% compared to the conventional fertilizer (Table 2). Two irrigations per day also increased substrate moisture by 44.0% compared to one irrigation per day (Table 3).

    Table 6.  Daily water use measured on two dates and substrate moisture measured on 27 June 2018 of seven June-bearing ('Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour') and three day-neutral ('Evie 2', 'San Andreas', and 'Seascape') strawberry cultivars grown in containers in Starkville, Mississippi.
    CultivarDaily water use
    (L per day)1    		Substrate moisture (%)
    19 June26 June27 June
    Allstar0.67 ab0.7828.0 a
    Chandler0.58 abc0.7325.0 ab
    Darselect0.60 abc0.6623.1 b
    Earlyglow0.58 abc0.6726.8 ab
    Evie 20.53 bc0.6526.9 ab
    Honeoye0.65 abc0.7227.5 a
    Jewel0.57 abc0.6227.3 ab
    L'Amour0.71 a0.7223.8 ab
    San Andreas0.54 bc0.6125.5 ab
    Seascape0.53 c0.5725.0 ab
    P-value0.00040.0740.0037
    1 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
     | Show Table
    DownLoad: CSV

    Gas exchange

    Net photosynthetic rate (Pn) was the highest in 'L'Amour' of 14.4 µmol·m−2·s−1, similar to 'San Andreas' or 'Seascape', but higher than the other seven cultivars ranging from 9.7 to 11.2 µmol·m−2·s−1 (Table 7). Stomatal conductance (gs) was similar among all cultivars ranging from 0.072 mol·m−2·s−1 in 'Darselect' to 0.14 mol·m−2·s−1 in 'L'Amour' or 'San Andreas'. The conventional fertilizer increased Pn by 12.1% compared with the organic fertilizer (Table 2). 'San Andreas' had the highest transpiration rate (E) of 6.65 mmol·m−2·s−1, similar to 'Allstar', 'Chandler', 'Earlyglow', 'Evie 2', 'L'Amour', and 'Seascape', but higher than 'Darselect', 'Honeoye', or 'Jewel' with E ranging from 3.16 mmol·m−2·s−1 to 3.98 mmol·m−2·s−1. Gas exchange measurements including Pn, gs, and E were not affected by irrigation frequency.

    Table 7.  Gas exchange measurements including net photosynthetic rate (Pn), stomatal conductance (gs), and transpiration rate (E) of seven June-bearing ('Allstar', 'Chandler', 'Darselect', 'Earlyglow', 'Honeoye', 'Jewel', and 'L'Amour') and three day-neutral ('Evie 2', 'San Andreas', and 'Seascape') strawberry cultivars grown in containers in Starkville, Mississippi.
    CultivarPn
    (µmol·m−2·s−1)1    		gs
    (mol·m−2·s−1)    		E
    (mmol·m−2·s−1)
    Allstar9.8 d0.10 a4.37 ab
    Chandler11.2 bcd0.12 a4.73 ab
    Darselect10.3 bcd0.072 a3.16 b
    Earlyglow10.7 bcd0.11 a5.57 ab
    Evie 211.2 bcd0.11 a4.61 ab
    Honeoye9.7 d0.089 a3.74 b
    Jewel9.9 cd0.083 a3.98 b
    L'Amour14.4 a0.14 a5.53 ab
    San Andreas13.4 ab0.14 a6.65 a
    Seascape13.0 abc0.12 a5.09 ab
    P-value< 0.00010.0260.0006
    1 Different lower-case letters within a column suggest significant difference indicated by Tukey's HSD test at P ≤ 0.05.
     | Show Table
    DownLoad: CSV

    DISCUSSION

    The ten cultivars tested in this study generally showed satisfactory vegetative growth in terms of PGI, leaf SPAD, shoot and root dry weights, with five cultivars 'Allstar', 'Evie 2', 'Honeoye', 'L'Amour', and 'Seascape' having visual scores of 3 or above. The earliest ripening cultivars in this study were June-bearing 'Honeoye' and 'Earlyglow', producing ripe fruit 49.4 and 51.3 DAT, with cumulative GDDs of 536 and 556, respectively. The June-bearing 'Chandler' were the latest ripening cultivar, producing ripe fruit 65.7 DAT, with 783 GDDs.

    Strawberry harvest season in midsouthern states including Arkansas, Louisiana, Mississippi, Oklahoma, and Texas occurs from February to late May or early June, with peak production typically in April to May[3]. The first fruit harvest was in late April in this study, consistent with local strawberry harvest timing in an open field production system[30]. In this current study, the two earliest ripening June-bearing cultivars 'Earlyglow' and 'Honeoye' produced peak yield in April, all other tested cultivars produced peak yield in May. They may potentially be used in fall planting or in protected culture like high tunnels for off-season strawberry production.

    The ten cultivars generally produced lower yield and smaller fruit than reported ranges[13,31,32]. A possible reason might be the time of transplanting in spring using bare root liners. Local open field or high tunnel strawberry production systems in Mississippi typically use fall planting with plugs, which allows plants to establish vegetatively before flower and fruit production in spring[10]. Fall planted strawberry cultivars required 1,249.1 to 1,374.3 GDDs from transplanting to first ripe fruit in a high tunnel production system in the same location (unpublished data), and resulted in higher yield than spring planting. However, containerized strawberry plants can be marketed as hanging baskets and serve as ornamental plants, where overall visual quality can be valued as much as yield. The two day-neutral cultivars 'Evie 2' and 'Seascape' produced the highest and second highest total yield of all tested cultivars, higher than all June-bearing cultivars. 'Evie 2' also produced yield of 56.8 g per plant in June when all June-bearing cultivars produce less than 2 g berry per plant, showing potential for season extension into months with warmer temperatures. Local daily average air temperatures during the first two weeks of June were between 22.2 and 29.2 °C, with daily maximum air temperature ranging from 30 to 33.9 °C. High temperatures are the major limiting factor of using day-neutral cultivars to extend harvest season in Mississippi, requiring heat tolerant cultivars.

    Compared with the organic fertilizer, the conventional fertilizer increased plant growth index, leaf SPAD, visual score, yield in May, daily water use, and net photosynthetic rate regardless of strawberry cultivars in this current study. This agreed with our previous study using the same two fertilizer types but in container grown southern highbush blueberry (Vaccinium corymbosum L.) cultivars, where the conventional fertilizer increased blueberry yield in 2016[33]. The conventional fertilizer also tended to advance blueberry ripening for approximately one week compared to the organic fertilizer[33], whereas the same two fertilizer types resulted in similar strawberry harvest date in this study. Nutrients in organic fertilizers are in organic forms and must go through mineralization for nutrients to be available to plant uptake[34,35], resulting in a slow release of nutrient. Gaskell et al.[36] reported it to be unpredictable to synchronize nitrogen (N) demand for establishing strawberry plants with release of N from various organic nutrient sources compared to conventional N sources. Large quantity and continuous application of organic fertilizers are required to achieve certain fertility and soil organic matter level for optimal yield in organic farming[37,38]. The two fertilizer types are applied in proportion to provide the same total amount of nutrients. Their effects on plant growth and fruit production are subject to the rate of nutrient release and the total amount of fertilizer available to plants. Their different effects on plant growth and crop yield may become more significant over time. Therefore, organic fertilization in container grown strawberry plant may require supplement of liquid fertilizer for its fast-acting effects.

    The effect of irrigation frequency varied among plant species with different water requirements or soilless growing substrates with varying physical and chemical properties[26,27,39]. Increasing irrigation frequency can improve growth and plant nutrient uptake by continually resupplying nutrient solution to the depletion zone around the roots. Silber et al.[40] found that higher irrigation frequency led to more vegetative growth and higher concentrations of less mobile nutrients in iceberg lettuce (Lactuca sativa L.). Rhododendron species with low water requirement benefited from one irrigation per day over two irrigations: Encore azalea 'Chiffon' produced greater PGI, root biomass, and improved mineral nutrient uptake in roots under one irrigation per day[26]. Biomass production of Hydrangea macrophylla 'Merritt's Supreme' was not affected by irrigation frequency[27]. In this current study, two irrigations per day increased substrate moisture, which may affect nutrient availability in the substrate and merits further investigation. Two irrigations per day also increased plant shoot dry weight when fertilized with the conventional fertilizer, but did not affect plant size, visual quality, gas exchange, strawberry yield, or fruit quality of the ten tested strawberry cultivars. This was in agreement with Silber et al.[40] that higher irrigation frequency leads to increased vegetative growth, which can potentially be used in strawberry plant propagation to increase the number of runners per plant.

    Soilless culture of strawberries is used in limited areas due to high production cost and high demands for management expertise. It is mostly used in greenhouses or high tunnels, where off-season strawberry production and high market demand can justify the production cost[15]. Planting strawberry plants in containers alleviates extensive soil management and the need for soil fumigation, and may potentially increase production sustainability[41]. This study provides reference in fertilization and irrigation management in containers with soilless substrate. There might be potential of using container-grown strawberry plants in nursery production for propagation purposes or to be used in small-scale production for certain niche markets, which warrants further investigation.

    CONCLUSIONS

    Of the ten tested cultivars, the two day-neutral cultivars 'Evie 2' and 'Seascape' produced higher total and late-season yields than any other June-bearing cultivar, with 'Earlyglow' and 'Honeoye' being the most early ripening cultivar. The conventional fertilizer increased plant vegetative growth, yield in May, and net photosynthesis of strawberry plants compared to the organic fertilizer at comparable rates, but did not affect time of fruit production or fruit quality. Organically fertilized strawberry plants grown in soilless substrate would likely require a combination of granular and liquid fertilizer sources to satisfy plant nutrient requirements effectively. More frequent irrigation in combination with the conventional fertilizer was beneficial for plant vegetative growth with improved shoot dry weight

    ACKNOWLEDGMENTS

    This work was supported by the United States Department of Agriculture (USDA) National Institute of Food and Agriculture Hatch Project MIS-112040 and the Mississippi State University Agricultural and Forestry Experimental Station Strategic Research Initiative. Mention of a trademark, proprietary product, or vendor does not constitute a guarantee or warranty of the product by Mississippi State University or the USDA and does not imply its approval to the exclusion of other products or vendors that also may be suitable.

  • Guihong Bi and Tonyin Li are the Editorial Board members of journal Technology in Horticulture. They were blinded from reviewing or making decisions on the manuscript. The article was subject to the journal's standard procedures, with peer-review handled independently of these Editorial Board members and their research groups.

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  • Cite this article

    Zhou T, Wu J, Zhang M, Ke W, Shan K, et al. 2023. Effect of natural plant extracts on the quality of meat products: a meta-analysis. Food Materials Research 3:15 doi: 10.48130/FMR-2023-0015
    Zhou T, Wu J, Zhang M, Ke W, Shan K, et al. 2023. Effect of natural plant extracts on the quality of meat products: a meta-analysis. Food Materials Research 3:15 doi: 10.48130/FMR-2023-0015
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Effect of natural plant extracts on the quality of meat products: a meta-analysis

  • State key Laboratory of Meat Quality Control and Cultured Meat Development,Ministry of Science and Technology; Key Laboratory of Meat Processing, Ministry of Agriculture and Rural Affairs; Jiangsu Provincial Collaborative Innovative Center of Meat Production, Processing and Quality Control; College of Food Science and Technology, Nanjing Agricultural University, Nanjing, 210095, PR China

  • Received: 12 December 2022
  • Accepted: 16 June 2023
  • Published online: 04 August 2023
Food Materials Research  3,  Article number: 15  (2023)  |  Cite this article

Abstract: Natural plant extracts (NPE) from some organs of plants are rich in bioactive substances. They have special nutritional characteristics with strong antioxidant and antimicrobial activities. The potential of NPEs to maintain and improve the quality of meat products has attracted attention due to concerns about the safety hazards of synthetic food additives. This paper extensively reviewed the application of NPE in meat processing, and systematically analyzed the comprehensive effects of different NPE using meta-analysis. Fourty-eight articles from 23 countries were studied with standard mean deviation (SMD) using random effect model, and 28 indexes were isolated. Results showed that NPE can reduce the pH value of meat products, improve antioxidant capacity, reduce the degree of oxidation and inhibit microbial growth. In addition, it was found that NPE had a significant impact on the quality of meat products. This meta-analysis provides quantitative evidence to explain how NPE affects meat quality, and helps to better understand the role of NPE in meat processing.

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    Introduction

    • Meat is an important source of high-quality protein and essential fatty acids. In recent years, the consumption of meat products has increased greatly. According to the statistical results of the Organization for Economic Co-operation and Development (OECD)[1], the world's per capita meat consumption reached 42.4 kg in 2021, although there is still a large gap between developed and developing countries. Due to different traditions, cultures, religions and other factors, the main types of edible meat differ among countries. However, no matter which kind of meat, consumers' demand always focuses on nutrition, safety and sensory quality[2]. Freshness, long-term storage without deterioration, and no chemical preservatives are the most attractive factors for consumers[3]. pH, color, texture, antioxidant capacity, oxidation degree, microbial composition and other indicators are closely related to meat quality[4]. Maintaining the good quality of meat products could enhance consumers' purchasing desire, maintain the unique nutritional composition of meat products, and avoid food waste and potential economic losses[5,6]. Therefore, meat quality has become the key to restrict the development of the meat industry. The challenge to maintain the quality of meat products brings great interest in using plant extracts in meat products.

      There are many bioactive substances from plants, such as polyphenols, carotenoids and alkaloids[7]. The natural plant extract (NPE) refers to something rich in bioactive substances extracted from different organs of plants such as roots, stems, leaves, flowers, fruits and seeds by using different solvents and extraction methods[8,9]. Most of them have special nutritional properties and strong antioxidant activity. Added to the food system, they could ameliorate food quality, improve nutritional quality, inhibit microbial reproduction, prolong shelf life, enhance flavor and control the formation of environmental pollutants. Although many techniques have been studied for food preservation, such as refrigeration[10−12], modified atmosphere storage[13−15] and pickling[16,17], meat products with high fat content inevitably undergo oxidative rancidity. It has led to the widespread use of food additives, especially preservatives. Although the safety has been recognized through long-term research, consumers are worried about the possible safety hazards. Thus, people pay attention to natural plant extracts[18], which have a wide range of sources, and large space for selection, and rarely involve ethical issues. Therefore, the application of natural plant extracts in meat processing has become a hotspot of research.

      Many papers have reviewed the advantages of plant extracts for meat products comprehensively and systematically, including the extraction methods and antioxidant properties[19], preservative effect[20], and special effects of a certain or a class of extracts[21−25]. However, most of reviews have certain limitations and subjectivity, and do not fully consider the nature of meat products. They usually focused on storage or nutritional quality, but ignored the impact of natural plant extracts on the sensory and texture of meat. In addition, the lack of quantitative evidence is also one of the weaknesses of traditional reviews. Meta-analysis is a quantitative data mining method, which expands the sample size by reorganizing the data reported in different studies, so as to obtain more reliable results[26]. Meta-analysis accurately explore the source of heterogeneity through group analysis[27,28], which helps to identify potential content that needs further deep study. Meta-analysis is widely used in clinical medicine and biological research[29], but it has not been fully used in food science research. This paper summarizes the application of NPE in meat products in the last three years, and combined with the basic principles of meta-analysis, the purpose was to comprehensively evaluate the impact of NPE addition on the quality of meat products, including physical, chemical, sensory, nutritional and microbial indicators. In addition, we examined the heterogeneity of the response by meta-analysis to determine the factors that lead to the observed variability in the response variables. The findings are expected to contribute to explaining how NPE improve the quality of meat products.

    Details of the meta-analysis used in this study

      Literature search and study selection

    • A comprehensive literature search was carried out in the databases of 'Web of Science' and 'Elsevier' to determine the research on the application of natural plant extracts in meat processing and its impact on the quality of meat products. The scope of the included research was expanded by the method of reference tracing. In all databases, the keywords 'natural, plant extract, meat' were used. Between 2020 and 2022, 613 scientific publications were published. Referring to the method of Orzuna-Orzuna et al.[27], these publications were screened in two steps. First, the title and abstract were used for selection, excluding articles that raise animals, reviews, and unmeasured variables of interest. Then the following issues were considered[30,31]: (1) natural plant extracts were used in the processing; (2) pH, color, texture, oxidation index and microbial index were measured; (3) the studies have appropriate control and experimental groups; (4) the publications contain figures for analysis; (5) peer-reviewed journal articles were written in English; (6) experimental design was employed (rotating or continuous); (7) least squares means of the control and experimental groups were measured with variability (standard error or standard deviation); and (8) sample size was used.

      Data extraction

    • According to the selection criteria, 48 articles were included in the database for final analysis, and the number of articles included in different indicators was different. The response variables extracted for the meta-analysis include pH, L*, a*, b*, antioxidant activity-DPPH, antioxidant activity-AA, antioxidant activity-ABTS, antioxidant activity-FRAP, metal chelating capacity-BHA, peroxide value (PV), total volatile base nitrogen (TVB-N), thiobarbituric acid reactant (TBARS), total bacterial count (TVC), total mesophilic (TMVC), psychrophilic bacteria, lactic acid bacteria, pseudomonas, enterobacteriaceae, yeast and mold , moisture content, moisture activity, water holding capacity (WHC), extrusion loss, cooking loss, hardness, toughness, cohesiveness, elasticity, and chewiness. In addition, in order to investigate which aspects of meat products are more affected by all reported natural plant extracts, the results of different studies are combined through data consolidation.

      Other data were collected as much as possible, such as the characteristics of published studies (author, year of publication), the product form of meat, the source of natural extracts, and the number of repetitions. The article references contained in the dataset are listed in Supplemental Table S1. The mean, standard deviation (SD) and number of repetitions of each treatment were extracted from these articles. When the article introduces the SD of each experimental group, these values are directly used in the meta-analysis. If SD is not reported, it is calculated by standard error[32].

      Calculation, statistical analysis and heterogeneity test

    • The data involved in meta-analysis were analyzed using Review Manager Software (version 5.4.1). Response variables were analyzed through the standardized mean difference (SMD), also called effect size (ES), the difference between the means of the experimental and control groups was standardized using the SD of the groups with and without NPE[33]. The heterogeneity is tested by formula (1) and the model is selected for meta-analysis[34]. i2 represents the proportion of inter study variation observed (due to real heterogeneity rather than accidental observation), Q is the standardized weighted sum of squares of each study variation, and df is the degree of freedom.

      i2=100%×Q−dfQ (1)

      i2 range from 0 to 100%. Values close to 25% represent low heterogeneity, close to 50% represent moderate heterogeneity, and close to 75% represent high heterogeneity in the study[35]. When i2 is greater than 50%, the random effect model is used to perform the analysis, otherwise, the fixed effect model is used, and Tukey test was used to detect the difference between the treatment groups[32].

      Publication bias

    • The publication bias was evaluated by funnel plot[36]. When it was asymmetric, it was considered that there was a bias (p < 0.10)[37,38]. However, for the index that the number of articles included in the study is less than ten, the test of publication bias is not carried out, which may lead to false positive statements[39].

      In-depth analysis and subgroup analysis

    • When the overall effect of a certain type of index is significant (p < 0.05), select an appropriate single index (the number of studies available for analysis is greater than 5) for in-depth analysis, and take the source of meat as the main classification basis for subgroup analysis, which is generally divided into five categories: fish (aquatic products), pork, beef, chicken, lamb[27].

      Study attributes and excluded studies

    • From 2019 to 2022, online searches using two databases of scientific publications returned 613 publications. After selecting and excluding duplicate papers according to the criteria, 189 full-text articles were evaluated. Finally, 48 articles (Supplemental Table S1) were used to obtain quantitative data for meta-analysis. Descriptive statistics for meta-analysis are shown in Table 1.

      Table 1.  Descriptive statistical results of all indicators included in MA.

      Parameter MPQNMeanMedianMinimumMaximumSD
      ConNFEConNFEConNFEConNFEConNFE
      pH
      pH4026.145.855.866.104.624.816.897.540.44190.3588
      Color
      a*15010.4311.829.229.58−0.971.6133.8645.278.69478.9012
      b*14914.7614.7812.4912.64−0.43−2.1838.5428.207.00307.3735
      L*15849.2147.0948.8747.4920.189.3376.0078.0611.729811.4085
      Texture
      Chewiness2039.1124.8267.2026.1414.6715.101654.001675.0028.729011.0752
      Cohesiveness170.630.560.570.490.220.180.770.760.09960.1320
      CL, %3634.2034.0750.7048.173.827.7477.3179.2426.559626.3236
      Elasticity233.673.493.453.990.510.496.616.962.53012.4518
      Hardness, N1914.1714.2020.6310.242.344.8955.3567.6221.932722.9578
      Moisture, %3357.3449.0464.3755.5431.6329.4373.6973.7313.888111.5185
      PL, %1022.981.3322.9820.0422.9820.0422.9820.041.00000.2700
      Water activity180.950.930.970.940.880.871.000.990.03980.0383
      WHC, %946.3540.8736.7026.9536.7023.3065.6672.3714.486323.6829
      Antioxidant capacity
      DPPH, IC50 (μg)2041.51161.1221.2248.744.8411.1845.17228.0310.955884.4908
      Oxidation index
      Pv, mmol/kg184.511.811.131.031.130.537.114.472.65711.3670
      TBARs, mg/kg4026.145.850.721.230.140.1819.0321.980.44190.3588
      TVB-N, mg/100g32.8021.0217.1032.6910.9528.5731.2655.761.88277.6660
      Microbial index, log10 cfu/g
      Enterobacteriaceae345.263.363.482.501.340.995.814.202.49281.4109
      Enterococcus31.680.000.840.000.000.001.680.001.35000.0000
      LAB336.405.994.983.624.073.006.556.541.92511.6709
      Micrococcus/
      staphylococcus      		45.193.985.193.985.193.985.193.980.04000.0300
      Mold and yeast73.612.713.432.592.131.714.723.461.38630.9415
      Pseudomonas247.966.706.386.316.386.316.386.311.75110.7401
      Psychrotrophic135.814.765.104.191.300.005.375.102.37131.8038
      TAC127.156.927.156.927.156.927.156.920.11000.1200
      TAMB127.087.057.087.057.087.057.087.050.09000.0400
      TMB96.525.297.056.035.974.407.056.080.75412.1113
      TPC217.205.895.483.883.353.246.825.372.75111.9788
      MPQ: Meat product quality; N: number of comparisons; SD: standard deviation; Con: control; NFE: Natural plant extracts; CL: cooking loss; PL: press loss; WHC: Water holding capacity; DPPH: DPPH radical scavenging activity; Pv: Peroxide value; TBARs: Thiobarbituric acid reactant; TVB-N, Volatile base nitrogen; LAB: lactic acid bacteria; TAC: Total aerobic cryophage; TAMB: Total aerobic mesophilic bacteria; TMB; Total mesophilic bacteria; TPC: Total plate count.

      The included studies were conducted in 23 different countries (Supplemental Table S1). The sources of raw meat could be divided into six types, of which pork accounts for 40.0%, beef for 30.4%, chicken for 17.4%, fish for 10.9%, and mutton and rabbit meat for 2.2%. On the other hand, the sources of extracts are diverse, including thyme, rosemary, basil and other plants used as spices, as well as blueberries, grapes and other fruits, broccoli, cabbage and other vegetables, and quebracho Colorado wood. The main bioactive substances in different extracts are different, but they could generally be summarized as polyphenols, flavonoids, anthocyanins, tannins and alkaloids.

    Effect of NPE on meat quality

    • Figure 1 shows the effects of NPE on the pH, color, texture, antioxidant properties, oxidation degree and microbial growth of meat products. In general, the addition of NPE to meat products had a significant impact on the quality of meat products (SMD −0.73, 95% CI [−1.00, −0.45], sample size = 1682, i2 = 99%, p < 0.00001), but had no significant impact on color (SMD −0.08, 95% CI [−1.84, 1.67], sample size = 457, i2 = 56%, p = 0.93) and texture (SMD −0.20, 95% CI [−0.44, 0.04], sample size = 185, i2 = 82%, p = 0.10). However, it is worth noting that although there is no significant difference between the two indicators on the whole, specific trends could be found according to the forest plot, such as 'chewiness' and 'press loss' are obviously more inclined to the experimental group.

      Figure 1. 

      The forest plot on the effect of NPE addition on the quality of meat products. The forest plot was extracted by RevMan Software (Version 5.4.1). The first author and year of publication is listed in the first column. (Complete list can be referred to from the References). CI, confidence interval; IV, inverse variance; S.D., standard deviation; std, standard. Vertical line in last column indicates no effect line, horizontal line indicates individual study—where the length determined by sample size. Diamond symbol indicates overall effect tendency. p-values following Chi2 stands for heterogeneity, whereas the p-value following Z stands for statistical significance.

      Except for color and texture, significant differences were found in all other indicators (p < 0.05). Specifically, adding NPE to meat products can reduce the pH of meat products (SMD -0.29, 95% CI [−0.34, −0.23], sample size = 402, p < 0.00001), improve antioxidant capacity (SMD 119.61, 95% CI [82.87, 156.95], sample size = 20, p < 0.00001), reduce the oxidation degree of meat products (SMD −5.98, 95% CI [−10.49, −1.48], sample size = 446, i2 = 97%, p = 0.009) and inhibit microbial growth (SMD −0.87, 95% CI [−1.40, −0.34], sample size = 172, i2 = 99%, p = 0.001). It is found that the different indicator subgroups are related to redox, which may indicate that the role of NPE in improving the quality of meat products is based on its antioxidant properties.

      Effect of NPE on pH of meat products

    • Figure 2 shows the effect of adding NPE on the pH of meat products from different raw materials. The summary results of meta-analysis show that addition of NPE reduces the pH (SMD −0.23, 95% CI [−0.32, −0.13], sample size = 402, study = 51; i2 = 100%; p < 0.00001). Four studies have reported the effect of NPE on the pH of fish meat products. Meta-analysis showed that the pH of all fish meat products decreased after the addition of NPE (SMD −0.26, 95% CI [−0.28, −0.24], sample size = 33, study = 4; i2 = 55%; p < 0.00001).

      Figure 2. 

      The forest plot on the effect of NPE on pH of meat products produced with different raw materials.

      In the subgroups of pH of products from other raw meat, the addition of NPE significantly reduced the pH of beef products (SMD −0.28, 95% CI [−0.50, −0.07], sample size = 128, study = 16; i2 = 100%; p = 0.008). However, high heterogeneity was observed in the results. Among the 16 studies, the results of Al-Juhaimi et al.[40] and Hastaoğlu et al.[41] showed that the addition of NPE had no significant effect on the pH of beef products, and its weight share was 0.8%, 0.7%, 2.2% and 2.2% respectively, 30.5% of which was the total weight of the subgroup.

      In selected studies, the addition of NPE reduced the pH of pork products (SMD −0.16, 95% CI [−0.28, −0.04], sample size = 108, study = 20, i2 = 99%, p = 0.008). The overall effect showed that the addition of NPE had a significant effect on the pH of pork products, but still showed high heterogeneity. Eight studies crossed the invalid boundary.

      In the study on the pH of other meat products, the addition of NPE significantly reduced the pH of chicken products (SMD −0.23, 95% CI [−0.44, −0.02], sample size = 128, study = 9, i2 = 100%, p = 0.003), and also significantly affected the pH of mutton products (SMD −0.34, 95% CI [−0.41, −0.27], sample size = 5, study = 1, p < 0.00001).

      Taken together, the pH of fish, beef, pork, chicken and mutton products will be significantly reduced after adding NPE. The heterogeneity among different subgroups is low, and there is no significant difference (i2 = 49.9%, p = 0.09), indicating that NPE may delay the oxidation of meat products, thus showing a lower pH, and this effect is independent of the type of meat.

      Effect of NPE on oxidation degree of meat products

    • According to the analysis, NPE in meat products are based on their antioxidant properties, so it is necessary to further study their antioxidant properties in different meat products and the oxidation degree with or without NPE. TBARS and TVB-N were selected as the main analysis dimensions according to the number of studies available for analysis.

      Figure 3 shows the effect of adding NPE on TBARS values of different meat products. The summary results of meta-analysis showed that NPE had a significant impact on the TBARS value of meat products (SMD −0.93, 95% CI [−1.65, −0.20], sample size = 304, study = 36, i2 = 100%, p = 0.01). However, the results of different subgroups have certain heterogeneity, in other words, the antioxidant capacity of NPE in different raw meat may be different (i2 = 64.5%, p = 0.02).

      Figure 3. 

      Forest plot on the effect of NPE on TBARS of meat products produced with different raw materials.

      Specifically, in beef products (SMD −0.85, 95% CI [−1.10, −0.60], sample size = 107, study = 11, i2 = 100%, p < 0.00001) and chicken products (SMD −0.47, 95% CI [−0.61, −0.33], sample size =128, study = 12, i2 = 99%, p < 0.00001), addition of NPE has a significant impact on the TBARS value. However, there was no significant difference among meat products prepared with fish (SMD −0.30, 95% CI [−0.68, 0.08], sample size = 27, study = 4, i2 = 99%, p = 0.12), pork (SMD −0.24, 95% CI [−0.56, 0.08], sample size = 31, study = 6, i2 = 99%, p = 0.15) and mutton (SMD −0.64, 95% CI [−1.37, 0.10], sample size = 11, study = 3, i2 = 100%, p = 0.09). The above results may indicate that NPE has different antioxidant capacity in different raw meat, and it may also indicate that some NPE play a role in meat products independent of antioxidant capacity to enhance flavor, color, and taste.

      Volatile base nitrogen, another important indicator for the degree of oxidation in meat products is shown in Fig. 4. Subgroup analysis was not conducted due to the small number of studies available for analysis. However, the overall effect showed that the addition of NPE could significantly reduce the TVB-N value of meat products (SMD −18.32, 95% CI [−23.11, −13.54], sample size = 26, study = 4, i2 = 100%, p < 0.00001). The four studies included in the analysis showed consistency. In all studies, the TVB-N values of the groups treated with NPE were lower than control without NPE.

      Figure 4. 

      Forest plot on the effect of NPE on TVBN of meat products produced with different raw materials.

      Effect of NPE on the total plate count of meat products

    • The growth of microorganisms has an important impact on the sensory, safety and shelf life of meat products[42]. The analysis includes several indicators closely related to the growth of microorganisms. However, due to the difference in categories of microorganisms in different meat products and storage methods in different studies, there is a small number of studies for further analysis of each indicator, and only the total number of colonies is used for in-depth analysis.

      The results of TPC showed that the addition of NPE could inhibit the growth of microorganisms, which was manifested by significantly reduced TPC of meat products (SMD 0.90, 95% CI [0.30, 1.49], sample size = 21, study = 6, i2 = 99%, p = 0.003) (Fig. 5). This result is confirmed by pH results above. NPE may prevent the pH rise of meat products through antioxidant effect, thus creating an adverse growth environment for microorganisms. It may also inhibit the growth of microorganisms through antibacterial effect, so that meat products show a low pH.

      Figure 5. 

      The forest plot on the effect of NPE on total plate count (TPA) of meat products produced with different raw materials.

      Publication bias detection

    • The funnel plot was used to detect the publication bias of indicators. Publication bias is a measure in meta-analysis. The more obvious the processing effect of the study, the easier it is to be published, which leads to publication bias[43]. In addition, poor experimental design, reporting bias and errors also lead to publication bias[34]. Sterne et al.[44] believe that large heterogeneity (i2 > 75%) will affect the detection of publication bias. The publication bias detection of this meta-analysis is shown in Fig. 6. It can be seen from Fig. 6a that the oxidation index shows an obvious asymmetric trend, which may be due to the error effect caused by too few studies available for meta-analysis. The texture index also shows an obvious asymmetric trend, but it is mainly located in the triangle of 95% confidence interval, indicating that the publishing bias is small. The publication bias detection of meta-analysis for pH and TBARS is shown in Fig. 6b & c. The beef and chicken groups show asymmetry, which may be caused by the high heterogeneity. In addition, the points of the funnel plot accumulate at the top of the plot, indicating a low-risk bias.

      Figure 6. 

      Funnel plot of studies to detect the publication bias for the selected parameters. (a) Overall effect. (b) pH. (c) TBARS.

    Mechanisms of NPE to improve the meat quality

    • NPE come from a wide range of sources and are rich in active ingredients. Rational use of NPE extracted from low value parts such as pericarp, seeds and rhizomes is of great significance to the food industry[19,45]. Most of the isolated NPE with antioxidant effect are polyphenols with metastable antioxidant properties or secondary metabolites with conjugated double bonds[46]. Their main active components are polyphenols, flavonoids, phenolic diterpenes and tannins[47]. Many studies have been done on the extraction, separation, identification and application of NPE in meat products[48,49]. The results showed that based on its antioxidant properties (Fig. 7), it played a role in delaying oxidation, controlling pollutants, inhibiting microorganisms, alternating nitrate, enhancing flavor and improving quality in meat products[19]. However, relevant studies also show some heterogeneity, which indicates that the effect of NPE on meat products may be diversified. In addition, few qualitative or descriptive review articles are reported in peer-reviewed computable journals. There is no statistical review on the comprehensive quality impact of NPEs on different meat products. The present study evaluated the impact on different indicators, the consistency of evaluation results and their relationship.

      Figure 7. 

      Effect of NPE based on antioxidant properties on meat product quality.

      With high nutritional value, meat products provide human beings with proteins, lipids, minerals, vitamins and other trace elements necessary for growth and development[45,50]. However, rich nutrients also make it easy to deteriorate. It is generally believed that bacterial growth and lipid oxidation are the main reasons for the degradation of meat quality[51]. Storage and processing are the critical points to control the quality of meat. However, the potential safety hazards of using artificial preservatives, the cumbersome and uneconomical treatment of freezing, curing, air drying and other treatments, as well as the impact on the sensory quality of meat, have led people to focus on NPE[52].

      As for the mechanism of NPE in meat products, inhibition of lipid and protein oxidation is the basis (Fig. 8). Due to the free radical chain reaction, the reactive oxygen species and metal ions cause oxidative damage to meat protein[53], and also produce unpleasant flavour substances such as malondialdehyde through oxidation reaction[54,55]. In addition, hemoglobin and myoglobin also promote lipid oxidation in meat products[56]. Here, antioxidants react with free radicals to form stable inactive products[57]. According to relevant studies, antioxidants could be divided into two categories according to their action modes. One is called broken chain antioxidant compounds, which react directly with lipid free radicals by providing hydrogen atoms, and the other loses catalytic function by combining with metal ions[58]. NPE might have the function of two kinds of antioxidants at the same time because it contains a variety of active ingredients (Fig. 9). For example, phenolic acids and phenolic diterpenes have a strong ability to provide hydrogen atoms, while flavonoids and other phenolic compounds are considered to be able to chelate with metal ions[59−61].

      Figure 8. 

      Possible mechanism of NPE improving meat product quality.

      Figure 9. 

      Antioxidant mechanism of common bioactive substances in NPE.

      Evidence has shown that synthetic antioxidants (butyl hydroxyanisole, butyl hydroxytoluene, propyl gallate and tert butyl hydroquinone) have potential genotoxicity, and high-dose use might even cause cancer[62]. However, there is little evidence that NPE has adverse effects on meat products or human body. NPE could not only prevent the oxidation of lipids and proteins, but also maintain the normal texture, color, taste and flavor of meat products, and avoid the destruction of vitamins and the formation of toxins[63,64]. In particular, ascorbic acid, anthocyanins, carotenoids, dehydroascorbic acid, glutathione, phenols and flavonoids in NPE are recognized antioxidants[65,66]. Some studies showed that addition of NPE to the formula has excellent antioxidant potential. If appropriate NPE were supplemented, and appropriate treatment or processing methods were applied, meat products will show strong antioxidant properties[67].

      In this meta-analysis, the summary results of pH, antioxidant properties, oxidation degree and microbial growth showed that the addition of NPE significantly delayed the oxidation of meat products but had no effect on color and texture. Some earlier studies indicate that NPE can protect the color of meat products by delaying the oxidation of hemoglobin[68]. However, after processing, the effect of its ingredients on color may be greater than that of hemoglobin. As for the impact on texture, earlier studies indicated that NPE changed the water retention capacity of meat products, thereby affecting other texture indicators[69]. The difference among these studies could be due to the fact that the antioxidant properties of NPE are not as strong as those of natural active substances artificially separated and purified, or that the color and texture of meat products themselves do not change significantly during the reported storage period.

      NPE based on phenols, flavonoids and tannins show the ability to limit and scavenge reactive oxygen species[70,71], and are fully used in different forms of meat products. For example, olive leaf essential oil rich in polyphenols can inhibit the microbial growth of fresh poultry and prolong its shelf life[72]. Garlic extract containing flavonoids and sulfur compounds can effectively inhibit lipid oxidation of sausage[10]. Rosemary extract rich in rat tail oxalic acid and terpene dienes can effectively reduce the TBARS value of beef balls during 12 d of storage[73]. When NPE with strong antioxidant capacity are added to meat products, they still have antioxidant potential, and based on their antioxidant properties.

      Different NPE extraction methods might have an impact on its antioxidant effect. Awad et al.[19] summarized the common NPE extraction schemes, including traditional water extraction, alcohol extraction, soxhlet extraction and emerging supercritical fluid extraction, ultrasonic assisted extraction, subcritical water extraction, microwave-assisted extraction and real-time pressure drop extraction. The application of various extraction technology combinations can play a synergistic effect.

      Many studies have analyzed the impact of NPE on human health. Rosemary extract (rosmarinic acid) has anti-inflammatory activity by stimulating the secretion of interleukin-10[74]. Origanum extract controls stress gastritis and hypersensitivity by inhibiting the secretion of cyclooxygenase-2 (COX-2) in epithelial cancer cells[75,76]. Kaempferol, a aglycone flavonoid abundant in Aloe Vera and peaking spurge, could prevent hepatocellular carcinoma by controlling oxidative stress caused by reactive oxygen species[77]. In addition, some flavonoids from moss can upregulate caspase-3/cleaved-caspase-3 and induce apoptosis of A549 cells by inhibiting the expression of XIAP and Survivin[78]. Luteolin and other flavonoids could selectively reduce the vitality of cancer cells and change some signal pathways, thus playing an anti-cancer effect in the human body[79]. The health effects of these NPE on human body have been very clear, but considering that they are often added to meat products, whether the final products are still beneficial to human health remains to be further studied.

      Consumer demand for natural preservatives is the main driving force for the research on the application of NPE in meat products. However, the bad taste and color of some NPE might adversely affect the sensory properties of products, so the combination of multiple NPE may be a feasible way. In addition, another challenge in the application of NPE is interaction with different meat products, which leads to the fact that some compounds play an effective antioxidant effect in vitro even at low concentrations, but they need to be used in high concentrations in meat products[80]. In particular, phenols and carotenoids can bind to meat protein or lipids, so the structure-activity relationship and dose effect are worthy of attention[23].

    Conclusions

    • Consumers' preference for natural ingredients makes them prefer meat products that use NPE as preservatives and nutritional enhancers rather than synthetic compounds. Therefore, many studies have applied NPE to improve the quality of meat products. The present study indicates that NPE has a positive effect on the quality of meat products. The addition of NPE reduces the pH of meat products, improves antioxidant capacity, delays product oxidation and inhibits microbial reproduction. Specifically, NPE reduce the pH, peroxide value, TBARS and TVB-N value of meat products, inhibit the growth of bacteria such as Enterobacteriaceae, Enterococcus, micrococcus/staphylococcus and Pseudomonas, reduce total microbial cryophase and total plate count, and increase DPPH free radical scavenging activity. NPE effectively protect meat products, reduce the degree of lipid and protein oxidation, and prolong the shelf life without changing the basic properties of meat products, such as color and texture. The results might help to better understand the role of NPE in meat processing and it offers an advantageous method to quantitatively analyze how food components affect food matrix. Given the numerous and intricate sources of NPE, it is essential to classify it based on biochemical makeup and do a thorough investigation. The dose-effect relationship between the addition of NPE and the quality of meat products still need more study. Further investigation should be done in the future on the association between meat products containing NPE and human health from the standpoint of metabolic pathways, taking food safety concerns into consideration.

      Acknowledgments

      • This study was funded by the Jiangsu Innovative Group of Meat Nutrition and Biotechnology.

      Conflict of interest

      • The authors declare that they have no conflict of interest. Chunbao Li is the Editorial-Board member of Food Materials Research, who was blinded from reviewing or making decisions on the manuscript. The article was subject to the journal's standard procedures, with peer-review handled independently of this Editorial-Board member and his research groups.

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      • Copyright: © 2023 by the author(s). Published by Maximum Academic Press on behalf of Nanjing Agricultural University. This article is an open access article distributed under Creative Commons Attribution License (CC BY 4.0), visit https://creativecommons.org/licenses/by/4.0/.
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    Zhou T, Wu J, Zhang M, Ke W, Shan K, et al. 2023. Effect of natural plant extracts on the quality of meat products: a meta-analysis. Food Materials Research 3:15 doi: 10.48130/FMR-2023-0015
    Zhou T, Wu J, Zhang M, Ke W, Shan K, et al. 2023. Effect of natural plant extracts on the quality of meat products: a meta-analysis. Food Materials Research 3:15 doi: 10.48130/FMR-2023-0015
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  • Introduction
  • Details of the meta-analysis used in this study

  • Literature search and study selection

  • Data extraction

  • Calculation, statistical analysis and heterogeneity test

  • Publication bias

  • In-depth analysis and subgroup analysis

  • Study attributes and excluded studies

  • Effect of NPE on meat quality

  • Effect of NPE on pH of meat products

  • Effect of NPE on oxidation degree of meat products

  • Effect of NPE on the total plate count of meat products

  • Publication bias detection

  • Mechanisms of NPE to improve the meat quality
  • Conclusions
  • Acknowledgments
  • Conflict of interest
  • Supplementary information
  • Rights and permissions
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