Correlations between the phenolic and fibre composition of mushrooms and the glycaemic and textural characteristics of mushroom enriched extruded products

Journal Pre-proof Correlations between the phenolic and fibre composition of mushrooms and the glycaemic and textural characteristics of mushroom enriched extruded products Xikun Lu, Margaret A. Brennan, Joan Narciso, Wenqiang Guan, Jie Zhang, Li Yuan, Luca Serventi, Charles S. Brennan PII:

S0023-6438(19)31072-2

DOI:

https://doi.org/10.1016/j.lwt.2019.108730

Reference:

YFSTL 108730

To appear in:

LWT - Food Science and Technology

Received Date: 6 March 2018 Revised Date:

30 September 2019

Accepted Date: 10 October 2019

Please cite this article as: Lu, X., Brennan, M.A., Narciso, J., Guan, W., Zhang, J., Yuan, L., Serventi, L., Brennan, C.S., Correlations between the phenolic and fibre composition of mushrooms and the glycaemic and textural characteristics of mushroom enriched extruded products, LWT - Food Science and Technology (2019), doi: https://doi.org/10.1016/j.lwt.2019.108730. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Published by Elsevier Ltd.

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Correlations between the phenolic and fibre composition of mushrooms and the glycaemic and textural characteristics of mushroom enriched extruded products

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Xikun Lu

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Serventi , Charles S. Brennan

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a,b,c

a

a

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a

a

b

d

d

, Margaret A. Brennan , Joan Narciso , Wenqiang Guan , Jie Zhang , Li Yuan , Luca a,b,c

*

Department of Wine, Food and Molecular Biosciences, Lincoln University, P O Box 84, Lincoln 7647,

Christchurch, New Zealand b

Tianjin Key Laboratory of Food Biotechnology, College of Biotechnology and Food Sciences, Tianjin

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University of Commerce, Tianjin, China c

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Riddet Institute, Palmerston North, New Zealand

d

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Institute of Food Science and Technology, Chinese Academy of Agricultural Sciences/Key Laboratory

of Agro-products Processing, Ministry of Agriculture, Beijing 100193, China

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*Correspondent: E-mail: [email protected]; postal address: department of Wine, Food

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and Molecular Biosciences, Lincoln University, P O Box 84, Lincoln 7647, Christchurch, New Zealand

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E-mail addresses: [email protected] (X.K. Lu), [email protected] (M.A.

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Brennan), [email protected] (J. Narciso), [email protected] (W.Q. Guan),

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[email protected] (J. Zhang), [email protected] (L. Yuan), [email protected] (L. Serventi),

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[email protected] (C.S. Brennan).

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Abstract

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In this study, semolina extruded snack products were supplemented with white

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button mushroom (Agaricus bisporus), shiitake (Lentinula edodes) and porcini

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mushrooms (Boletus edulis). The functional properties of the products were analysed,

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including the nutritional profile, starch characteristics (content, gelatinization and

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digestibility) and antioxidant activities (total phenolic content, DPPH and ORAC),

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colour, and textural properties. Compared to the control samples,

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supplemented with mushroom powder showed a reduced product expansion,

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decreased water absorption index, increased water solubility index and altered

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microstructure characteristics. Differences in starch gelatinization and starch

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hydrolysis resulted in a reduced predictive glycaemic response value for mushroom

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supplemented extrudates. Inclusion of mushroom material resulted in higher levels

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of phenolic compounds and antioxidants.

extrudates

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Keywords: mushroom; hot extruded snack; glycaemic index; antioxidant capacity

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1. Introduction

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Hot extrusion is a thermal process that includes mixing, forming, texturizing and

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cooking (Brennan, Derbyshire, Tiwari, & Brennan, 2013). The popularity of hot

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extruded snack products is increasing due to their puffy, crisp and crunchy textures

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(Wani & Kumar, 2016). Most extruded snacks are derived from cereals and are often 2

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nutritionally unbalanced; for example, they are low in vitamins, minor minerals,

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dietary fibre, essential amino acids and other bioactive compounds (Brennan et al.,

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2013). These products exhibit increased starch digestibility attributed to starch

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gelatinisation and fragmentation by the shearing process, and are treated as high

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glycaemic index foods (Brennan et al., 2013). The addition of bioactive

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phytochemicals provides can improve their nutritional components (Wani & Kumar,

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2016).

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Mushrooms are good sources of protein, bioactive polysaccharides, vitamins, minor

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minerals, dietary fibre and unsaturated fatty acids (Lu, Brennan, Serventi, Mason, &

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Brennan, 2016). In particular, they contain ergothioneine, which humans cannot

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synthesise themselves (Weigand-Heller, Kris-Etherton, & Beelman, 2012).

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White button mushroom (Agaricus bisporus) is the most commonly consumed edible

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mushroom in the US and European countries (Breece, 1990). Shiitake (Lentinula

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edodes) and porcini mushrooms (Boletus edulis) are regarded as specialty

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mushrooms.

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Recently, attention has focused on the use of mushroom bioactive ingredients in

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functional food products and how consumers perceive these products (Tepsongkroh

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et al., 2019). For instance mushroom materials have been used as nanoparticles to

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be included in the food industry as effective functional food ingredients (Wang et al., 3

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2018). Jin et al. (2018) illustrated that ingredients from Pleurotus eryngii could be

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used to reduce post-prandial cholesterol levels. The challenge is how to ultilise these

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ingredients in food systems rather than just in isolated forms, and how the antioxidant and

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bioactive ingredients could be used for human nutrition (Adebayo et al., 2018; Li et al.,

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2018). Mushroom materials have been used in bread and pasta product to enrich the

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protein and fibre contents to great effect (Lu et al., 2018) and also in snack food products

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(Vallée et al., 2017). In a recent study, researchers have also used shitake mushrooms

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in muffins in order to increase the phenolic content of muffins and improve the nutritional

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quality of these foods (Olawuyi and Lee, 2019). The benefits of such inclusions coming

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from the bioactive ingredients found in the mushroom materials (Bach et al., 2017; Vital et

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al., 2017)

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The objectives of the current study were to determine how inclusion of mushroom

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bioactive compounds alters the physical, textural and nutritional properties of

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extruded products.

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2. Material and methods

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2.1 Materials

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Commercial semolina (Sun Valley Foods, Auckland, New Zealand), dried shiitake

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mushroom and porcini mushroom sliced (Jade Phoenix, Guangzhou, China) and fresh

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white button mushroom (Meadow Mushrooms, Christchurch, New Zealand) were 4

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used.

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2.2 Extrusion processing

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Extruded products were produced using a single screw extruder (screw

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configurations being: screw length: 30 cm, screw diameter: 30 mm, barrel length 300

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mm, inside screw shaft diameter 30 mm, outside screw shaft diameter 40 mm, die

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diameter 3 mm) obtained from Northern finance Ltd (MM1, Auckland, New Zealand).

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Table 1 summarizes operating details. Expanded snack products were collected,

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cooled and stored in sealed polyethylene bags at room temperature for further

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analysis.

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Nine samples supplemented with mushroom powder were produced by substituting

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durum wheat semolina with white button mushroom, shiitake mushroom and porcini

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mushroom powder respectively. The level of mushroom powder replacement for

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flour was at 5 g/100 g, 10 g/100 g and 15 g/100 g (w/w) of semolina flour

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respectively with a control reference being exclusively durum wheat semolina (Fig.

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1-supplementary).

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2.3 Near infrared spectroscopy

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Near infrared spectra of ground extruded products was determined using Calorie

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AnswerTM (CA-HM, JWP, Japan) according to the method reported by (Lau, Goh, Quek,

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Lim, & Henry, 2016): the wavelength ranged from 1100-2200×10-9 m, the resolution

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was 7.5×10-9 m, and the data interval was 2.0×10-9 m. The reflectance mode was

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used for the powders, and the reference reflectance was analysed by a calcium

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carbonate filled cell. Samples were scanned in cylindrical sample cell and the

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powdered cereals and dried noodles mode of the machine was selected as the

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analysis setting. Each triplicate portion was scanned 10 times. The averaged mean

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spectrum was obtained in order to improve accuracy by the inbuilt computer

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software (CA-HM Measurement Application Software, JWP, Japan). All the data was

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transformed into log 1/R and the calorie content was calculated according to the

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regression expressions pre-programmed by this software, which was in accordance

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with the selected setting for analysis.

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2.4 Physicochemical characteristics

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The hardness and crunchiness of all extruded products were analysed using a TA-XT2

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Texture Analyzer (Stable Micro Systems, Surrey, UK). An aluminum cylinder probe of

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25 mm diameter was used with a test speed of 1 mm/s at a trigger force of 5 g and

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the extruded samples were compressed to 50% of original height. The peak force

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recorded represented the hardness of the product, whereas the number of fracture

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peaks represented crunchiness. All measurements were performed for a minimum of

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12 samples (Brennan et al., 2013).

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The extruded samples were measured for their length (le), diameter (De) and mass

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(me) using 20 pieces of hot extruded from each treatment. The radial expansion ratio

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of the extruded samples (ER) and specific length of the samples (lsp) were obtained

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by the formulas below (Karkle, Keller, Dogan, & Alavi, 2012): 1

=

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2

=

(

/ )

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where Dd = die diameter (3 mm).

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The product density and the percentage expansion of samples (using the formula

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below) were calculated following the method of Brennan et al., (2013): 3 % Expansion =

× 100

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The water absorption index (WAI) and water solubility index (WSI) were determined

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by the method described by Anderson, Conway, & Peplinski, (1970). The moisture

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content of samples were analysed according to the air-oven method at 105℃ (AACC,

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2010).

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Total dietary fibre (TDF) content was determined in duplicate using a Total Dietary

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Fibre assay kit (Megazyme International Ireland Ltd, Wicklow, Ireland).

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Measurements were recorded for soluble (SDF) and insoluble fibre (IDF) composition

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as described by Brennan et al. (2013). The protein content was determined using a 7

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Rapid Max N exceed (Elementar, Langenselbold, Germany) using the conversion

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factor of 6.25.

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2.5 Colour

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The colour of all extruded samples was measured using a colorimeter CR-210

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(Minolta, Tokyo, Japan). The results were expressed using the L*, a* and b* values.

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The total colour difference ∆E* between the control and mushroom enriched

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samples was determined by the following formula: 4 ∆

∗

= #∆$∗ + ∆&∗ + ∆' ∗

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2.6 Differential scanning calorimetry (DSC)

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Differential scanning calorimetry (DSC; TA Q20, TA Instruments, Newcastle, DE) was

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used to measure the starch gelatinisation characteristics of hot extruded samples

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using the method reported by Aravind, Sissons, Egan, & Fellows, (2012). Samples (4-6

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mg) were weighed into a hermetic DSC pan with 10 µl of water,

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hermetically sealed and allowed to equilibrate overnight at room temperature. The

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reference was an empty pan and lid which was pressed together. The samples were

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heated from 10 ℃ to 110 ℃ at a rate of 10 ℃/min. A DSC heating curve was

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generated in this process, and measurements were done in duplicate. Temperatures

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of onset (Tonset), gelatinisation (peak), endset (Tendset) and the enthalpy of the

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samples were

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transition (∆H) were obtained in this process.

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2.7 Total phenolic content and antioxidant capabilities

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Total phenolic content (TPC) of all samples was measured using 0.2 N Folin-Ciocalteu

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reagent (Sigma, St Louis, USA) according to the method reported by Singleton & Rossi

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(1965). The results were expressed as gallic equivalent per gram dry weight. The

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ability of all the samples to scavenge DPPH (1,1-diphenyl-2-picrylhydrazyl) radical was

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determined as described by Floegel, Kim, Chung, Koo, & Chun

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were expressed as micromoles of Trolox per gram dry weight. The oxygen radical

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absorbance capacity-fluorescence assay (ORAC) was carried out using the method

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described by Thaipong, Boonprakob, Crosby, Cisneros-Zevallos, & Hawkins Byrne

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(2006). The results were expressed as micromoles of Trolox per gram dry weight.

(2011). The results

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2.8 Starch content and in vitro starch digestibility analysis

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Total starch was determined using the Total Starch assay kit (Star) from Megazyme

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International (Wicklow, Ireland).

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The potential amount of glucose released over 120 min was conducted for each

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pasta type was conducted as described previously Foschia, Peressini, Sensidoni,

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Brennan, & Brennan (2015). The amount of reducing sugars released were recorded

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at 0, 20, 60 and 120 min during the digestion process. The glucose released curves

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could be obtained and then the areas under the curve (AUC) could be measured by

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the trapezoid rule.

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2.9 Microscopy

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The microstructure of the extruded products was evaluated by scanning electron

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microscope (SEM, Joel 75, Tokyo, Japan). Samples were coated with gold using a

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MCI000 Ion Sputter Coater, then were viewed using a SU8010 SEM at 500×

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magnification level.

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2.10 Statistical analysis

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Unless stated elsewhere, the experiments were performed in triplicate. Statistical

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differences were determined by one-way analysis of variance (ANOVA) and Tukey’s

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comparison test (p ≤ 0.05). Pearson’s correlations were also carried out to analyse

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the significant correlations at p ≤ 0.05, p ≤ 0.01, and p ≤ 0.001, respectively.

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3. Results and discussion

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3.1 Near-infrared spectroscopy

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The fat, carbohydrate, water and calorie contents of the control and mushroom 10

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supplemented hot extruded samples were measured using a Calorie AnswerTM

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machine which has been calibrated or cereal and vegetable products (Table 2).

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The carbohydrate content of most of the mushroom enriched samples did not show

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any significant differences (p ≤ 0.05) from the control. The fat content of all the

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mushroom extruded products was significantly higher (p ≤ 0.05) than that the control

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extruded sample, and increased with increasing mushroom powder content. Lu et al.

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(2016) had previously shown that all three mushroom species contained more fat

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than semolina on a dry weight basis: (white button (2.42 ± 0.04 %), shiitake

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mushroom (1.48 ± 0.02 %), porcini mushroom (3.03 ± 0.03 %) and semolina (1.17 ±

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0.09 %)).

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The addition of mushroom powder increased the samples’ energy compared to the

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control (Table 2). Such an increase may be attributed to increased fat content.

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Significant positive correlation (Table 3) exists between sample energy and fat

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content (r=0.857, at p≤0.001).

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3.2 Physicochemical properties

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The expansion ratio of the three different mushroom species of enriched samples

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showed an inverse relationship with the amount of enriched mushroom powder

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incorporated. These results were all significantly lower, or similar, to the control

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except for the 5 % white button mushroom substitution (Table 4). All three

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mushroom species contained higher total dietary fibre than semolina (as shown in

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Table 4). The IDF and TDF contents of mushroom enriched products increased

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significantly (p≤0.05) and proportional to substitution levels compared to the

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control (Table 2). Such higher dietary fibre contents and the relative absence of

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starch could decrease the free water of the raw materials in the extruder barrel. This,

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in turn, may limit the expansion of the products as reported previously (Brennan et

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al., 2013). This hypothesis is confirmed by the negative correlations between the

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expansion of sample and all IDF, SDF and TDF values (Table 3). The reduced

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expansion ratio of the mushroom enriched samples may also be due to the higher fat

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contents in the mushroom powder than in the semolina which may reduce the

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extrudate viscosity and, consequently, reduce the pressure difference the pre- and

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post- the die face as mentioned by Robin, Dubois, Pineau, Schuchmann, & Palzer,

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(2011). Table 3 demonstrates negative correlation between sample expansion and fat

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content (r=-0.420, p≤0.05). Generally, the sample density showed an inverse trend

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of expansion ratio in this study (r=-0.669, p≤0.001); this supports the work of Karkle

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et al., (2012). However, the specific length of the extruded samples increased

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compared to the control. Some researchers have reported similar results, showing

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that the inclusion of fibre rich materials resulted in increased longitudinal expansion

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(Karkle et al., 2012). This observation is consistent with that of Table 3 illustrating

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positive correlations between the specific length and both IDF and TDF (r=0.888,

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0.858, respectively, at p≤ 0.001). A significant positive correlation is observed 12

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between specific length and fat content (Table 3). This phenomenon may be

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explained by the reduced viscosity caused by enriched lipids or other ingredients

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changing the expansion direction.

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Water absorption index (WAI) values of the supplemented samples decreased

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significantly (p≤0.05) compared to the control. In contrast, the water solubility index

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(WSI) values of the white button enriched samples increased slightly and the other

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two mushroom samples increased significantly when compared to the control (Table

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4). The WAI results were similar to previous observations, investigating the influence

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of the inclusion of chestnut mushroom co-products on extruded snack products,

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where the WAI values decreased with increasing levels of substitution (Brennan et al.,

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2013). Table 3 illustrates negative correlations between WAI and the proportion of

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IDF, SDF and TDF. WAI relates to the proportion of intact starch granules that were

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fully gelatinized; researchers have shown a positive relationship between the degree

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of starch fragmentation and gelatinisation and the WAI (Brahma, Weier, & Rose,

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2016). This fact is further supported by the significant negative correlation between

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∆H and WAI (r=-0.7, p≤0.001) found in this study (Table 3). A higher WAI is an

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indication of shorter starch chains arising from the fragmentation of the long chains

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during shearing during extrusion; the shorter chains having stronger solubility

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capacity (Hagenimana, Ding, & Fang, 2006). Table 3 illustrates a positive correlation

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between starch content and WAI (r=0.634, r≤0.001). The starch contents of the

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three mushroom powders were much lower than those of semolina (semolina (73.11 13

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± 1.17 %); white button (1.90 ± 0.02 %); shiitake mushroom (2.45 ± 0.14 %] and

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porcine mushroom (2.62 ± 0.08 %) on a dry weight basis). The WSI indicates the

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amount of soluble starch present after extrusion (Brahma et al., 2016). There were

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positive correlations between the WSI and both IDF and TDF (r=0.747 and 0.759,

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respectively, at p≤0.001). One can suggest that the additional mushroom fibre may

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interrupt the protein and starch networks, thus increasing the WSI. The WAI was

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inversely related to the WSI values in this study (r=-0.513, p≤0.01) and a similar

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finding has been reported by (Pęksa et al., 2016). Interestingly, Pęksa and others

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(2016) reported that there was no obvious relationship between WAI and the

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textural attributes of the hot extruded samples. However, Table 3 illustrates a

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significant positive correlation between WAI and sample expansion, and negative

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correlations between WAI and both sample density and specific.

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3.3 Textural properties

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The structure of an extruded sample illustrate the presence of an outer area, formed

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by a layer of collapsed gas cells, which was relatively hard, as well as an inner section,

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formed by gas cells, which was brittle. In this way, the integrity of the outer coat

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formation and the expansion extent of the extrudate determines the textural

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characteristics (Brennan et al., 2013). The hardness of extrudates with white button

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mushroom decreased initially then increased compared to the control; shiitake

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mushroom samples decreased significantly (p≤0.05) with increasing incorporation

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levels; porcini mushroom substitution showed no obvious difference from the control

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(Fig. 2-supplementary). Previously research illustrated differences in protein and

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carbohydrate affects moisture, molecular gelatinisation, starch degradation, and the

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textural quality of product (Korkerd, Wanlapa, Puttanlek, Uttapap, & Rungsardthong,

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2015). Inclusion of high amounts of protein and dietary fibre into extruded products

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increase hardness (Korkerd et al., 2015), as observed in the results of the white

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button mushroom samples. Crunchiness was inversely correlated to hardness (Table

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3, r=-0.973, at p≤0.001). Table 3 demonstrates positive correlations between

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crunchiness and expansion (r=0.620, p≤0.001), radial expansion (r=0.613, p≤0.001)

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and specific length (r=0.399, p≤0.05).

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3.4 Colour

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Table 1-supplementary illustrates that the lightness/darkness (L*) of some of the

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mushroom enriched samples decreased significantly (p≤0.05) compared to the

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control. The lower L* values may due to the reduced expansion and porosity due to

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moisture retention induced by increased fibre content of the extrudates instead of

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chemical reactions (Yu, Ramaswamy, & Boye,

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yellowness (b*) values increased compared to the control, possibly due to the higher

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protein levels in the formulations and the effects of protein degradation. All three

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mushroom samples provided more protein to the final products than semolina

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(semolina [11.32 ± 0.28 %]; white button [30.52 ± 0.13 %]; shiitake mushroom [15.04

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2013). Both the redness (a*) and

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± 0.04 %] and porcini mushroom [23.83 ± 0.19 %] on a dry weight basis).

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Furthermore, the other factors involved in these colour differences may be the

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Maillard reactions during the hot extrusion process or the oxidation of mushroom fat

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under thermal treatment.

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3.5 Thermal properties

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The ∆H values of most of the products were zero, indicating that the hot extrusion

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treatment resulted in complete starch gelatinisation or dextrinization, and protein

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denaturation (no peaks) (Ai, Cichy, Harte, Kelly, & Ng, 2016) (Table 2-supplementary).

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A negative correlation existed between ∆H and starch content (r=-0.597, p≤0.001).

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In addition, the 10 %, 15 % shiitake mushroom and 15 % porcini mushroom enriched

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samples had low ∆H values. These results showed a similar trend to that of the total

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dietary fibre contents in semolina and the other mushroom powders. Positive

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correlations were observed between ∆H and IDF (r=0.739; p≤0.001), SDF (r=0.550; p

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≤0.01) and TDF (r=0.803; p≤0.001). Research had previously shown correlations

325

between the inclusion of insoluble dietary fibre and an increase of DSC parameters

326

(Aravind et al., 2012). This is similar to our observations.

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3.6 Total phenolic contents and antioxidant capabilities

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The total phenolic content and antioxidant activities of the control and mushroom

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enriched extruded samples were studied (Fig. 1). The inclusion of mushroom powder

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into extruded snacks had a significant (p≤0.05) effect on increasing the total

332

phenolic contents and antioxidant activities of the samples. According to Fig. 1, the

333

results of the total phenolic contents and the DPPH and ORAC assays showed similar

334

trends. Table 3 illustrates positive correlations between TPC and both DPPH and

335

ORAC values (r=0.973 and 0.822, respectively; p≤0.001). The relationship between

336

the total phenolic contents of the samples and their antioxidant activities agreed

337

with several earlier reports (Jaworska, Pogon, Skrzypczak, & Bernas, 2015). Edible

338

mushrooms have been proven to play an important role in protection against oxidant

339

stress and the inhibition of cancerous cells (like HT-29 cells) (Sanchez, Jimenez-Perez,

340

Liedo, 2015). The antioxidant properties of edible mushrooms were due to

341

phytochemicals such as gallic acid, ascorbic acid, tocopherols, flavonoids, carotenoids

342

and selenium (Jaworska et al., 2008). Furthermore, mushrooms are a good source of

343

ergothioneine. This sulfur amino acid could act as an antioxidant, and is present in

344

levels of up to 0.4-2.0 mg/g in dry mushrooms (Weigand-Heller et al., 2012). The

345

antioxidant activity of ergothinoeine is based on multiple mechanisms among which

346

the capability to scavenge free radicals was quite powerful. This may explain the

347

increased DPPH scavenging activity and oxygen radical absorbance capacity of the

348

mushroom enriched samples in this study. Positive correlations were observed

349

between fat content and TPC (r=0.520, p≤0.01), DPPH (r=0.581, p≤0.001) and

350

ORAC (r=0.784, p≤0.001). Table 3 also indicates that there were positive correlations

351

between antioxidant capabilities (DPPH and ORAC) and all IDF, SDF and TDF fibre 17

352

contents, even though no correlation was observed between ORAC and SDF.

353

According to Fig. 1, under the same substitution levels there were significant (p≤

354

0.05) differences between different species of mushroom enriched samples. The

355

different antioxidant components and other bioactive compounds of the different

356

mushroom species played important roles in this observation. In this study, positive

357

correlations existed between protein content and antioxidant activities, whereas

358

negative correlations existed between starch content and both DPPH and ORAC

359

values (Table 3). During hot extrusion processing the raw materials suffered from

360

high temperatures and this tended to decrease the total phenolics compounds and

361

antioxidant capacities of the samples because of the increased oxidation of the total

362

phenolics (Korkerd et al., 2015). Little work has been undertaken to study the effect

363

of hot extrusion on mushroom bioactivity, that the correlations reported in this

364

paper are valuable in understanding such relationships.

365

366

3.7 The starch content and in vitro digestibility

367

According to Fig. 2, the addition of mushroom powder into extruded products

368

lowered the starch contents compared to the control. With the increasing amounts

369

of mushroom powder, the starch content decreased gradually, as shown by the

370

results of the semolina and mushroom starch contents. Negative correlations were

371

observed between starch content and fat, protein, IDF and TDF contents (p≤0.001),

372

and this suggests that the higher protein, fat and dietary fibre contents of mushroom

18

373

materials diluted the starch within the mushroom enriched samples.

374

375

The reducing sugars released from mushroom enriched products over 120 min of in

376

vitro digestion were lower than that of the control. The concentration-time curve

377

(AUC) bar chart represented this trend more clearly (Figs. 2 and Fig.

378

3-supplementary), illustrating that with increased mushroom contents, the AUC

379

values of extrudates decreased significantly (p≤0.05). This observation could be

380

confirmed by the strong positive correlation between AUC and starch content

381

(r=0.826; p≤0.001) found in this study. Rapidly digested starch (RDS) is the starch

382

digested in the first 20 min, which rapidly increases the blood glucose levels (Englyst,

383

Kingman, & Cummings, 1992). According to Fig. 3-supplementary, all the mushroom

384

enriched snack samples (except at the 5 % substitution level) had lower RDS levels

385

compared to the control. Slowly digested starch (SDS) is the amount of starch

386

completely digested in 20 to 120 min in the human small intestine (Englyst et al.,

387

1992). Inclusion of mushroom powder reduced the SDS fractions of the hot extruded

388

products. Thus, the decrease in the predicted glycaemic response may be attributed

389

to the higher amounts of resistant starch (RS) in the mushroom enriched samples.

390

Previous research illustrated that when chestnut mushroom co-products were added

391

to hot extruded snack products a reduction in glucose was observed throughout the

392

digestion (Brennan, Derbyshire, Tiwari, & Brennan, 2012). According to Table 2,

393

mushroom enriched samples contained significantly higher contents of IDF and TDF

394

than control. Many authors have reported that fibre fractions were able to 19

395

encapsulate starch granules and prevent the penetration of enzymes; thus, inhibiting

396

the release of glucose (Brahma et al., 2016; Brennan et al., 2012; Brennan et al.,

397

2013). In addition, the viscous nature of the fibres possibly inhibited the activity and

398

efficiency of the digestive enzymes (Aravind et al., 2012; Brennan et al., 2013). These

399

observations are supported by the negative correlations observed between AUC and

400

IDF (r=-0.799; p≤0.001), SDF (r=-0.452; p≤0,05) and TDF (r=-0.833; p≤0.001) in

401

Table 3. Table 3 also demonstrates a negative correlation between AUC value and

402

protein content (r=-0.6; p≤0.001). It is possible that hot extrusion produced a very

403

close protein network and enhanced the entrapment of starch granules; thus,

404

reducing the activity of digestive enzymes. Previously, researches have also shown

405

that the interactions of lipids with other components may result in decreasing

406

susceptibility to digestive enzymes (Holm et al., 1983). Table 3 illustrates a similar

407

observation in that a negative correlation was observed between the AUC for the

408

predictive glycaemic index and the fat content of all the samples (r=-0.855; p≤

409

0.001).

410

411

3.8 The relationship between antioxidant activity and the

412

glycaemic response

413

The results of the glycaemic response of all snack products in this study showed an

414

inverse relationship with their antioxidant capabilities (Figs. 1, 2b and Fig.

415

3-supplementary), Table 3 further illustrates strong negative correlations between

20

416

AUC and DPPH (r=-0.686; p≤0.001) and ORAC (r=-0.776; p≤0.001). To be specific,

417

the addition of mushroom powder increased the antioxidant properties of the final

418

products and limited the release of reducing sugars. This observation may be

419

ascribed to the ability of the mushroom enriched samples to decrease oxidative

420

stress. Moraes et al. (2015) showed that the glycaemic response may be negatively

421

correlated to the phenolic compounds and antioxidant capacities. This phenomenon

422

may due to the effect of the phenolic components on enzyme inhibition and starch

423

molecule interactions, that result in impaired starch digestibility and increased levels

424

of resistant starch (Mkandawire et al., 2013). The correlations illustrated in Table 3

425

advocate our understanding of such relationships to extruded snack products.

426

427

3.9. Scanning Electron Microscope (SEM)

428

The microstructure properties of control and mushroom enriched extrudates are

429

illustrated by SEM images presented in Fig. 4-supplementary. There was a more

430

continuous matrix of amorphous starch formation within the control sample

431

compared to mushroom enriched samples. The micrograph of mushroom enriched

432

samples indicate that gas cells were accumulated with the formation of large fissures

433

between cellular structures. Generally, Fig. 4-supplementary showed that individual

434

intact starch granules were not evident after suffering the hot extrusion. This agrees

435

with the DSC results, some starch molecules were not gelatinised in the 10 % and 15 %

436

shiitake mushroom extrudates (Table 2-supplementary). The image of 5 % white

21

437

button sample represented fibrous-lamellar structure, and 10 % white button and 5 %

438

shiitake mushroom samples obtained a rippled structure and the structural

439

orientation was random distributed with big fractures. This might play a role in their

440

higher crunchiness values than control. An ordered arrangement of cells and fibres

441

existed in the matrix of the 15 % white button mushroom extrudate, resulting in a

442

compacted and well-organized formation which in turn may have led to its highest

443

hardness value compared to other samples (Dar, Sharma, & Kumar, 2014).

444

445

4. Conclusion

446

Inclusion of mushroom powder into extruded snacks resulted in increased specific

447

length, water solubility index, energy value, fat and total phenolic content, while

448

decreased water absorption index, moisture and carbohydrate and total starch

449

content. Inclusion also reduced the degree of starch gelatinization and digestibility,

450

while improved the antioxidant activities of snack samples. All these changes were

451

correlated with the different inner structure alteration after the addition of

452

mushroom powder. In conclusion, hot extruded products incorporated with

453

mushroom powder could drastically provide more beneficial health influences.

454

455

Acknowledgements

456

This work was supported by Meadow Mushroom Ltd. in the supply of white button

22

457

mushroom material and the award of a student bursary to Xikun Lu.

458

459

Funding

460

This research received funding from the Ridett Institute, Palmerston North, New

461

Zealand, and the Tianjin Municipal Government, China, under a 1,000 expert

462

international talent project.

463

464

Declaration of interest

465

Declarations of interest: none.

466

467

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468

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Table 1. The processing parameters of hot extruded cooking Sample

Shaft speed (rpm) Feed rate Current Torque (g / min) (Amps) (Nm) CHE 200 20 5.53 56.5 5 % WBHE 200 25 5.77 60 10 % WBHE 200 25 5.98 64.5 15 % WBHE 200 25 5.95 61.7 5 % SHE 200 15 5.44 46 10 % SHE 200 15 4.92 42 15 % SHE 200 15 3.65 48.4 5 % PHE 200 25 6.04 70 10 % PHE 200 30 6.17 66.8 15 % PHE 200 30 6.22 62.8 Abbreviations: CHE=control hot extruded; WBHE=white button mushroom hot extruded; SHE=shiitake mushroom hot extruded; PHE=porcini mushroom hot extruded

Table 2. The nutrient components of hot extruded samples Sample

Energy kcal

Fat (g/100g DMB)

Carbohydrate (g/100g DMB)

Water (g/100g DMB)

CHE 5 % WBHE

355.33±1.53 e 357±0 e

0.37±0.058 e 1.1±0.1 d

78.73±0.50 a 78.2±0.36 a,b

7.13±0.25 b,c 7.13±0.15 b,c

Protein (g/100g DMB) 11.46±0.13 i 12.61±0.020

IDF (g/100g DMB) 2.44±0.19 d 3.00±0.097 c,d

SDF (g/100g DMB)

TDF (g/100g DMB)

2.65±0.045 a,b 2.27±0.30 b

5.09±0.15 e 5.27±0.21 e

2.49±0.18 b 2.24±0.10 b 2.42±0.44 b

6.94±0.34 c,d 7.47±0.15 b,c 5.96±0.60 d,e

e,f

360.67±0.58 c,d 364.67±0.58 a 359.67±0.58 d

10 % WBHE 15 % WBHE 5 % SHE

1.53±0.12 b,c 1.83±0.058 a,b 1.27±0.058 c,d

77.67±0.51 a,b,c 76.8±0.17 c 76.87±0.29 c

6.6±0.1 c,d 5.83±0.058 e 6.53±0.15 d

14.01±0.12 c 4.45±0.17 b,c 15.80±0.028 a 5.23±0.25 b 12.35±0.074 3.53±0.16 c,d e,f,g

10 % SHE 362±0 b,c 1.4±0.1 c,d 78.03±0.25 a,b 6.43±0.29 d 12.76±0.088 e 5.46±0.85 b 2.64±0.19 a,b 8.10±0.66 b,c 15 % SHE 363.33±0.58 a,b 2±0.1 a 78.13±0.47 a,b 6.6±0.1 c,d 12.52±0.11 e,f 8.00±0.21 a 2.94±0.25 a,b 10.93±0.46 a 5 % PHE 355.67±0.58 e 1.1±0.17 d 78.33±0.50 a,b 7.73±0.25 a 12.22±0.18 f,g 3.15±0.19 c,d 2.75±0.0032 a,b 5.90±0.20D e 10 % PHE 359.33±0.58 d 1.4±0.2 c,d 78.07±0.23 a,b 7.4±0.36 a,b 13.43±0.077 d 4.34±0.63 b,c 3.13±0.25 a,b 7.47±0.39B c 15 % PHE 361±0 c,d 1.6±0.1 b,c 77.6±0.26 b,c 7.17±0.12 a,b,c 14.58±0.22 b 5.23±0.49 b 3.62±0.44 a 8.85±0.057 b Mean ± standard deviation. Values within a vertical column followed by the same letter are not significantly different from each other (p < 0.05). Abbreviations: CHE=control hot extruded; WBHE=white button mushroom hot extruded; SHE=shiitake mushroom hot extruded; PHE=porcini mushroom hot extruded; IDF=insoluble dietary fibre; SDF=soluble dietary fibre; TDF=total dietary fibre.

Table 3. Pearson’s correlation coefficient (r) of physicochemical and nutritional properties of hot extruded products T

DPP

ORA

AUC

ST

EN

FT

PT

MS

DS

CRU

HAR

H

EXP

ER

Lsp

IDF

SDF

TDF

WAI

WSI

P C TPC

DPPH

ORAC

AUC

ST

EN

FT

PT

H

C

0.9 73* **

0.8 22* **

-0.6 71** *

-0.4 59*

0.41 7*

0.52 0**

0.76 3***

-0.2 8

0.8 36* **

-0.5 4**

0.54 8**

0.39 0*

-0.7 29** *

-0.7 12** *

0.13 9

0.34 4

0.6 26* **

0.46 6**

-0.7 53** *

0.06 9

0.8 82* **

-0.6 86** *

-0.4 59*

0.43 2*

0.58 1***

0.78 1***

-0.3 05

0.8 60* **

-0.5 06**

0.53 3**

0.31 3

-0.7 24** *

-0.7 08** *

0.15 8

0.36 9*

0.5 57* **

0.47 2**

-0.7 62** *

0.05 6

-0.7 76** *

-0.6 55** *

0.60 8***

0.78 4***

0.82 8***

-0.5 62** *

0.6 35* **

-0.1 3

0.15 6

0.30 1

-0.5 04**

-0.4 88**

0.27 2

0.53 1**

0.3 27

0.56 1***

-0.7 27** *

0.13 7

0.82 6***

-0.7 68** *

-0.8 55** *

-0.6 00** *

0.71 8***

-0. 336

-0.0 7

0.10 2

-0.5 57** *

0.59 3***

0.58 9***

-0.6 94** *

-0.7 99** *

-0. 452 *

-0.8 33** *

0.80 0***

-0.5 75** *

-0.9 06** *

-0.8 62** *

-0.5 72** *

0.91 0***

-0. 031

-0.3 61*

0.37 2*

-0.5 97** *

0.33 8

0.33

-0.7 21** *

-0.9 ***

-0. 223

-0.8 67** *

0.63 4***

-0.6 05** *

0.85 7***

0.66 9***

-0.8 91** *

0.0 32

0.26 2

-0.2 54

0.43 7*

-0.4 11*

-0.4 01*

0.72 4***

0.81 6***

0.0 25

0.74 2***

-0.5 39**

0.53 8**

0.63 3***

-0.8 10** *

0.1 83

0.27 8

-0.2 48

0.46 9**

-0.4 20*

-0.4 10*

0.66 0***

0.82 3***

0.1 52

0.78 ***

-0.6 15** *

0.50 3**

-0.5 13**

0.5 77* **

-0.3 08

0.34 1

0.11

-0.5 56** *

-0.5 34**

0.11 1

0.35

0.0 66

0.33 2

-0.4 69**

-0.0 93

MS

DS

CRU

HAR

H

EXP

ER

Lsp

IDF

0.1 36

-0.4 78**

0.46 6**

-0.5 24**

0.19 5

0.18 5

-0.7 54** *

-0.8 71** *

-0. 042

-0.7 96** *

0.52 3**

-0.6 00** *

-0.7 52** *

0.78 7***

0.03 5

-0.6 69** *

0.65 8***

-0.1 97

-0.0 49

0.4 84* *

0.07 7

-0.5 21**

-0.2 74

-0.9 73** *

0.24 9

0.62 0***

0.61 3***

0.39 9*

0.41 4*

-0. 318

0.29 4

0.09 5

0.47 4**

-0.2 3

-0.5 94** *

-0.5 83** *

-0.4 28*

-0.4 18*

0.2 71

-0.3 1

-0.1 04

-0.5 07**

-0.2 87

-0.2 85

0.64 9***

0.73 9***

0.5 50* *

0.80 3***

-0.7 00** *

0.64 8***

0.99 9***

-0.3 37

-0.3 78*

-0. 468 **

-0.4 58*

0.55 9***

-0.1 16

-0.3 42

-0.3 76*

-0. 472 **

-0.4 57*

0.55 3**

-0.1 23

0.88 8***

0.2 29

0.85 8***

-0.5 86** *

0.88 2***

0.2 78

0.97 1***

-0.6 94**

0.74 7***

* SDF

0.5* *

TDF

WAI

-0.6 54** *

0.34 5

-0.7 88** *

0.75 9***

-0.5 13**

TPC, mg GAE/g DM; DPPH, μM TE/g DM; ORAC, μM TE/g DM; AUC, In vitro area under the curve value; ST, Starch %; EN, Energy (kcal); FT, Fat %; PT, Protein %; MS, Moisture %; DS, Density g/L; CRU, Cruchiness/Number of peaks; HAR, Peak force/Hardness of product; H, △H J/g; EXP, Expansion; ER, Radial expansion ratio; Lsp, Specific length; IDF, Insoluble dietary fibre %; SDF, Soluble dietary fibre %; TDF, Total dietary fibre %; WAI, Water absorption index; WSI, Water solubility index. *, significant at p ≤ 0.05. **, significant at p ≤ 0.01. ***, significant at p ≤ 0.001.

Table 4. Physical and textural properties of extruded snack products Sample

% Expansion

ER

Lsp (mm/g)

CHE 5 % WBHE 10 % WBHE 15 % WBHE 5 % SHE 10 % SHE

394.9 ± 31.02 b,c,d 446.68±32.46 a 406.52±23.33 b,c 346.18±16.23 g 400.45±26.46 b,c,d 420.07±25.14 b

15.69±2.51 b,c,d 20.05±2.98 a 16.58±1.91 b,c 12.01±1.12 g 16.1±2.13 b,c,d 17.71±2.14 b

45.36±2.50 e 44.01±3.85 e 45.04±2.94 e 52.43±3.01 b,c 51±4.60 b,c,d 54.18±7.30 b

Product Density (g/l) 138.83±5.13 c,d 139.37±3.51 c,d 148.31±4.28 c 162.95±2.26 b 138.68±1.85 c,d 131.28±4.68 d

WAI (g/100g) 6.55 ± 0.41 a 6.31 ± 0.098 a,b 6.027 ± 0.22 a,b,c 5.71 ± 0.092 b,c,d 6.27 ± 0.18 a,b 5.61 ± 0.18 c,d

WSI (g/100g) 11.063 ± 1.029 e 11.21 ± 1.35 e 11.32 ± 0.37 e 12.018 ± 0.018 c,d,e 14.72 ± 1.16 b,c 17.49 ± 0.79 a,b

Moisture content (g/100g) 8.24±0.05 a 7.80±0.20 c,d 7.46±0.08 d,e,f 7.18±0.22 f,g 7.86±0.12 b,c 7.20±0.03 e,f,g

15 % SHE 375.45±19.62 d,e,f 14.13±1.48 d,e,f 60.97±4.85 a 135.01±2.45 d 5.31 ± 0.096 d,e 18.89 ± 0.59 a 6.96±0.18 g 5 % PHE 388.73±22.87 c,d,e 15.16±1.82 c,d,e 47.55±2.66 d,e 165.17±7.04 b 5.80 ± 0.051 b,c,d 11.48 ± 1.37 d,e 8.18±0.10 a,b 10 % PHE 366.3±25.28 e,f,g 13.48±1.81 e,f,g 50.27±3.08 c,d,e 167.41±1.61 a,b 5.42 ± 0.22 c,d,e 14.28 ± 1.08 c,d 7.74±0.03 c,d 15 % PHE 359.18±22.08 f,g 12.95±1.65 f,g 49.69±4.44 c,d 177.66±6.36 a 4.97 ± 0.28 e 14.40 ± 0.34 c 7.55±0.03 c,d,e Mean ± standard deviation. Values within a vertical column followed by the same letter are not significantly different from each other (p < 0.05). Abbreviations: CHE=control hot extruded; WBHE=white button mushroom hot extruded; SHE=shiitake mushroom hot extruded; PHE=porcini mushroom hot extruded.

(a) 8 a

7

mg GAE/ g DM

6 5

b

b

4 c

3

c

c

d e

2

e

f 1 0 CHE

5 % WBHE

10 % WBHE

15 % WBHE

5 % SHE 10 % SHE 15 % SHE 5 % PHE 10 % PHE 15 % PHE

(b) 4.5 a

4

µmol TE/g DM

3.5 b

b 3 2.5 2

c

cd

d

1.5

e

ef

1

f

0.5 g 0 CHE

5% WBHE

10 % WBHE

15 % 5 % SHE WBHE

10 % SHE

15 % SHE

5 % PHE

10 % PHE

15 % PHE

(c) 12

a a

10

µmol TE/g DM

b

b c

8

c

cd 6

d

4

e

2 f 0 CHE

5% WBHE

10 % WBHE

15 % WBHE

5 % SHE 10 % SHE 15 % SHE 5 % PHE 10 % PHE 15 % PHE

Fig. 1. Values for total phenolic component (TPC) (a); antioxidant capacities: the DPPH. scavenging activities (b); and the ORAC assay results (c). Comparing the control (CHE) to all mushroom powder enriched hot extruded samples: white button mushroom hot extruded products (WBHE); shiitake mushroom hot extruded products (SHE) and porcini mushroom hot extruded products (PHE). Error bars represent standard deviation of replicates. The same letter is not significantly different from each other (p < 0.05).

(a) 80 75

a

a

Starch % Dry Basis

b

bc

70

cd de

65

e

e

de f

60 55 50 45 40 CHE

5% WBHE

10 % WBHE

15 % WBHE

5 % SHE 10 % SHE 15 % SHE 5 % PHE 10 % PHE 15 % PHE

(b) 1100 a 1000

ab cd cd

AUC

900

bc

cde

de

cde e

e

800 700 600 500 400 CHE

5% 10 % 15 % 5 % SHE 10 % WBHE WBHE WBHE SHE

15 % SHE

5% PHE

10 % PHE

15 % PHE

Fig. 2. The total starch content (a) and values for area under the curve (AUC) (b). Comparing the control (CHE) to all mushroom powder enriched hot extruded samples: white button mushroom hot extruded products (WBHE); shiitake mushroom hot extruded products (SHE) and porcini mushroom hot extruded products (PHE). Error bars represent standard deviation of replicates. The same letter is not significantly different from each other (p < 0.05).

1. Incorporation of mushroom altered the physical and textural properties of hot extruded products. 2. Incorporation of mushroom increased the insoluble and total dietary fibre contents of final samples, whereas reduced the starch content of final products gradually. 3. Addition of mushroom limited the starch gelatinisation and digestibility of hot extruded products. 4. Addition of mushroom enhanced the antioxidant abilities of hot extruded snacks.

AUTHOR DECLARATION TEMPLATE

We wish to confirm that there are no known conflicts of interest associated with this publication and there has been no significant financial support for this work that could have influenced its outcome.

We confirm that the manuscript has been read and approved by all named authors and that there are no other persons who satisfied the criteria for authorship but are not listed. We further confirm that the order of authors listed in the manuscript has been approved by all of us.

We confirm that we have given due consideration to the protection of intellectual property associated with this work and that there are no impediments to publication, including the timing of publication, with respect to intellectual property. In so doing we confirm that we have followed the regulations of our institutions concerning intellectual property.

We understand that the Corresponding Author is the sole contact for the Editorial process (including Editorial Manager and direct communications with the office). He/she is responsible for communicating with the other authors about progress, submissions of revisions and final approval of proofs.

Professor Charles Brennan 08/07/2019