Functionality and nutritional aspects of microcrystalline cellulose in food

Carbohydrate Polymers 172 (2017) 159–174

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Carbohydrate Polymers journal homepage: www.elsevier.com/locate/carbpol

Review

Functionality and nutritional aspects of microcrystalline cellulose in food John Nsor-Atindana a,b , Maoshen Chen a , H. Douglas Goff c , Fang Zhong a,∗ , Hafiz Rizwan Sharif a , Yue Li a a State Key Laboratory of Food Science and Technology, School of Food Science and Technology, Jiangnan University, 1800 Lihu Avenue, 214122 Wuxi, Jiangsu Province, China b Department of Nutrition and Dietetics, University of Health Allied Sciences, Ho, Ghana c Department of Food Science, University of Guelph, Canada

a r t i c l e

i n f o

Article history: Received 30 November 2016 Received in revised form 21 March 2017 Accepted 9 April 2017 Available online 14 April 2017 Keywords: Microcrystalline cellulose Prebiotics Physicochemical properties Functional ingredient Dietary fiber

a b s t r a c t Microcrystalline cellulose (MCC) is among the most commonly used cellulose derivatives in the food industry. In order assess the recent advances of MCC in food product development and its associated nutraceutical implications, google scholar and database of journals subscribed by Jiangnan university, China were used to source literature. Recently published research articles that reported physicochemical properties of MCC for food application or potential application in food and nutraceutical functions were reviewed and major findings outlined. The selected literature reviewed demonstrated that the material has been extensively explored as a functional ingredient in food including meat products, emulsions, beverages, dairy products, bakery, confectionary and filling. The carbohydrate polymer also has many promising applications in functional and nutraceutical food industries. Though widely used as control for many dietary fiber investigations, MCC has been shown to provide positive effects on gastrointestinal physiology, and hypolipidemic effects, influencing the expression of enzymes involved in lipid metabolism. These techno-functional and nutraceutical properties of MCC are influenced by the physicochemical of the material, which are defined by the raw material source and processing conditions. Apart from these functional properties, this review also highlighted limitations and gaps regarding the application of material in food and nutritional realms. Functional, Nutritional and health claims of MCC. © 2017 Elsevier Ltd. All rights reserved.

Contents 1. 2.

3.

4.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160 Preparation and structure of particles of cellulose microcrystals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 160 2.1. Cellulose (raw material) sources . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 2.2. Preparation of particles of microcrystals . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 2.3. Chemical structure and morphology . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 161 Critical material attributes of microcrystalline cellulose as related to functionality . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164 3.1. Degree of polymerization, molecular weight and degree of crystallization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 164 3.2. Particle size and shape . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165 Techno-functional properties of MCC in processed food . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165 4.1. Emulsion, suspension and foam stabilization . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 165

Abbreviations: CMC, carboxymethyl cellulose; DP, degree of polymerization; GIT, gastrointestinal tract; GRAS, generally regarded as safe; HDL, high density liproprotein; LDL, low density liproprotein; LODP, level of degree of polymerization; MCC, microcrystalline cellulose; NCC, nanocrystalline cellulose; ND, not detected; O/W, oil in water; SCFA, short chain fatty acids; SEM, scanning electron microscope; TBA, total bile acids; TEM, transmission electron microscope; Tg, glass transition; TG, triglyceride; VLDL, very low density lipoprotein. ∗ Corresponding author. E-mail address: [email protected] (F. Zhong). http://dx.doi.org/10.1016/j.carbpol.2017.04.021 0144-8617/© 2017 Elsevier Ltd. All rights reserved.

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5.

6. 7.

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4.2. Fat substitutes or replacers and bulking agent . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 4.3. Wall material for encapsulation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 4.4. Reinforcement of edible films . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 167 Nutritional and health benefits of microcrystalline cellulose . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168 5.1. Hypoglycemic and hypolipidemic effects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 168 5.2. Prebiotic effect . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170 5.3. Bowel movement and constipation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170 5.4. Obesity management . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170 Gaps and implications for future research . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 170 Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171 Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171 References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 171

1. Introduction Cellulose, the earth’s most abundant natural material, is a long chain carbohydrate polymer of repeating glucose units. Structurally, parent cellulose has both amorphous and crystalline regions. Isolation of the later is achieved by chemical, mechanical, and biological means to produce a number of functional ingredients in the form of cellulose crystals with variable shape and size, including microcrystalline cellulose (MCC), microfibrillated cellulose, nanocrystalline cellulose, nanofibrillated cellulose and bacterial cellulose, based on the preparation techniques and sources (Habibi, Lucia, & Rojas, 2010). Although significant progress has been made towards commercialization of the various forms of the crystalline cellulose, only MCC has been successfully commercialized and produced in a powdered form or co-processed with a hydrophilic dispersant to yield a colloidal form (Jia et al., 2014). MCC is a porous, aggregate, white, odorless, impurity-free crystalline powder (Hamid, Chowdhury, & Karim, 2014). It is characterized by lower degree of polymerization when compared with the starting material (Leppänen et al., 2009). The crystallinity of MCC depends largely on the degree of crystallinity of its starting material and processing technology. The application areas of MCC are huge, encompassing many industrial sectors such as food, pharmaceutical, cosmetics, cement, and plastic industries. Consequently, the global market for MCC, particularly in North America has witnessed tremendous growth with positive future prospects. In 2015, a report by Transparency Market Research Analysis indicated that the global market for the MCC is expected to reach $1.08 billion USD by 2020, with the pharmaceutical and the food sectors as the biggest beneficiaries. Thus, in terms of value, its market is expected to witness a compound annual rate of growth of 7.2% between 2015 and 2020. This stems from the fact that MCC is non-toxic, physiologically inert, renewable and biodegradable. Additionally, micro/nano-scale particles of crystalline celluloses have unique physicochemical properties, offering the material excellent functional properties such as rheological, thermal and mechanical characteristics (Hamid et al., 2014). Generally considered as safe (GRAS), several studies have demonstrated that MCC has gained recognition and applications within the food industry beyond its original role as a dietary fiber. MCCs have been used in dairy products, baked foods, desserts, sausage, frozen food and other food systems as a bulking agent. Their presence in these products gives better consistency, mouthfeel and other organoleptic properties (Imeson, 2010; Schuh et al., 2013; Thoorens, Krier, Rozet, Carlin, & Evrard, 2015). Additionally, several studies have been published regarding the use of the material to produce edible films, act as stabilizers and emulsifiers in emulsions among others (Alves, dos Reis, Menezes, Pereira, & Pereira, 2015; Boluk, Lahiji, Zhao, & McDermott, 2011; Kalashnikova, Bizot, Cathala, & Capron, 2011; Onyango, Unbehend,

& Lindhauer, 2009; Paunonen, 2013; Pereda, Amica, Rácz, & Marcovich, 2011; Tang et al., 2013; Zhao, Kapur, Carlin, Selinger, & Guthrie, 2011). MCC has also received attention in the nutritional and functional foods realms. According to FMC health and nutrition department, Powdered and colloidal MCC are reported to contain 93 g and 98 g of insoluble dietary fibers, respectively, per 100 g. Despite its approval for use in food as dietary fiber additive (Ghanbarzadeh, Almasi, & Entezami, 2010), reports of studies on the nutraceutical functions of MCC are inconsistent, unlike many other soluble dietary fibers. Some studies have reported reducing cholesterols levels in experimental animals fed with MCC fortified diets (Adel & El-shinnawy, 2012; Hongjia et al., 2015; Imeson, 2010; Lu, Gui, Guo, Wang, & Liu, 2015). In general, the physicochemical properties, which define functionality of MCC, are determined by both the raw material and the preparation technique (Qiang, Zhang, Li, Xiu, & Liu, 2016). In this regard, the scientific community has extensively investigated the material as demonstrated by the increasing number of research contributions in form of original research articles and patents (Adedokun et al., 2014; de Souza Lima & Borsali, 2004; Elsakhawy & Hassan, 2007; Imeson, 2010; Kalashnikova et al., 2011; Kopesky, Camden, Ruszkay, & Hockessin, 2006; Nguyen, 2004; Pachuau, Vanlalfakawma, Tripathi, & Lalhlenmawia, 2014; Schuh et al., 2013; Thoorens et al., 2015; Wanrosli, Rohaizu, & Ghazali, 2011) focused on describing the influence of preparation techniques as well sources of MCC and impact on functionality in food product development and nutritional claims. Though many research articles have demonstrated the functionality of MCC in food product development as well as the nutraceutical in the health realms, the available technical reports from suppliers of MCC and a book by Imeson (2010) on MCC mainly focused only the techno-functionality of the material in food. Moreover, the available recent reviews (Potu, Raja, Thimmaraju, & Neralla, 2013; Thoorens, Krier, Leclercq, Carlin, & Evrard, 2014) of research articles on the material largely focused on the functionality of MCC as an excipient in pharmaceutical industry, though new research findings on the material in food and nutritional perspectives have been reported in recent times. Therefore, this review presents a discussion on recent advances of the physicochemical properties and functionality of MCC in food product development. The paper also highlights the potential roles of the polysaccharide from nutritional and nutraceutical perspectives. Research gaps on the on the material have also been highlighted and discussed briefly in this paper.

2. Preparation and structure of particles of cellulose microcrystals MCC can be extracted from a variety of sources broadly categorized as plants and bacterial origins. Cellulose microcrystal types

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produced from a wide range of these two main sources have been investigated for myriad of commercial applications. Generally, the diversity of particles of microcrystals arises from two main factors: (i) the biosynthesis of the crystalline regions of the ␣-cellulose, which depends on the raw material source, and (ii) the extraction process and conditions. This section presents a brief description of the raw material sources, major commercial extraction techniques, the crystalline, morphological and chemical structure of MCC. 2.1. Cellulose (raw material) sources The raw materials are categorized into two groups; wood and non-wood sources. While the wood sources include hardwood, softwood and cotton linter (Nada, El-Kady, El-Sayed, & Amine, 2009), the non-wood sources are mainly lignocellulosic materials, especially agricultural residues. The raw material is characterized by a high molecular weight regardless of its source (Habibi et al., 2010). The chemical constituent (celluloses, hemicelluloses and lignin) of the raw material differs considerably in chemical proportions and structural organization; crystalline regions that are sandwiched by two amorphous regions. Moreover, the surface area, molecular weight, crystallinity, moisture content, and porous structure are influenced by the material origin (Ibrahim, El-Zawawy, Jüttke, Koschella, & Heinze, 2013; Kusumattaqiin & Chonkaew, 2015). Plants materials usually rich in ␣-cellulose (woody sources and cotton linters) are mainly used as the raw material for the production of the micro scale crystalline material because the cellulose strands are structurally arranged with layers of the cellulose chains bonded together by a cross-linking polymer (lignin) and strong hydrogen bonding (Chukwuemeka & Okhamafe, 2012; Osong, Norgren, & Engstrand, 2016; Thoorens et al., 2014). Apart from wood, other plants sources, mainly agricultural residues (i.e cellulose rich lignocellulosic biomasses), have been investigated as alternative sources (Table 1). Physicochemical properties of bacterial crystalline cellulose have also been studied (Jia et al., 2014; Kalashnikova et al., 2011). Unlike green plant sources, bacteria cellulose is pure and it requires no extensive processes for the removal of impurities such as lignin, pectin and hemicellulose (Lin et al., 2013). Therefore, MCC obtained from unlike sources would portray different physicochemical properties and performance. 2.2. Preparation of particles of microcrystals Preparation of microcrystalline cellulose from a raw material source entails two steps: i) the pretreatment (purification) step to obtain purified cellulose (the starting material for MCC production) and ii) the treatment of the purified cellulose to obtain MCC. The purification step is largely dependent on the type of raw material source of the cellulose. For example, the pretreatment for plants sources such as wood, partially or completely removes hemicellulose, lignin and other impurities to obtain pure cellulose fiber. The pretreatment of tunicate on the other hand isolates mantel from the animal, following which the cellulose fibers are isolated with the elimination of protein matrix (Moon, Martini, Nairn, Simonsen, & Youngblood, 2011). In the cases of algal and bacterial celluloses, culturing methods, and subsequent purifications are usually employed to eliminate the wall matrix, bacteria and the other media to obtain the starting material. Extensive works have been done detailing the description of these pretreatments to obtain pure cellulose for MCC production within the available references in the following: bacteria (Adedokun et al., 2014; Castro et al., 2011), wood (Okwonna, 2013; Rojas & Kumar, 2011), lignocellulosic materials/agricultural residues (eg, oil palm fruits bunch and front, banana stems hull, rice straw, corn husk/comb, bamboo, etc) (Azubuike & Esiaba, 2012; Murigi et al., 2014; Ngozi, Chizoba, & Ifeanyichukwu,

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2014; Xiang, Mohammed, & Samsu Baharuddin, 2016) algae (Jmel, Ben Messaoud, Marzouki, Mathlouthi, & Smaali, 2016) and tunicate ˇ (Sturcová, Davies, & Eichhorn, 2005). The second step basically involves the treatment of the purified celluloses to obtain MCC. Though many methods exist for the production of MCC, such as conventional acid hydrolysis (Kalita, Nath, Ochubiojo, & Buragohain, 2013), enzymatic technology (Anderson et al., 2014), mechanical techniques (Khalila et al., 2014), ionic method (Abushammala, Krossing, & Laborie, 2015) or combination of two or more of these techniques exist, the acid extraction method is the most common for commercial production of MCC due its relatively lower cost coupled with shorter duration of production (Abeer, Zeinab, Ibrahim, & Al-Shemy, 2011; Li, Zhang, Zhang, Xiu, & He, 2014). The main steps involved in a typical acid production process of MCC are illustrated in Fig. 1 and briefly discussed in the preceding paragraphs. For the acid hydrolysis technique, the acid causes the cellulose (usually purified/bleached pulp) to undergo partial depolymerization to form microcrystalline cellulose (Costa, Moris, & Rocha, 2011). The hydrolysis process is stopped when the desired level-off degree of polymerization (LODP) (Qiang et al., 2016; Vanhatalo & Dahl, 2014) is attained. The LODP is raw material specific and typically found in the 180–350 ranges, as in the cases of 180–210 range for hardwood pulps, 210–250 softwood pulps (Thoorens et al., 2014) and 182 for Bambusa vulgaris (Ngozi et al., 2014) as an example of non-wood biomass. Following acid treatment, the residual mass is neutralized and thoroughly washed to remove impurities. The wet mass is then dried to obtain MCC powder or mechanically wet milled and co-processed with a dispersing agent (Fig. 2) to prevent aggregation of the MCC individual particles after drying. Spray drying is a common technology for drying the wet matter, although alternative methods may be used (Gamble, Chiu, & Tobyn, 2011). Typically, less than 10% of the final product has particle size of less than 5 ␮m (Vanhatalo & Dahl, 2014). Different strong mineral acids, including hydrochloric acid, nitric acid, phosphoric acid, sulfuric acid and ammonium persulfate have been employed for selective hydrolysis of the amorphous regions (Chukwuemeka & Okhamafe, 2012; Follain, Marais, Montanari, & Vignon, 2010; Qiang et al., 2016; Tang et al., 2013). Hydrolysis involving the use of sulfuric acid often results in highly soluble particles with a charged surface of sulfate ester (Anderson et al., 2014). The intensity of the acid hydrolysis also affects final product particle size. Vanhatalo and Dahl (2014), observed that mild acid treatment produced broader particle size distribution, while small particles with a narrower particle size distribution were obtained under intensive acid treatment. Recent technological advances of MCC isolation and characterization has been discussed in detailed in the review of Trache et al. (2016). Bacterial cellulose has emerged as a green technology for the production of MCC. Unlike wood fiber and other plants parts fibers, cellulose obtained from bacteria is free from other contaminating polysaccharides and do not require energy and chemicals to isolate it, thereby elimination environmental problems arising from wood pulping. The technology has been described in details in the works of Keshk (2014), Moon et al. (2011) and de Oliveira et al. (2011). In the work of de Oliveira et al. (2011), they reported the properties of MCC obtained bacterial cellulose were similar to that commercial MCC and could be potentially commercialized. 2.3. Chemical structure and morphology Cellulose, the raw material of MCC, is a polysaccharide consisting of tens of thousands of glucose units linked together by ˇ-1, 4-glycosidic linkages to form a linear polymer. As a product of purified cellulose, MCC particles are also composed of glucose units

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Fig. 1. The overview of steps involved in the production of MCC by acid hydrolysis method. Adapted from Thoorens et al. (2015).

Fig. 2. Schematic presentation of microcrystals of cellulose co-processed with CMC.

Fig. 3. Chemical structure of microcrystalline cellulose.

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Table 1 Summary of studies on physiochemical properties of MCC extracted from different sources using different acids. xx means not reported by the authors cited. Source of Raw material

Acid type used

DP

CRI (%)

Properties studied

Reference

Waste paper

Book paper

H2 SO4

200

77.9

pH, porosity, density moisture sorption, viscosity, chemical structure, particle size

Okwonna (2013)

H2 SO4

196

76.9

Oil palm

Ground wood/newsprint Paper board Empty fruits bunch

H2 SO4 H3 PO4 /P2 O5 /Et3 PO4

186 xx

71.6 xx

Water swelling capacity, morphological structures, thermogravimetric analysis, rheological properties, binding

Wanrosli et al. (2011)

HCl

xx

82.2

Stalk

HCl

xx

82.5

Frond

HCl

86

71

Soybean hulls

H2 SO4

xx

70

Cotton: Linters

HCl/H2 SO4

79

77

Stalk Alfafa fiber

HCl/H2 SO4 HCl

xx 77

77 73

Corn/maize: Cob Husk

HCl, H3 PO4

xx

78

Kenaf fiber

HCl

310

68.6

Rice: Hulls

H2 SO4

151

82

Straw Bean: Hulls Mulli bamboo Indian bamboo

HCl, H2 SO4 HCl

xx 190

78 92

Banana stem Water hyacinth Papyrus reeds

CH3 CO3 H, HCl

xx

xx

Bagasse

HCl/H2 SO4

xx

76

Bamboo

HCl

182

xx

Green macro-algae Enteromorpha sp.

HCl

xx

36

linked together by ˇ-1, 4-glycosidic linkages to form a linear polymer chain of shorter length. Each glucose monomer in the polymer chain has three free hydroxyl groups on C2, C3 and C6 (Fig. 3), which define the chemical reactivity of the crystalline polymer. These reactive sites allow possible modification of the cellulose crystals into a number of functionalized materials for specific applications. Several studies devoted to modifying the structure of the cellu-

Particle size, crystallinity, dimension, chemical structure, water sorption capacity. Particle size, crystallinity, dimension, chemical structure, water sorption capacity. Molecular structure, DP, particle size, length, shape, water sorption, crystallinity, mechanical properties Molecular weight, crystallinity, fermentation

Molecular weight, crystallinity, fermentation Porosity, crystallinity, density, tableting, tensile, porosity, properties, moisture, heat stability Density, morphology, crystallinity, particle size and distribution, DP Mechanical properties, tableting properties, particle size, density (bulk density, tapped density, hausner ratio) particle size

Porosity, density (bulk density, tapped density, Hausner ratio), particle size, DP, viscosity, moisture, crystallinity, morphology, swelling capacity, tableting, and compressibility Density, (bulk density, tapped density, Hausner ratio), chemical structure, wettability, particle size, morphology DP, crystallinity index, crystallinity particle size, density (bulk density, tapped density, hausner ratio), and thermal stability Density (bulk density, tapped density, hausner ratio), solubility, color, swelling capacity tableting, etc Rheological properties moisture, crystallinity, chemical structure, etc

Hussin et al., (2016), Xiang et al. (2016) Mohamad Haafiz et al. (2013) Hussin et al. (2016)

Merci et al. (2015)

Nada et al. (2009), Rojas and Kumar (2011) Yang et al. (2010) Azubuike and Esiaba, (2012), Chukwuemeka and Okhamafe (2012) Wang, Shang, Song, and Lee (2010) Abeer et al. (2011), Ibrahim et al. (2013)

Ngozi et al. (2014), Pachuau et al. (2014)

Murigi et al. (2014)

Elsakhawy and Hassan (2007)

Ngozi et al. (2014)

Jmel et al. (2016)

lose to enhance its functionality have been reported (Bilbao-Sainz, Avena-Bustillos, Wood, Williams, & McHugh, 2010; Kalashnikova et al., 2011; Pereda et al., 2011; Schuh et al., 2013; Zhao et al., 2011). Table 2 displays the comparison of cellulose content, lignin content, DP, and crystallinity index of different starting materials and their respective resultant MCC. Various investigators have reported the crystalline structures of MCC as well that the starting materials

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Table 2 Characteristics of purified cellulose starting materials and their respective MCC: cellulose and lignin content, degree of polymerization (DP) and degree of crystallinity. Starting material and its MCC

cellulose content (mass %)

lignin contnent (mass %)

DP

Crystallinity index (%)

Reference

Birch Sulphite Pulp (BSP) MCC from BSP Coniferous Sulphite pulp (CSP) MCC from CSP coniferous kraft pulp (CKP) MCC from CKP Poplar kraft pulp (PKP) MCC from PKP Aspen kraft pulp (AKP) MCC from AKP Cotton linters (CL) MCC from CL Flax cellulose (FC) MCC from FC Avicel Bleached Rice Hull (BRH) MCC from BRH Bleached Bean hull (BBH) MCC from BBH Bacterial cellulose (BC) MCC from BC Vegetal Cellulose (VC) MCC from VC Oil palm front cellulose (OPFC) MCC from OPFC

95.8 97.3 96.2 98.8 97.8 98.6 96.4 97.6 96.8 97.5 98.5 99.8 97.9 99.6 99.9 91.8 xx 95.0 93.2 xx xx xx xx XX xx

1.4 0.5 1.3 0.4 1.1 0.5 1.2 0.8 1 0.6 0.7 0 1.2 0 0 3.8 0 1.0 0 xx xx xx xx XX xx

1600 175 1310 275 1135 150 1300 250 1250 230 220 165 470 170 150 407 151 336 190 2800 230 1300 170 174 86

52 54 58 59 50 63 xx 60 xx 63 xx 65 xx 60 59 80 82 87 92 76 69 79 88 47 71

Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Leppänen et al. (2009) Abeer et al. (2011) Abeer et al. (2011) Abeer et al. (2011) Abeer et al. (2011) de Oliveira et al. (2011) de Oliveira et al. (2011) de Oliveira et al. (2011) de Oliveira et al. (2011) Hussin et al. (2016) Hussin et al. (2016)

xx means not reported by the authors.

(Abeer et al., 2011; de Oliveira et al., 2011; Leppänen et al., 2009) using X-ray diffraction technology. The literature reviewed in this paper noted that the crystallinity index of MCC is only marginally higher than that of the native starting cellulose by 1%–15% (Table 2). It is believed that the slightly higher crystallinity in MCC is due to the partial removal of the amorphous parts of native cellulose during the hydrolysis process, which promotes the hydrolytic cleavage of the glycosidic bonds, and causes the reorganization of the cellulose polymer chains (Adel & El-shinnawy, 2012; Leppänen et al., 2009; Mohamad Haafiz, Eichhorn, Hassan, & Jawaid, 2013). The morphology of MCC obtained from different sources such as cotton, wood, rice straw, bean hull, alfalfa fiber, oil palm front, empty palm fruit bunch, rice hull, bean hull, and commercial MCC (Fig. 4) are somewhat similar (Abeer et al., 2011; Mohamad Haafiz et al., 2013; Nada et al., 2009; Wanrosli et al., 2011). However, surface morphology of the material may change in terms of size and level of smoothness (Trache et al., 2016). SEM and TEM analysis of MCC obtained from variety of sources revealed the presence of rodlike or needle-like aggregates of particles, and further analysis of these particles showed that they could be of varied particle size and shape (Abeer et al., 2011; Castro et al., 2011; Habibi et al., 2010). Thus, MCC is distinguished from native purified starting material by the measure of its DP (usually less than 400 glucose units) (Vanhatalo & Dahl, 2014). The detailed morphological structure and architecture of MCC compared with wood and other starting raw materials have been discussed in the reviews of the following reference: (Habibi et al., 2010; Leppänen et al., 2009; Moon et al., 2011; Qiang et al., 2016). Apart from the raw material, the extent of processing significantly defines the chemical composition and the morphological characteristics (Hamid et al., 2014). Although MCC is made up of water-soluble glucose units, it is poorly soluble in aqueous media due to its crystalline structure. The crystallinity is due to an ordered array of tightly packed linear glucose polymers connected with intra- and intermolecular hydrogen bonds (Takahashi, 2009). According to Hamid et al. (2014) the degree of crystallinity achieved following hydrolysis of the parent cellulose is a very important attribute of the polymer because it defines and influences several characteristics of the material.

3. Critical material attributes of microcrystalline cellulose as related to functionality The following parts summarize studies on MCC and highlight some critical material attributes relevant for food applications. These attributes are broadly categorized under the following: degree of crystallinity, degree of polymerization and molecular weight, particle size and shape, mechanical properties, thermal stability, porous structure, surface area and moisture content characteristics. 3.1. Degree of polymerization, molecular weight and degree of crystallization The literature reviewed on the effects of DP on some physicochemical properties showed that correlation of DP with physicochemical properties would only be true provided that the material is procured from the same source and produced with the same processing conditions. There was a significant correlation between DP and compressibility, compactibility and particle size when mechanical and physical properties of MCC powders produced from the same material with varying DPs were studied (Kleinebudde, Jumaa, & Saleh, 2000; Zeug, Zimmermann, Röder, Lagorio, & San Román, 2002). However, there was no apparent correlation between DP and mechanical properties when a study on the mechanical properties of MCC powders with varying DP produced from unlike sources were studied (Elsakhawy & Hassan, 2007). The influence of DP also impacts on other physicochemical properties of MCC. For example, higher DPs of the cellulose have been reported to show higher water holding capacity when compared to those with lower DPs (Zeug et al., 2002) probably due to the relatively large number of hydroxyl groups in bigger DPs, which make them more hygroscopic (Thoorens et al., 2014). Moreover, such larger DP MCC solid particles would likely be less crystalline due to presence of more amorphous regions, which are more hygroscopic, compared to shorter DPs. Similarly, the study indicated that positive correlations existed between DPs and storage properties (bulk and tapped densities) of the MCC powders. The bulk and tapped

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Fig. 4. SEM of three different avicel pH MCC taken at the same magnification. Images adopted from FMC (Reier, 2000).

densities affect Hausner’s ratio, which is used to measure flowability of food powders. These properties exhibited by the powders due to the influence of DP are relevant during its selection for use as anti-caking agents or hygroscopic agents in food systems. Generally, anti-caking agent should have good powder flowability with no or minimal adhesion among the individual particles. The degree of crystallization, a distinctive feature of MCC relative to the parent cellulose, is very important due to its influence on many properties, including stabilizing capacity for suspension and emulsion, thermal properties and hydration capacity of MCC particles. According to Chukwuemeka and Okhamafe (2012), these properties impact the flow capacity of the cellulose crystals during its use as excipients or ingredient in the final pharmaceutical or food products. In their study of the effects of carrier types (waxy starch, maltodextrin and Arabic gum) with MCC and concentration on solubility and glass transition temperature (Tg) of pomegranate juice powder, Yousefi, Emam-Djomeh, and Mousavi (2011) observed that both solubility and the Tg were greatly influenced by the addition of MCC. The crystalline cellulose induced its insolubility property on the spray dried pomegranate juice powder and significantly reduced the solubility of all samples due to the MCC ordered array of tightly packed linear glucose polymers connected with intra- and intermolecular hydrogen bonds (Takahashi, 2009). Tg temperature of the pomegranate juice powder samples with waxy starch, maltodextrin and Arabic gum increased from 25.1, 40.0, and 52.8 ◦ C respectively to 48.0, 59.9 and 77.0 ◦ C in the same order when 3% of MCC was added to each samples (Yousefi et al., 2011). MCC is generally known for its good thermal properties due to its crystalline nature. The degradation temperature is proportional to the degree of crystallinity (Kalita et al., 2013). The increase in Tg temperature of the pomegranate juice powder samples with MCC as a secondary carrier, induced its thermal properties on the powder and caused the decomposition temperature to change. The higher Tg temperatures induced by the presence of the crystalline cellulose points to more stable powders during production and, storage. Thus, the presence of MCC in a food system ensures that there is minimal breakdown of products at high temperatures during processing. The addition of MCC decreased the stickiness of mango juice powders due to the creation of crystalline surfaces caused by the presence of the crystalline cellulose (Cano-Chauca, Stringheta, Ramos, & Cal-Vidal, 2005). Wang and Zhou (2015) also reported a reduced stickiness of soy sauce powder when MCC was added to samples prior to spray drying because the presence of the crystalline cellulose induced its crystalline property on the soy sauce powder. According to the authors, XRD analysis showered an increased crystallinity of the spray dried soy sauce powder with the crystalline cellulose.

3.2. Particle size and shape Flow properties of powders are influenced by particle size, shape and other characteristics. Studies on the effects of particle size and shape on flowability of some powders including MCC powders have been reported (Gamble et al., 2011; Horio, Yasuda, & Matsusaka, 2014; Mellmann, Hoffmann, & Fürll, 2013). Commercially, grades of highly functional MCC powders have been developed to enhance these flow properties. MCC powders with spherical and porous structure exhibit better compressibility and enhanced powder flowability (Horio et al., 2014). The particle populations of the polymer comprise a mixture of ‘rod like’ primary particles and agglomerates, and contribute to the bulk properties of these materials (Gamble et al., 2011). ® The particle size of the commercial grade MCC, Avicel P101 which was originally 50 ␮m, had high compatibility but often exhibited poor flow property (Rowe, Sheskey, Cook, & Fenton, 2006). By using alternative techniques to deal with the issue, different Avicel grades of MCCs: pH 102 with mean particle size of 100 ␮m and pH 200 with particle size of 180 ␮m (Fig. 4), having enhanced flow properties while retaining majority of the functionality of the parent material have been introduced into the market (Gamble et al., 2011). Apart from increasing the particle size of the material, alternatives techniques have been used to improve bulk properties of MCC powders. The use of raw material with enhanced densities or co-processing techniques and variation of spray drying techniques can be employed. Particle size and shapes of MCC also critically influence the rheological and other functional properties of cellulose. The critical material attributes including the crystallinity, DP, particles and shapes are discussed in detailed in the preceding sections under techno-functional properties of MCC in processed foods. 4. Techno-functional properties of MCC in processed food Several grades of MCC with different properties are applicable to various processed food systems (Table 3). Texture, taste and other organoleptic properties of food decisively influence the choice and acceptance of food product. 4.1. Emulsion, suspension and foam stabilization In general, crystals of cellulose within micro/nano-scale dimension (MCC/NCC) by virtue of their amphipathy are able to stabilize emulsions since the presence of the free hydroxyl groups on the material surface acts as hydrophilic points, while the crystalline portion could function as the hydrophobic edge, giving overall amphiphilic character (Kalashnikova et al., 2011). These particle-stabilized emulsions are termed ‘Pickering’ emulsions.

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Table 3 Application and functonality of MCC in different processed food systems. Food system/product

MCC functions

Reference

Bakery and confectionary fillings toppings

Improve rheological and sensory properties of dough and baked products. Also act as fat replacer in low calorie baked products. Enhancement of dough textures, taste and other sensory properties of the final product Acted as fat replacer (Improve texture, moisture retention and mouth feel, reduced lightness and tenderness) Improvement of the stability of suspensions, creaminess and particle suspensions Thickening agent, crystallization of ice in ice creams, stabilization of the foam Reduction of the stickiness of powdered sauce, prevention of caking of powdered sauce Thickens and enhance the viscosity and stability of emulsions Steric hindrance Enhancement of the mechanical properties of films and coatings

Correa et al. (2010), Gómez et al. (2010), Onyango et al. (2009)

Meat product (beef sausage) Beverages (e.g., cocoa drinks) Dairy products, (e.g., ice creams, frozen desserts, processed cheese) Dressings, sauce and spreads Emulsions/dispersions Edible films and coatings Probiotics and encapsulated foods Soybean protein hydrolysates

Encapsulation/entrapment bacteria within the MCC matrix to ensure delivery to the colon Improvement of the microrheological properties of the products

The mechanism of stabilization is based on particle shape, size, and partial dual wettability defined by crystallinity (Capron & Cathala, 2013; Hu, Ballinger, Pelton, & Cranston, 2015). Two major mechanisms have been put forward for the stabilization of particlestabilized emulsions. Firstly, the solid particles can be irreversibly (Tavernier, Wijaya, Van der Meeren, Dewettinck, & Patel, 2016) adsorbed at the interface creating a layer around the emulsion droplets to prevent their coalescence (Dickinson, 2013). For the second mechanism, stabilization of particle-stabilized emulsion can be achieved by the formation of two or three dimensional networks (Winuprasith & Suphantharika, 2015; Xu, Zhang, Cao, Wang, & Xiao, 2016). MCCs are good candidates for interfacial stabilization, particularly for food use due to their nontoxicity, sustainability, biodegradability and renewability in addition to excellent native physiochemical properties including large elastic modulus and high aspect ratio (Boluk et al., 2011; Kalashnikova et al., 2011; Winuprasith & Suphantharika, 2015). Kalashnikova et al. (2011) previously demonstrated that cellulose microcrystals in the absence of a dispersing agent could effectively stabilize o/w emulsions for several months by the Pickering mechanism of stabilization provided the particles are properly dispersed. Similarly, cellulose crystals in nano scale dimension obtained from asparagus by sulphuric acid hydrolysis were used to successfully form stable Pickering emulsions for several weeks in a palm oil/water (30/70, v/v) model solution (Wang et al., 2016) Colloidal MCC (11% MCC combined with 1% sodium carboxymethylcellulose) have also used to stabilize oil-in water (O/W) emulsion and water-in-oil-in water (w/o/w) multiple emulsions via a formation of a network around the emulsified oils (Jia et al., 2014; Oza & Frank, 1989). MCC in such systems functions to orientate at the oil-water interface thereby offering mechanical barrier to oil droplet coalescence (Dickinson, 2013), while the other material in the system mainly acts as a dispersing and protective colloid for the MCC (Jia et al., 2014). Colloidal MCC not only thickens the continuous phase between the droplets, but also effectively builds a weak three-dimensional network anticipated to stabilize the emulsions (Winuprasith & Suphantharika, 2015; Xu et al., 2016). However, the strength of the networks formed by the cellulose depends on its aspect ratio, which is invariably defined by the particles size and shape. Microfibrillated cellulose by virtue of its high aspect ratio reportedly formed strong entangled disordered networks in contrast to low aspect

Brewer (2012), Gibis et al. (2015), Schuh et al. (2013) Imeson (2010), Yaginuma and Kijima (2006b) Nawar, Hassn, Ali, Kassem, and Mohamed (2010), Soukoulis et al. (2009) Wei and Zhou (2015) Imeson (2010), Winuprasith and Suphantharika (2015) Alves et al. (2015), Paunonen (2013), Tang et al. (2013), Wang et al. (2013) de Barros et al. (2015), Harel and Tang (2014) Xu et al. (2016)

ratio MCC, which created feebly bonded networks (Pääkkö et al., 2007). Suspensions of MCC are shear-thinning and thixotropic but the extent differs according to the raw material source and the preparation technology. For instance, suspension of MCC produced by HCl hydrolysis was more shear-thinning compared with sulphuric acid hydrolysis MCC suspension. While the former is thixotropic at concentrations greater than 0.5% (w/v), the latter is not (Araki, Wada, Kuga, & Okano, 1998) due to the introduction of sulphate charges on the surface of the MCC particles prepared with sulfuric acid (Tang et al., 2013). In products such as cocoa beverages, the presence of MCC in the systems improved creaminess and stability of the suspension because the MCC particles associated with other particles in the system to form poorly or highly aggregated structures including network structures (Araki et al., 1998; Yaginuma & Kijima, 2006a). In a recent study involving the use of MCC in active pharmaceutical ingredient nanocrystal suspensions for spray drying, it was realized that the polymeric dispersant was not only able to prevent the aggregation of the nanocrystals in the suspensions state but also eliminated agglomeration throughout the spray drying process (Dan et al., 2016). The authors explained that MCC in water forms “charged network” structure, which adsorbs the active ingredients onto its surface and prevents them (the active pharmaceutical ingredients) from particle–particle associations and agglomerations. At pH below 3 MCC exhibits solid-like behavior due to the formation of the three-dimensional network structures of the aggregates via non-electrostatic and electrostatic interactions (Yaginuma & Kijima, 2006b). Tang et al. (2013) reported that micro or nanocrystalline cellulose produced using sulfuric acid hydrolysis led to the formation of stable suspensions in water due to the formation of surface charges on the final crystalline material. In using both sulfuric and hydrochloric acids to produce cellulose crystals from the same source, it was observed that the products obtained by sulfuric acid treatment had negatively charged surfaces, due to the introduction of O-SO3 during the acid treatment, while the sample treated with hydrochloric acid did not have charges on the surfaces (Tian et al., 2016). Moreover, the researchers noted that the zeta potential values of the charged cellulose increased with both sulphuric acid concentration and treatment time. Accordingly, stability of the cellulose suspension improved with increasing reaction time and acid concentration. In foam based food products, materials with amphipathic characteristics are commonly employed to stabilize the system due

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to the ability of such ingredients to undergo flexible activation of their lyophilic and lyophobic groups. MCC is a promising material for foam systems stabilization due to its amphipathicity, and large elastic modulus. The utilization of MCC in foam system demonstrated improvement in stand-up ability, stiffness, and stability of ice cream (Soukoulis, Lebesi, & Tzia, 2009), bread and dough ˜ Pérez, & Ferrero, 2010; Majzoobia, Farahnaky, & (Correa, Anón, Ostovan, 2007; Onyango et al., 2009) and cakes (Gómez, Moraleja, Oliete, Ruiz, & Caballero, 2010). The physical and textural characteristics of cake showed similar results when six different fibers including MCC were investigated for the particle size effect on cake quality (Gómez et al., 2010). Ice creams are complex food systems and often require low levels of stabilizers (usually 0.1–0.5%) to achieve good stability and other relevant functions (Bahramparvar & Tehrani, 2011). Polysaccharides including MCC been recognized as good stabilizers of ice creams and its roles in ice creams have been discussed in detailed by some authors (Bahramparvar & Tehrani, 2011; Glicksman, 1986). MCC may be used alone or in combination with other polysaccharides in ice cream to achieve specific functions including stability and ice rheology. MCC gel has successful applications in ice cream stabilization and overrun control (Goff & Caldwell, 1991). In order to maintain the original structure of ice creams during storage and distribution, the incorporation of 0.4% of MCC to ice cream caused a gel to form and also improved the ice cream resistance to heat shock via the maintenance of the three-phase system of air–fat–water in the product (Glicksman, 1986). In corporation of MCC in ice creams also allows the increase of solid content of the product as well as a source of dietary fiber for consumers.

4.2. Fat substitutes or replacers and bulking agent MCC has been successfully used as fat substitute or replacer in some selected food systems. Prior to use, the material is often dispersed into aqueous medium and used to simulate fat in food system. A significant amount of work has been conducted to reduce the amount fats in ground meat, frozen desserts, dairy and baked products (Table 3). By virtue of its insoluble nature in water, the use of MCC as fat replacement or substitution in food systems reportedly produced excellent results. Gibis, Schuh, and Weiss (2015) observed that MCC could effectively replace up to 50% fat compared to standard product when they studied the effect of MCC as a fat replacer on microstructure and sensory properties of fried beef patties. The authors also noted that sensory evaluations of the MCC-based beef patties exhibited fat-like mouthfeel and were generally acceptable to the panelists. In the fried beef patties, it was observed heated samples with MCC had more juiciness than control and so had better fat-like mouthfeel (Gibis et al., 2015). The authors explained that since MCC is largely crystalline with no net charge, it formed particle gel network as an inert molecule and filled the gaps of the tight meat fiber network and MCC particles may not cause any disturbance of the protein network during heating. In emulsified sausage, the cellulose microcrystals positively impacted on the mechanical properties of the product by enhancing the firmness of the final product due to its high compactibility in the meat matrix (Schuh et al., 2013). Apart from meat, MCC has also been used to replace fats in emulsions, baked products, frozen desserts, mayonnaise, gravies and sauce. For instance, a 60% of soybean oil emulsion had similar stability characteristics and rheological properties as a 20% soybean oil emulsion containing 1–1.5% colloidal MCC (Imeson, 2010). Replacement of fat with MCC gives a rich creamy texture in low fat sauces and dressings because the material is insoluble and can mimic fat.

167

4.3. Wall material for encapsulation Nedovic, Kalusevic, Manojlovic, Levic, and Bugarski (2011) have reported the use of carbohydrate polymers as wall materials for encapsulation, because they are edible, biodegradable and able to form a barrier between the core and surroundings. de Barros, Lechner, Charalampopoulos, Khutoryanskiy, and Edwards (2015) reported improved survival of probiotic cells during extrusion/spheronization as well as excellent protection from gastric acid, when they fabricated MCC calcium cross-linked alginate as the wall material. The researchers also observed that efficient sphere disintegration and rapid release of the probiotics in intestinal conditions could be achieved with the combination of MCC and sodium alginate. Apart from protection of probiotics, other food bioactive components such as essential oils and volatile compounds could be encapsulated to protect them from degradation and evaporation. MCC could produce coats to provide protection for the sensitive bioactive food components against moisture, oxygen, light and temperature due to their barrier effects (Shokri & Adibkia, 2013). Koupantsis, Pavlidou, and Paraskevopoulou (2014) reported good shell formation with good protective ability of essential oils when they investigated the complex coacervation of milk proteins using carboxymethylcellulose (CMC) and MCC as the wall materials. Sometimes a native material/hydrocolloid may be modified for use as a wall material for encapsulation. For instance, during comparative study of different carriers on properties of spraydried rosemary essential oil, Fernandes, Borges, and Botrel (2014) reported that modified starch and inulin could be a good substitute for gum arabic. It is therefore important to note that since MCC is a hydrocolloid with multiple hydroxyl groups, it could be modified for use as a wall material. The surface charges of MCC produced with sulfuric acid could be ideal for encapsulation of flavors by coacervation. Additionally, the good thermal and barrier effects of MCC positions it as an ideal shell wall material for encapsulates which are usually subjected to high thermal treatment. 4.4. Reinforcement of edible films Generally, the application of edible films in food, particularly fresh farm produce is fundamentally constrained by the need to address diverse properties and needs; cost, availability, functionality, mechanical properties, attributes, optical behavior, barrier effects against moisture and gases and resistance to microbes ˜ (Falguera, Quintero, Jiménez, Munoz, & Ibarz, 2011). MCC isolated from variety of cellulosic sources have been used to form composite films with clear improvements in the optical and mechanical ´ properties and thermal stability (Galus & Kadzinska, 2015; Pereda et al., 2011; Suppakul, Jutakorn, & Bangchokedee, 2010). In their study of composite edible films fabricated with HPMC reinforced with three different MCC nanoparticles Bilbao-Sainz et al. (2010) investigated the mechanical and barrier properties of the composite nanocrystals. The incorporation of unmodified MCC led to appreciable reinforcement of the HPMC matrix, regardless of the particle size. Additionally, the presence of MCC in nano scale dimension (nanocrystals) obtained from bacteria cellulose not only improved the mechanical properties of gelatin nanocomposites film but also reduced the moisture affinity of gelatin (George & Siddaramaiah, 2012). Crystallinity was generally identified and accepted as the key property responsible for the mechanical and thermal stabilities of micro/nano crystalline celluloses. Under such conditions, hydrogen bonds conform the cellulose polymers in closed packed crystals, thereby enhancing the mechanical and chemical stability of the material (Takahashi, 2009). Cao, Chen, Chang, and Huneault (2007) reported that nano/micro scale dimension particles of crystalline

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Table 4 Typical Nutritional content of MCC (per 100 g). Nutrient

Colloidal Avicel

Powdered Avicel

Total Calorie Total fat Total dietary fiber Soluble dietary fiber Sugar Protein Vitamin A Vitamin C Sodium Iron Calcium Ash

20 cal 0 93 g 5g ND ND ND ND 934 mg 0.5 mg 2g 2g

0 cal 0 98 g 0g ND ND ND ND 4 mg 0.24 mg 0.1 mg 1g

Adopted from FMC, ND = not detected.

cellulose are favored as reinforcing fillers in polymeric matrices due to their good mechanical properties with very high bending strength and stiffness (e.g. Young’s modulus of about 150 GPa). In the micro/nano-scale range, materials may present different chemical properties, which in turn affects their optical, catalytic and other reactive properties (Pereda et al., 2011). Most grades of MCC have good moisture sorption properties (Merci, Urbano, Grossmann, Tischer, & Mali, 2015; Okwonna, 2013; Rojas & Kumar, 2011) and therefore negatively influence films produced with only MCC; less desirable water and gas barrier functions. The challenges of moisture and gas barrier function inefficiencies are minimized when materials with excellent moisture and gas barrier properties but poor mechanical integrity are combined with MCC particles to fabricate a composite film. The use of MCC in edible coating has been rarely investigated and so very limited information is available. Suppakul et al. (2010) indicated that cellulose-based coatings could prolong the shelf life and maintain the quality of fresh eggs by three weeks compared to control, when stored at room temperature. This suggests that fresh horticultural products such as fruits and vegetables could also be protected using colloidal MCC to prolong shelf life and slow down their deterioration rate. 5. Nutritional and health benefits of microcrystalline cellulose The nutritional effect of MCC in humans could best be described as indirect, principally because human carbohydrate digestive enzymes cannot degrade ␤-glycosidic linkages. The major constituent of MCC is cellulose (Table 4), which is widely accepted as a dietary fiber. Many dietary fibers have been shown to offer potential health benefits to the gastrointestinal tract. Mechanisms proposed for these dietary fibers beneficial effects include but not limited to the control of gastric emptying and ileal brake (satiety effect), hypoglycemic response (diabetes), plasma cholesterol levels (cardiovascular disease) (Gidley, 2013). However, the mechanisms controlling the positive nutritional and health effects may vary according to fiber type. This is because each dietary fiber has distinct physicochemical properties, which define its functionality. Additionally, distinct fiber-based processes occur in the gastric, small intestinal and large intestinal environments, with significant biological cross talk between the sites (Gidley, 2013). Recent advances of MCC on nutritional and health perspectives are summarized in Table 5 and further discussed in the sections below. 5.1. Hypoglycemic and hypolipidemic effects Hypocholesterolemic and hypoglycemic effects of MCC have been studied, both in vivo (Bartley et al., 2010; Ibrugger, Kristensen,

Mikkelsen, & Astrup, 2012; Marounek, Volek, Skˇrivanov, Taubner, & Duˇskova´ı, 2016; Niemi, Kienanen-Kiukaanniemi, & Salmela, 1988; Shao et al., 2013) and ex-vivo (Zhu et al., 2015) models. However, the results are contradictory and may be related to the MCC concentration and source, duration of feeding, the subjects and other unknown factors. van Bennekum, Nguyen, Schulthess, Hauser, and Phillips (2007) observed that MCC had no effect on intestinal cholesterol in rats. Similarly, Shao et al. (2013) in their study of the effect of fiber types on hamsters fed with high lipid diets, reported that MCC had insignificant effect on plasma cholesterol concentra˚ & Duˇsková, 2010). tions (Marounek, Volek, Skˇrivanová, Tuma, On the contrary, recent studies on hypolipidemic effects of MCC demonstrated better cholesterol lowering ability of the crystalline cellulose. MCC-potato starch composites exhibited better antilipidemic effects in rats compared to other fiber composites, when the effects of five different fiber composites on obesity-induced rats were evaluated (Adel & El-shinnawy, 2012). Similarly, the inclusion of MCC to feed of growing greatly reduced cholesterol in contrast with control groups (Wu, Xie, & Zhang, 2016). Golden Syrian hamsters fed either freeze-dried ground pizza, pound cake, or hamburger and fries fortified with MCC greatly increased fecal excretion of saturated and trans fatty acids (Yokoyama et al., 2011). In their study of the effects of different particle sized MCCs on lipid metabolism using ovariectomized rats, Lu et al. (2015) demonstrated that MCC extracted from sweet potato residues exhibited better hypolipidemic effects, in contrast with the control groups with the effect being more pronounced in smaller particle sized MCC fed rats. Induced-MCC viscosity of the digesta led to increase in the intestinal pool of bile acids and fecal excretion, and caused a down regulation of enzymes involved in lipid synthesis, while those responsible for ileal apical sodium- dependent bile acid transporter and intestinal bile acid binding protein were up-regulated (Hongjia et al., 2015; Lu et al., 2015). Apart from viscosity, it is possible that fat and bile acid binding abilities of MCC may be due to its increased hydrophobicity as a result of its crystalline component. Modification of crystalline cellulose to increase hydrophobic interactions with bile acids has been reported in literature. When investigating the interactions between amphiphilic microfibrillated cellulose and bile salts, Zhu et al. (2015) reported optimum chemical structure of hydrophobic modified microfibrillated cellulose for bile binding. They noted that binding capacity of the modified polymer to bile acids due to the hydrophobic interactions significantly increased to optimum as the chain length of the alkyl substitutes (R2 ) increased to chain length of C16 . Studies on hypoglycemic effects of MCC are very limited. Takahashi, Karita, Ogawa, and Goto (2005) observed that glucose did not bind to MCC in vitro in humans. Similarly, MCC had no significant ability to reduce blood glucose levels in type-2 diabetics compared to control groups Niemi et al. (1988). However, in pigs (Lattimer & Haub, 2010) and rats (Takahashi et al., 2005), MCC reduced blood glucose significantly. According to Takahashi et al. (2005), the viscosity and viscoelasticity of the small intestinal content of rats were increased by the presence of the MCC. The increase in viscosity and viscoelasticity of the gastric, small, and, cecal contents from rats were also reported in vitro (Eswaran, Muir, & Chey, 2013). The authors concluded that MCC reduced the rate of absorption of glucose by retarding diffusion within the lumen by increasing digesta viscosity. In summary, the possible underlying mechanisms of the hypolipidemic and hypoglycemic actions of MCC in the body relate to the following: 1) prebiotic effect, which modulates gut microbiota and increases host metabolism; 2) dietary energy restriction due to dilution of nutrients by the fiber; 3) improved viscosity of GIT content due to the fiber influences; 4) increased fecal excretion

Table 5 Summary findings of in vivo and in vitro studies on the effects of MCC on nutrition and health. Parameters studied

Species/study model

Duration of feeding (days)

Quantity of MCC in diet

MCC source

Effect feeding/treatment

Reference Bartley et al. (2010), Yokoyama et al. (2011) Marounek et al. (2010)

Male Golden Syrian hamsters

28

5%

unknown

No effect on quantity of food intake

10

95%

Rice hull and straw, Bean hull

Significantly reduced food intake

Body weight

Hyperlipidemic Induced adult male albino rats (Rattus norvegicus) Growing pigs Female Wistar rats Male Golden Syrian hamsters

60 28 28

5% 29% 5%

Unknown Unknown Unknown

No effect on food intake No effect on food intake No effect on body weight loss

Ovariectomized Rats

28

10%

Sweet potato residues

Growing pigs Female Wistar rat Hyperlipidemic Induced adult male albino rats (Rattus norvegicus) Humans (Diabetic male and female patients) Ovariectomized Rats

60 28 10

5% 29% 95%

Unknown unknown Rice hull, rice straw, bean hull

Minimal on body weight reduction and reduction become more pronounced as MCC particle size reduced Significantly decreased body No effect on body weight Significantly reduced body weight

48

15 g per day

Unknown

28

10%

Sweet potato residue

Growing pigs

60

5%

Unknown

Male albino rats (Rattus norvegicus)

10

95%

Rice hull, rice straw, bean hull

Effect on excretion of saturated fatty acids and trans fatty acids

Male Golden Syrian hamsters

28 days

5%

Unknown

Gene expressions of enzymes involved in lipid anabolism

Ovariectomized Rats

28 days

10%

Sweet potato residues

Expression of genes involved ileal apical sodium- dependent TBAs transporter and intestinal bile acid binding Total bile acids (TBAs)

Ovariectomized Rats

28 days

10%

Sweet potato residues

Ovariectomized Rats

28 days

10%

Prebiotic effect (SCFAs)

Ovariectomized Rats

28 days

10%

Sweet potato residues Sweet potato residues

Growing pigs

60 days

5%

Effects on diabetics Plasma lipids/total cholesterol (VLDL, LDL, HDL, TG)

unknown

No significant effect on blood glucose control -No effect on HDL cholesterol. -Significantly reduced triglycerides in MCC treated rats compared with control group. -Reducing the particles size of MCC to nano scale dimension significantly reduced LDL-C, and non-HDL-C of rats under treatment compared with control -Significantly reduced serum total cholesterol and LDL cholesterol and also increased HDL cholesterol of MCC fed- pigs than control groups. -No effect on Triglycerides levels Significantly reduced all plasma lipid profiles and showed good antilipidemic activity Increased fecal excretion of Saturated and trans fatty acids better than controls Caused down regulation of the expression of enzymes involved lipid synthesis Caused up-regulation of ileal apical sodium- dependent bile acid transporter and intestinal bile acid binding protein Decreased TBAs reabsorption, causing increased fecal excretion of TBAs SCFAs concentrations increased significantly in MCC fed rats compared to control groups Increased short SCFAs significantly

Wu et al. (2016) Marounek et al. (2010) Bartley et al. (2010), Yokoyama et al. (2011) Hongjia et al. (2015), Lu et al. (2015) Wu et al. (2016) Marounek et al. (2010) Adel and El-shinnawy (2012) Niemi et al. (1988) Lu et al. (2015)

Wu et al. (2016)

Adel and El-shinnawy (2012)

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Food intake

Yokoyama et al. (2011)

Lu et al. (2015)

Lu et al. (2015)

Lu et al. (2015) Lu et al. (2015)

Wu et al. (2016) 169

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and intestinal bile acid due to the increased hydrophobic interactions between bile acids and MCC; and 5) improved hydrophobicity due to its crystalline nature. 5.2. Prebiotic effect MCC is indigestible in the upper GIT but partially fermentable in the colon (Paturi et al., 2010) and so may potentially have limited use as a prebiotic in functional food. The ability of crystalline cellulose to undergo fermentation in the cecum, however, depends on its physicochemical properties. Recent findings revealed that the reduction of sweet potato cellulose particle size to MCC and NCC fiber powders effectively enhanced the physicochemical properties and consequently improved its physiological and biological effects (Hongjia et al., 2015; Lu et al., 2015; Lu, Gui, Zheng, & Liu, 2013). In vitro fermentation of MCC and NCC demonstrated that the smaller particle size cellulose elevated SCFA production better than that of the larger particle size ones (MCC) in rats (Lu et al., 2015), primarily due to the better physicochemical properties of the smaller particles size samples (Lu et al., 2013). When rats were fed with both high fat and low fat diets supplemented with MCC, appreciable quantities of SCFAs were observed during the analysis of the cecal SCFAs (Paturi et al., 2010). Analysis of in vitro fermentation of adult rabbits cecal content fed on MCC isolated from alfalfa hay, produced significant levels of SCFAs (Yang, Cao, & Zhang, 2010). The products of the cecal fermentation of MCC are mainly SCFAs including acetate, propionate and butyrate (Yang et al., 2010; Zhou et al., 2014) as well as other metabolites, such as lactate, pyruvate, hydrogen and succinate (Gibson, 1999), similar to the products of highly fermentable soluble prebiotics. In addition to SCFAs, MCC fermentation in the colon also produces gases. In vitro cecal content fermentation of adult rabbits fed on MCC isolated from alfalfa hay yielded CH4, H2 and CO2 gases, similar to the gases produced by inulin, fructo-oligosaccharide, and guar gum during other in vivo studies (Bianchi & Capurso, 2002; Gibson, 1999; Li & Nie, 2016; Paturi et al., 2010). It is believed that SCFAs may activate the enteroendocrine cells of the gut to secrete a host of metabolically active peptides that regulate satiety (Tolhurst et al., 2012). Moreover, butyric acid producing bacteria are of interest because of their health-promoting effects (Paturi et al., 2010). A common feature associated with highly fermentable soluble fibers is the production large of large volumes of gases. Depending on the doses of these gases, they might create unwanted symptoms such as flatulence bloating, and cramps (Ducrotteì, 2010; Li & Nie, 2016). The low solubility and tight packing of the glucose polymers in MCC reduces its fermentability by the colonic microflora, leading to less gas production compared to the highly soluble fibers such as inulin and guar gum (Bianchi & Capurso, 2002). This suggests that MCC could be prebiotic with less associated unwanted symptoms. 5.3. Bowel movement and constipation Reduction of particle size of crystalline cellulose from micro to nano level increased the specific area, water-holding capacity, swelling capacity, and oil-holding capacity of the cellulose crystals (Lu et al., 2013). In the colon, the relatively low fermentable crystalline cellulose absorbs water and improves fecal bulking. Its swellability is due to the absorption of only a small fraction of water that is able to penetrate the individual MCC particles, causing them to swell, with the remaining bulk of the water existing in free state between the particles (Ngozi et al., 2014). The SCFAs produced by MCC are believed to modulate the motility by exerting a trophic effect on the epithelial cells, thereby elevating the blood flow in the region (Ducrotteì, 2010). In order to move the more viscous and viscoelastic intestinal content containing dietary MCC, more pressure is needed in the intestinal lumen

(Takahashi, 2009). Increased viscosity and viscoelasticity by MCC in the small intestine increased the pressure during segmental contractions and peristalsis in rats and increased the water potential and stimulated water absorption (Takahashi et al., 2005). Greater proportion of propulsive duodenal contractions and antral motility index are associated with the consumption of meals fortified with MCC, due to the higher pressure and water potential created by the fiber (Takahashi, 2009). Similarly, an increase in water absorption in the jejunum of pigs fed with MCC has been observed (Lattimer & Haub, 2010). Intestinal dysbiosis, characterized by an imbalance between undesirable and beneficial bacteria with the undesirables dominating, relates positively to chronic constipation syndrome (de Souza Lima Sant’Anna & de Luces Fortes Ferreira, 2014). The imbalance may affect the movements of the large intestine via alteration of the metabolic environment of the colon. The pH of the colon with higher levels of undesirable bacteria is higher due to the reduction in the production of physiologically beneficial compounds such as SCFAs (Gerritsen, Smidt, Rijkers, & de Vos, 2011). The imbalance may be corrected by probiotics or symbiotics and dietary fibers with prebiotic effects such as MCC, that stimulate the growth of the desirable colonic bacteria (e.g lactobacilli and bifidobacteria). Although colonic fermentation of MCC is partial, significant amount of SCFAs, particularly butyrate, which is proven to be effective on the modulation of intestinal motility (Gunaranjan, Butts, Stoklosinski, & Ansell, 2012) is produced. Among the SCFAs, Soret et al. (2010) observed that butyrate is the preferred energy source for the colonic mucosa cells and has positive effects on mesenteric neurons and motility in rats. 5.4. Obesity management Hypoglycemic and hypolipidemic effects of food are important in the management of obesity and diabetes mellitus. The important functions of dietary fibers in body weight maintenance and overall health is increasingly recognized so daily dietary recommendation of >25 g for healthy persons has been given by WHO. However, it is generally recognized that various dietary fiber types vary greatly in their physicochemical characteristics and hence may differ greatly in their physiological effects (Brownlee, 2011). Using obesity induced mice, Li, Guo, Ji, and Zhang (2016) qualitatively demonstrated differences in the capabilities of dietary fiber types to suppress high-fat diet induced obesity, and reported that insoluble fibers were more effective in suppressing high-fat induced obesity than soluble fibers. Similarly, Adel and Elshinnawy (2012) observed that rats fed on MCC-potato composites had the lowest food consumption as well as the most decrease body weight when they evaluated the effects of five different fiber composites on previously induced hyperlipidemic rats. The addition of MCC in the diet of experimental ovariectomized rats significantly decreased body weight gain compared with the control group (Lu et al., 2015). Similarly, the smaller particle-sized MCC reportedly produced the highest weight loss when four groups of rats were fed with high fat diet supplemented with MCC of unequal particles size (Hongjia et al., 2015). 6. Gaps and implications for future research The application and trading of the cellulose have become a global business. Its applications are well established across diverse areas creating continual demands for it globally. The over reliance and general dependence of wood pulp as the major raw materials by many MCC manufacturers raises potential environmental concerns in relation to deforestation. Though the literature reviewed clearly showered that extensive works have been done in identi-

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fying new sources of MCC including agricultural residues, which are relatively cheaper than wood, most of these research works have mainly concentrated on the extraction methods and physicochemical properties of the crystalline celluloses with negligible emphasis on industrial application (particularly, food). Hence, it will be an interesting area to consider in the efforts to make these new sources more acceptable, particularly to the food and pharmaceutical industries, which are the major users of MCC. In the pharmaceutical industry, MCC is the most widely used excipient for production of tablets, due to its unique characteristics of plasticity and cohesiveness when wet. Also the fact that MCC forms sufficiently hard tablets, which rapidly disintegrate making it more relevant in the pharmaceutical industry. However, the material still has certain limitations, such as the slow release rate of bioactives with low water solubility. To overcome these disadvantages, co-processing of the MCC with other excipients has been identified to produce mixed excipient with better functionality. Development of new colloidal cellulose by co-processing MCC with cheap and lesser-known dispersible materials for food applications can potentially overcome the poor solubility of the material and improve its functionality in food product development. According to the literature reviewed in this paper, it is obvious that MCC obtained from wood and other plant sources is not purely (100%) cellulose. Traces of lignin, and other contaminating polysaccharides may be present. However, the contribution of these traces of polysaccharides in the MCC on functionality, particularly surface activity has not been reported. It would be interesting for future research on the material to consider it. Increasingly knowledgeable consumers expecting high food product quality have challenged food scientists to innovate in product development. Primarily, the efforts are geared towards providing products with enhanced organoleptic and sensory properties with a healthier image or extended shelf-life, at reduced production cost by incorporating less costly ingredient that give better manufacturing efficiency through new processing technology. An area at the forefront of MCC research is the development of new functional foods or nutraceuticals. Advances in the functional food industry have released potential design-directed functional foods formulations using the cellulose based on its indigestibility as a dietary fiber. Though MCC has no direct nutritional contribution, its presence in food has physiological effects on gastrointestinal health. Largely, studies on nutritional and health effects of MCC remain skeptical and less understood compared to soluble fibers. Mechanisms underlying the nutritional and health effects of MCC are poorly understood. Therefore, with advancement modern technology in food and nutritional sciences, the area presents opportunity for more scientific exploration.

7. Conclusions MCC has many applications in the food industry and has improved the quality of new products and their properties. The ingredient is used as a fat substitute or replacer in meat products (sausages, beef patties), baked (bread, cakes, etc.,) and emulsion based products, suspending agent for beverages and thickening agent for emulsions and suspensions. The presence of MCC in these products not only impact mechanical, and rheological properties of the final product for better textural, sensory and organoleptic attributes, but also reduces calorie levels. While there are countless applications of MCC in food and beverages, its places second to pharmaceutical uses as far its industrial consumption is concerned. As a dietary fiber, its roles are recognized in the physiological functions of the gastrointestinal tract and its nutrient dilution effect. Though widely accepted as a good source of dietary fiber, the literature reviewed seems to suggest that the mechanistic under-

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standing of MCC nutraceutical functions is not fully understood in contrast to soluble dietary fibers. It is also established that unlike most prebiotics especially soluble fibers, MCC has minimal colonic fermentation in contrast with soluble dietary fibers such as inulin.

Acknowledgments This project was supported by the Self-determined Research Program of Jiangnan University (JUSRP 115A22) and by program of “Collaborative innovation center of food safety and quality control in Jiangsu Province.

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