\r\n\t• Role of technological innovation and corporate risk management \r\n\t• Challenges for corporate governance while launching corporate environmental management among emerging economies \r\n\t• Demonstrating the relationship between environmental risk management and sustainable management \r\n\t• Contemplating strategic corporate environmental responsibility under the influence of cultural barriers \r\n\t• Risk management in different countries – the international management dimension \r\n\t• Global Standardization vs local adaptation of corporate environmental risk management in multinational corporations. \r\n\t• Is there a transnational approach to environmental risk management? \r\n\t• Approaches towards Risk management strategies in the short-term and long-term.
",isbn:"978-1-83968-906-2",printIsbn:"978-1-83968-905-5",pdfIsbn:"978-1-83968-907-9",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!1,hash:"9b65afaff43ec930bc6ee52c4aa1f78f",bookSignature:"Dr. Muddassar Sarfraz and Prof. Larisa Ivascu",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10226.jpg",keywords:"Global Risk Management, Risk Assessment, Climate Risk, Environmental Management, International Business, Business Sustainability, Corporate Governance, Financial Market, Financial Risks, Sustainable Economic Environment, Business Valuation, Organizational Behavior",numberOfDownloads:131,numberOfWosCitations:0,numberOfCrossrefCitations:0,numberOfDimensionsCitations:0,numberOfTotalCitations:0,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"September 24th 2020",dateEndSecondStepPublish:"October 22nd 2020",dateEndThirdStepPublish:"December 21st 2020",dateEndFourthStepPublish:"March 11th 2021",dateEndFifthStepPublish:"May 10th 2021",remainingDaysToSecondStep:"4 months",secondStepPassed:!0,currentStepOfPublishingProcess:4,editedByType:null,kuFlag:!1,biosketch:"Dr. Muddassar Sarfraz focuses on corporate social responsibility, human resource management, strategic management, and business management. He is a member of the British Academy of Management (UK), Chinese Economists Society (USA), World Economic Association (UK), American Economic Association (USA), and an Ambassador of the International MBA program of Chongqing University, PR China, for Pakistan.",coeditorOneBiosketch:"Dr. Larisa Ivascu's area of research includes sustainability, management, and strategic management. She has published over 190 papers in international journals. She is vice-president of the Society for Ergonomics and Work Environment Management, Timisoara, and a member of the World Economics Association (WEA), International Economics Development and Research Center (IEDRC), Engineering, and Management Research Center (CCIM).",coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"260655",title:"Dr.",name:"Muddassar",middleName:null,surname:"Sarfraz",slug:"muddassar-sarfraz",fullName:"Muddassar Sarfraz",profilePictureURL:"https://mts.intechopen.com/storage/users/260655/images/system/260655.jpeg",biography:"Dr Muddassar Sarfraz is working at the Binjiang College, Nanjing University of Information Science and Technology, Wuxi, Jiangsu, China. He has obtained his PhD in Management Sciences and Engineering from the Business School of Hohai University. He holds an International Master of Business Administration (IMBA) from Chongqing University (China) and Master of Business Administration (HR) from The University of Lahore. He has published tens of papers in foreign authoritative journals and academic conferences both at home and abroad.\nHe is the Book Editor of Sustainable Management Practices, Analyzing the Relationship between Corporate Governance, CSR, Sustainability, and Cogitating the Interconnection between Corporate Social Responsibility and Sustainability. He is the Associate and Guest Editor of Frontiers in Psychology, International Journal of Humanities and Social Development Research and the Journal of Science and Innovative Technologies. He is an Editorial Board Member of the International Journal of Human Resource as well as a member of the British Academy of Management (UK), Chinese Economists Society (USA), World Economic Association (UK), American Economic Association (USA), and an Ambassador of the International MBA program of Chongqing University, PR China, for Pakistan. \nHis research focuses on corporate social responsibility, human resource management, strategic management, and business management.",institutionString:"Binjiang College, Nanjing University of Information Science &Technology, Wuxi, Jiangsu",position:null,outsideEditionCount:0,totalCites:0,totalAuthoredChapters:"0",totalChapterViews:"0",totalEditedBooks:"1",institution:null}],coeditorOne:{id:"288698",title:"Prof.",name:"Larisa",middleName:null,surname:"Ivascu",slug:"larisa-ivascu",fullName:"Larisa Ivascu",profilePictureURL:"https://s3.us-east-1.amazonaws.com/intech-files/0030O00002bRfMOQA0/Profile_Picture_1594716735521",biography:"Dr Larisa IVAȘCU is currently an associate professor at the Politehnica University of Timisoara. 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1. Introduction
In the last decades the destination of biomass, especially agro-industrial residues, is an important world problem that has been target of many researches. Accumulation of agro-industrial residues in the environment can cause serious ecological problems. On the other hand, these kinds of rich carbohydrate materials can aggregate economical value to different biotechnological process as for example in the microbial fermentative processes. According to this, the proposal of this chapter is to describe and discuss the utilization of biomass from agro-industrial residues and products and its transformation by microbial enzymes to obtain products (saccharides) with industrial interest. This is a subject that has attracted the attention of many researches and industrial sectors. To organize the information concerning this subject in a chapter is very interesting to qualify the state of the art on the utilization and importance of carbohydrates from the agro-industrial residues and products. The importance of microorganism for the transformation of biomass is another important aspect that will be highlighted.
Microorganisms, as bacteria and fungi, are able to use a great variety of inorganic and organic compounds as nutrients, reflecting an interesting metabolic diversity. Among these nutrients, nitrogen and carbon sources are indispensible for a primary metabolism. Others nutrients are required at low concentration, as vitamins. According to the growing, microorganisms are able to produce many enzymes that can show interesting biochemical properties for biotechnological application (Guimarães et al., 2006). Among these enzymes, some are constitutive while others are inducible. The induction of enzyme production by microorganisms can be obtained by use of properly biomass as carbon sources. Microorganisms are able to produce a diversity of enzymes as, for instance, the carbohydrate-active enzymes (figure 1). The glycoside hydrolases are enzymes able to acts on disaccharides, oligosaccharides and polysaccharides where can be found important enzymes as cellulases, amylases, inulinases and invertases (Table 1). Carbohydrate esterase is involved in the removal of O-(ester) and N-Acetyl moieties from carbohydrates. The polysaccharide lyase catalyzes the β-elimination reaction on uronic acid glucosides while the glycosyltransferase acts forming glycosidic bonds using activated sugar donors.
Figure 1.
Classes of carbohydrate-active enzymes.
Microorganisms
Enzymes
Cellulase*
Xylanase
Invertase
Inulinase
Amylase
Bacteria
Acremonium cellulolyticus
◆
◆
Arthrobacter sp.
◆
Bacillus amyloliquefaciens
◆
◆
Bacillus cellulyticus
◆
Bacillus circulans
◆
◆
Bacillus licheniformis
◆
◆
Bacillus subtilis
◆
◆
◆
Bifidobacterium sp.
◆
Cellulomonas sp.
◆
◆
Clostridium cellulolyticum
◆
Clostridium thermocellum
◆
◆
Lactobacillus sp.
◆
◆
Pseudoalteromonas sp.
◆
Streptomyces sp.
◆
Fungi
Aspergillus aculeatus
◆
◆
Aspergillus caespitosus
◆
◆
Aspergillus japonicus
◆
◆
Aspergillus niger
◆
◆
◆
◆
◆
Aspergillus ochraceus
◆
◆
Aspergillus oryzae
◆
◆
◆
◆
Aspergillus phoenicis
◆
◆
Aspergillus terreus
◆
◆
Chaetomium thermophilum
◆
◆
Emericella nidulans
◆
◆
◆
Fusarium oxyporum
◆
Humicola grisea
◆
◆
Humicola insolens
◆
◆
Neurospora crassa
◆
◆
◆
◆
◆
◆
◆
Trichoderma viride
◆
◆
Table 1.
Some microbial (bacteria and fungi) sources of the enzymes involved in the utilization of carbohydrates found in the plant biomass.
2. Microbial cultivation using biomass
Different kinds of biomass have been used as carbon sources in the microbial cultivations under submerged and solid-state fermentations. Agro-industrial residues and products as, for example, rice straw, fruit peels, sugar cane bagasse and oat meal are important alternatives of carbon sources for both kinds of fermentation. The solid-sate fermentation is characterized as a system constituted by solid material in absence of free water where microorganisms are able to grown. This condition is more similar than that found by microorganisms in the environment if compared to the submerged condition. In addition, some other advantages for use of solid-state fermentation has been mentioned as: i) higher yields of products; ii) similar or higher yield if compared to submerged fermentation; iii) uniform dispersion of spore suspension; iv) higher levels of aeration and v) reduction of problems with contamination by bacteria and yeast. It is also important to consider that the medium for solid-state fermentation is simple and low cost substrates as agro-industrial residues can be used.
According to the substrate nature, two processes can be used for solid-state fermentation. The solid substrate, in the first case, is used as both support and nutrient source. These substrates are obtained from agriculture activity or from by-products from food industry. Generally, they are heterogeneous and water insoluble. When substrates with amylaceous or lignocellulosic nature will be used, a pre-treatment is required to convert raw substrate into a suitable substrate. After, the liquid medium containing nutrients necessaries to the microbial growth can be used to moisten the inert support. The microbial growth and the product synthesis in solid state fermentation is influenced by environmental factors, such as water activity, moisture content of the substrate, mass transfer processes, temperature and pH. The control of these factors is not easy, configuring a negative aspect from solid-state fermentation. However, under economic view, solid-sate fermentation can be applied in different sectors for biotransformation of crop residues, food additives, biofuels, bioactive products, production of organic acids, detoxification of agro-industrial wastes, bioremediation, biodegradation and enzyme production (Pérez-Guerra et al., 2003).
The use of agro-industrial residues and/or products as substrates/ carbon source for SSF should be considered under some aspects. According to the biomass characteristics a pre-treatment step is necessary as cited above. To transform the raw material to the available form for microbial utilization it is necessary, many times, to reduce the size of the material using for example grinding among others. Other possibility is to promote damages on the superficial substrate layers using cracking, grinding or pearling. The utilization of chemical or enzymatic pre-treatments, cooking or vapor treatment and elimination of contaminants can be also utilized. According to the nutritional exigency of the microorganism, supplementation with phosphorus and nitrogen sources and salts can improve the microbial growth and the product yield. On the other hand, the influence of environmental factors on the SSF system also deserves consideration. The microbial growth as well as the obtainment of the products in SSF is directly affected by the moisture content. Excessive or reduced moisture content is prejudicial to the microorganism and, consequently, to the product recovery. According to this, the moisture content should be adjusted for each microorganism used in process considering the nature of the matrix used as substrate, and it has been used water content of substrate from 30% to 70% (Pérez-Guerra et al., 2003).
In SSF the gases and nutrients diffusion are severally affected by the matrix structure and also by the liquid phase in the system. The aeration permits an effective supplement of oxygen that can be used for aerobic metabolism and, at the same time, it promotes the removing of CO2 and water vapour as well as the heat and volatiles compounds produced by the microbial metabolism. The temperature in the SSF system is a consequence of the microbial metabolism if the heat is not removed. The acquirement of nutrients depends on both hydrolysis of the polymeric structure to obtain monomers and after diffusion through the cell membrane from outside to inside the cell. The pH is another factor that affects the SSF system but its control is difficult (for review, see Pérez-Guerra et al., 2007).
Advantages for enzyme and secondary metabolites productions have been reported for both fermentations. In addition, agro-industrial residues and products are excellent alternatives as substrates for solid-state fermentation. These substrates, and consequently their carbohydrate content, can be transformed by action of a set of enzymes instead the chemical conversion. Enzymatic technology is a clear and secure process minimizing the environment problems while chemical process can generate pollulents.
Sugar cane bagasse is one of the most important agro-industrial residues accumulating biomass in the environment (figure 2) that can be used for microbial transformation. In Brazil, around 80 million of ton of sugar cane bagasse is produced per year. This raw material is constituted by 26-47% cellulose, 19-33% hemicelluloses, 14-23% lignin and 1-5% ashes. Part of this biomass as used for electric energy generation, but the most part is accumulated without
Figure 2.
Utilization of sugar-cane bagasse as biomass source for microbial activity (photos by Guimarães L.H.S).
destination. So, sugar cane bagasse can be used for many other purposes as paper production, fertilizer, feeding for ruminant animals and ethanol production, among others. It is an interesting carbon source/substrate for microbial cultivation and enzyme production as verified for many filamentous fungi. High levels of β-fructofuranosidase were obtained using sugar cane bagasse as carbon source in submerged cultivation from Aspergillus niveus (Guimarães et al., 2009) and Aspergillus ochraceus (Guimarães et al., 2007).
Many others agro-industrial residues can be used for microbial cultivation such as wheat bran, which was used for invertase production by Aspergillus caespitosus under submerged and solid-state fermentation (Alegre et al., 2009).
Although the submerged fermentation and solid state fermentation as good option for microbial cultivation, a new kind of fermentation has been proposed. The biofilm fermentation (BF) is characterized by the fungal growing on the inert support as can be observed in the figure 3.
Figure 3.
The Aspergillus phoenicis biofilm on the polyethylene as inert support.
The adhesion on surface is a natural process observed for the filamentous fungi in the environment. This complex process involves the production of adhesive compounds that fix the spore to the substrate, germ tube formation, hyphae elongation and, finally, surface colonization. These events can be observed in the Aspergillus niger biofilm formation on polyester cloth as reported by Villena and Gutiérrez-Correa (2007). These authors observed that the morphological pattern for A. niger growth attached to the surfaces is similar to that found in microbial biofilms with micro colonies development, extracellular matrix production and formation of pores and channels. The fungal morphology is an important factor to the enzyme production and, compared to the submerged fermentation, biofilms are more productive and more efficient if considered the metabolism associated with the specific enzymes which act on biomass, as for instance lignocellulosic enzymes. Recently, the use of Aspergillus phoenicis biofilms was reported for fructooligosaccharides production by one simple step (Aziani et al., 2012).
3. Biomass conversion by microbial enzymes
Residues and products of plant origin are recognized by their carbohydrate composition. According to this composition, the action of different enzymes on polysaccharides permits the obtainment of a variety of mono- and oligosaccharides which can be used by different sectors including biofuel, food, beverage and pharmaceutical among others.
Nowadays, the future of our energy sources and consequently the life in the planet is target of discussion around the world with participation of different sectors of the society as researches, politicians, undertakers and third sector. It has been noted that there is an increasing interest on biomass utilization as renewable energy source since that there is a conscience that the fossil fuels are restricted. In addition, this kind of fuel is a determinant factor of pollution to the atmosphere, where the CO2 concentration has been increased. Hence, the utilization of biomass from plant residues for biofuel production is pointed-out as an important alternative for reduction of the energetic and environment problems. Brazil and USA are the main producer countries of ethanol to be used as fuel, the former using sugar cane and the later using the corn. For example, ton of sugar cane bagasse is generated as residue from the ethanol production in Brazil, which could be used for obtainment of fermentable sugars by enzymatic hydrolysis. In the next step, these sugars can be used for fermentation process to obtain ethanol.
3.1. Cellulases and lignocelullosic biomass
Considering the plant biomass, the main component from plant cell wall is the cellulose, the more abundant carbohydrate found in the planet. Structurally, this saccharide is constituted by glucopyranose monomers linked by β-1,4 glycosidic bonds with two distinct regions, the crystalline and amorphous regions. For the complete cellulose hydrolysis, an enzymatic complex (known as cellulases) constituted by endo-1,4- β-glucanases (EC 3.2.1.4), exo-1,4- β-glucanases or cellobiohydrolases (EC 3.2.1.91), and 1,4- β-glucosidases (EC 3.2.1.21), is necessary. Cellulases are modular enzymes included in the GH family (glycoside hydrolases). These enzymes have a complex structure with different modules as one or more catalytic domain and/or CBD module in the same protein. The CBD module is able to modify the catalytic domain and, consequently the cellulase properties, facilitating the interaction catalytic domain/crystalline cellulose. Cellulases can act using two main catalytic mechanisms, inversion or retention of the anomeric carbon. Two catalytic carboxylate residues are involved in both mechanisms and they are responsible for the acid-base catalysis in the reaction. Endoglucanases (EG; carboxymethiylcellulases, CMCase) catalyze random cleavage of cellulose internal bonds at amorphous region. Exoglucanases, also known as cellobiohydrolases (CBH) act at the chains ends (CBHI at the reduncing end and CBHII at non-reducing end), releasing cellobiose that can act as competitive inhibitor, while β-glucosidases (BGL) convert short cellooligosaccharides and cellobiose to glucose monomers. It is important to detach that the BGL activity is competitively inhibited by glucose. The GH1 family includes BGL obtained from bacteria, plant and mammalian and the GH3 family includes BGL from bacteria, fungi and plants. However, the full hydrolysis of cellulose depends on the previous hydrolysis of the other cell wall compounds, i.e. hemicelluloses and lignin (Dashtban et al., 2009; Bayer et al., 1998).
Hemicelluloses are polymeric molecules constituted by pentoses (as xylose and arabinose), hexoses (as mannose, glucose, galactose) and sugar acids. Because their heterogeneity, the hemicelluloses hydrolysis is only obtained by the action of different enzymes called hemicellulases. The most important hemicellulase is the enzyme that catalyzes the breakdown of β-1,4 linkages in the xylan, a polymer constituted by monomers of xylose. The oligomers obtained from this reaction are now substrates to the reaction catalyzed by β-xylosidase to obtain xylose (Dashtban et al., 2009).
Lignin is a heterogeneous aromatic polymer constituted by non-phenolic and phenolic structures that is able to link both cellulose and hemicelluloses making difficult the access of the enzymatic preparations to the cellulose and hemicelluloses. The enzyme able to catalyze the lignin hydrolysis are generically named as ligninases, which can be divided in two main families, phenol oxidase (laccase) and peroxidases that includes manganese peroxidase (MnP) and lignin peroxidase (LiP) (Dashtban et al., 2009).
The conversion of the lignocelluloses biomass from different sources to ethanol as can be observed in the figure 4 should take in account different steps as pre-treatment of the material, hydrolysis of the cellulose and hemicelluloses, fermentation and, finally distillation and evaporation. The pre-treatment will facilitate the asses of the hydrolases to the polyssacharides (they will be cleaved by cellulases and hemicellulases) through the lignin breakdown using physical-chemical or enzymatic process. The separated lignin can be used as matrix for energy production, as electricity. The hydrolysis and fermentation steps can be conducted separately or through of simultaneous saccharification and fermentation as shown in SSF square. Some considerations that will be done in next lines on the microorganism selection can be used for the others enzymes discussed in the next pages.
All enzymes from the cellulolitic complex, hemicellulases and lignin hydrolase can be obtained from microorganism as filamentous fungi. In the nature, filamentous fungi are able to produce and secrete different enzymes to the extracellular medium to hydrolyze polymeric compounds to obtain monomers that can be used as nutritional source.
3.2. Amylases, starch sources and structure
Another interesting carbohydrate found in the plant biomass is the starch, the main form carbohydrate reserve in these organisms. The starch is the result of interaction of two structure, one linear structure formed by glucose monomers linked by α-1,4 glycosidic bonds (amylose) with molar mass of 101 e 102 Kg/mol and another branched structure with α-1,6 bonds (amylopectin) with molar mass of 104 and 106 Kg/mol. The units of amylopectin can be classified in tree groups, A, B and C. The type A is simple and characterized by the α-1,6 linkage to the amylopectin structure. The type B is subdivided in B1, B2, B3 e B4 according to the size and the group formation. The type C is a mixture of A and B types. The starch granule is formed by 25% and 75% of amylase and amylopectin, respectively. The last one is responsible for the granule crystalinity. According to the crystallographic structure the native starch can be classified as cereal starch (type A), tuber starch (Type B) and leguminosea starch (type C), that corresponds to the amylopectin groups. The more stable structure for the α-1,4 chains, as observed for starch, is the helix with high degree of spiralization with intra chain hydrogen bridge. The helicoidal structure has six residues per loop where each glucose residue forming an angle of 60° with the next residue (Yoshimoto et al., 2000; Ritte et al., 2006).
Figure 4.
Schematic picture for the conversion of lignocellulosic biomass to ethanol, including the major steps (Original figure from Dashtban M., Schraft H., Qin W. Fungal Bioconversion of Lignocellulosic Residues; Opportunities & Perspectives. Int. J. Biol. Sci. 2009; 5(6):578-595. Available from http://www.biolsci.org/v05p0578.htm)
The starch synthesis is realized in the plastids and it is characterized, at the first step, by the conversion of glucose-1-phosphate and ATP to ADP-glucose and Pi by the ADP-glucose phosphorylase. After, the ADP-glucose can be used as a donor of glucose to different starch synthases that are able to elongate the glucan chain in the α-1,4 positions for both amylase and amylopectin. It is important to highlight the participation of the branching enzymes that are responsible to add α-1,6 linkages by re-organization of linear pre-existent chains. Some introduced branching can be removed by other enzymes to finalize the starch structure. The starch is highly hydrated because there are many hydroxyl groups permitting the interaction with the water. The starch is accumulated in the leaves during the day and it is used at night to maintain the respiration, the sucrose export and the grown. This transitory starch can be use through two ways, i) hydrolytic way to obtain maltose and ii) phosphorolytic way to provide carbon to the reactions in the chloroplast during the light phase.
Similar to the cellulose, the starch cleavage occurs under the action of an enzymatic complex (figure 5). The enzymes found in this complex are organized in four main groups: debranching enzymes; endoamylases; exoamylases; and transferases. The debraching enzymes are able to act exclusively on the α-1,6 glycosidic bonds and they are separated in isoamylase (EC 3.2.1.68) and pullulanase (EC 3.2.1.41). The former hydrolyze this kind of bond exclusively in amylopectin while the later hydrolyzes the α-1,6 bond from amylopectin and pullulan. Endoamylases acts on α-1,4 glycosidic bonds inside the amylose and amylopectin structure. In this group are located the α-amylases that release oligosaccharides with different length from their substrates. They can be found in many microorganisms as bacteria and fungi. Exoamylases are enzymes that hydrolyze the external bonds of amylase and amylopectin to release only glucose or maltose and β-limiting dextrin. Three main hydrolytic characteristics can be recognized for the exomylases: the specific breakdown of α-1,4 glycosidic bonds catalyzed by β-amylases (EC 3.2.1.2) and the breakdown of both α-1,4 and α-1,6 bonds catalyzed by amyloglucosidase (glucoamylase; EC 3.2.1.3) and α-glucosidase (EC 3.2.1.20). β-amylases as well as glucoamylase are able also to convert the anomeric configuration from α to β in the released maltose. In addition, glucoamylases act better on long-chain polysaccharide while α-glucosidases have preference on maltooligosaccharides. The last group of starch-converting enzymes, i.e. transferases, acts on α-1,4 glycosidic bonds of a donor molecule transferring part of this molecule to a glycosidic acceptor producing a new glycosidic bond. In this group are found the enzyme known as amylomaltase (EC 2.4.1.25), cyclodextrin glycosyltranferase (EC 2.4.1.19) and branching enzymes (EC 2.4.1.18). Amylomaltase and cyclodextrin glycosyltranferase have similar mechanism of reaction. Although the reduced hydrolytic activity from these enzymes, they are able to catalyze the transglycosylation reaction to obtain cyclodextrins by breakdown of α-1,4 glycosidic bonds and linkage of the reducing to the non-reducing end. However the product obtained by amylomaltase activity is linear while the cyclic product is obtained by cyclodextrin glycosyltranferase action (van der Maarel et al., 2002).
Many of these enzymes are involved in the complete hydrolysis of the starch. First, disbranching enzymes should act on the α-1,6 bonds to expose the linear structure that can be hydrolyzed by α-amylase and β-amylase (figure 5). Many authors have demonstrated the importance of obtainment of maltooligosaccharides from complex carbohydrate using amylolytic enzymes. Maltooligosaccharides can be used in different industrial sectors as food. Fungi are able to produce amylases. In addition, other important application of the starch is related with its use as source of renewable energy in the production of bioethanol as an alternative to the fossil fuels.
Figure 5.
Different enzymes involve in the degradation of the starch. The open ring structure represents the reducing ends of a polyglucose molecule (Original figure from van der Maarel MJEC, van der Veen B, Uitdehaag JCM, Leemhuis H, Dijkhuisen L. Properties and applications of starch-converting enzymes of the α-amylase family. J. Biotechnol. 2002; 94: 137-155).
3.3. Fructosidases and other carbohydrates from biomass
Other saccharides can be also obtained from plant sources as inulin and sucrose, which are substrates for fructofuranosidase action, as β-fructofuranosidases and inulinases, which can be produced by microorganism as for example yeast and filamentous fungi. These enzymes have an important role in the microbial nutrition since monomers can be obtained and used in the metabolism. On the other hand, the enzymes involved in this process can be used with biotechnological goal.
3.3.1. The inulin and its utilization
Inulin, a polymer constituted by linear chain of β-2,1 fructufuranose residues terminated by a glucose residue, can be obtained from plant sources, especially from tubers and roots, as for example chicory, dahlia, yacon and Jerusalen artichoke. The plant sources of inulin have been considered as renewable raw material for many applications such as ethanol, obtainment of fructose syrup and fructooligosaccharides (FOS) production. This carbohydrate can be hydrolyzed by action of inulinases (2,1 β-D-fructan fructanohydrolase; EC 3.2.1.7), which can be classified into endoinulinase that hydrolyze the internal linkages from inulin to obtain inulotriose, inulotetraose and inulopentaose as end products, and exoinulinase that acts removing the terminal fructose from the non-reducing end from the inulin until the last linkage to release glucose (Ricca et al., 2007). It is important to observe that the type of enzymatic action depends on the microbial source. The most of fungal inulinases acts using the exo-mechanism. However, it was demonstrated that Aspergillus ficuum was able to produce endo- and exo-inulinases with different properties. The mixture of both enzymes can be considered as a good strategy to increase the conversion of the inulin to fructose (for review, see Ricca et al., 2007). Despite the action and affinity similarities for sucrose as substrate, with fructosidases as invertase, inulinases has been separated since invertase has reduced activity on high molecular mass substrates as inulin. The relation S/I has been used to separate inulinase from invertase. The S/I values depends on the inulin sources and also on the methodology used to determine the enzyme activity. However, kinetic studies are good methodologies that can be help the differentiation of these enzymes as for example considering the substrate affinity and catalytic efficiency. On the other hand, the enzymes recognized as true invertases have no activity on inulin.
The inulinases obtained from yeast are enzymes that can be linked to the cell membrane and partially secrete to the extracellular environment. In addition the synthesis of these enzymes is subject to the catabolic repression. In addition, inulinases are recognized as inducible enzymes and they are encoded by INU genes. The enzymes obtained from filamentous fungi has demonstrated optimum of pH activity from 4.5 to 6.0 differing than that observed for some bacterial inulinases with higher pH of activity. The optimum of temperature for activity for the most inulinases is from 30°C to 55°C but higher temperatures can be also found.
3.3.2. The sucrose and its utilization
Sucrose, a disaccharide constituted by D-glucose and D-fructose linked by α-1,2 glycosidic bond, is the main carbohydrate produced by plants using photosynthesis to generate ATP and NADPH, which will be used in the Calvin Cycle to fix CO2 in the dark step. Two main enzymes are involved in the sucrose synthesis, the sucrose-phosphate syntase (EC 2.4.1.14) and the sucrose-phosphate phosphatase (EC 3.1.3.24) (Winter and Huber, 2000). After the synthesis, the sucrose produced in the photosynthetic leaves is distributed to the other plant organs and tissues. The ethanol production in Brazil is performed using rich-sucrose sugar cane juice. However, after the sucrose extraction, the residual sugar cane bagasse also has residual sucrose that can be used to obtain monosacharides by microbial action. These monomers can be used together with other monosaccharides obtained from the hydrolysis of polysaccharides present in the sugar cane bagasse, as cellulose, to fermentation process. The sucrose hydrolysis (figure 6) is catalyzed by the β-fructofuranosidases (invertases; EC 3.2.1.26), which are found in many microorganisms. The product obtained is an equimolar (1:1) mixture of the monosaccharides and residual sucrose known as invert sugar with wide application in the food and beverage industries. The fructose is much more attractive for application since it can has liquid and non-crystalizable constitution. The β-fructofuranosidases are located in the GH32 family of the glycosil hydrolases and grouped in different isoforms according to their pH of actuation as acid, alkaline and neutral enzymes (Vargas et al., 2003).
Figure 6.
Hydrolysis of sucrose by invertase.
The production of β-fructofuranosidases (FFases) by microorganisms has been characterized, especially for the yeast Saccharomyces cerevisiae. In this microorganism it was observed the synthesis of two isoforms of FFases where one is gylcosylated and another non-glycosylated. Both enzymes are result from the two mRNA (1.8 and 1.9 kb) encoded by the same gene SUC2. The glycosylated enzyme is found in the periplasmic space while the non-glycosylated is found in the citosol (Belcarz et al., 2002). In S. cerevisiae the sucrose metabolism occurs throughout two main ways: i) the sucrose is hydrolyzed in the extracellular environment by extracellular invertases to liberate glucose and fructose, which can be transported to inside of the cell by hexose transporters and ii) the sucrose is actively transported to inside of the cell by proton-symport mechanism and after hydrolyzed by intracellular invertase. The expression of the SUC2 gene that encodes both enzymes is severally regulated by glucose (Basso et al., 2011).
The production of FFases by other microorganism, especially filamentous fungi as Aspergillus genera, among others, has been studied. In this situation, different fermentation processes are used, which many times the residual biomass are used as carbon sources (submerged fermentation) and/or substrates (solid-sate fermentation). Some microorganisms are able to produce multiple β-fructofuranosidases as observed for Aureobasidium pullulans (Yoshikawa et al., 2006). In this situation the authors observed the presence of five FFases (I, II, III, IV and V) with high FFase I activity at the initial times of culture and reduced FFase II-V activities. After initial times the FFase II-V activities are increased. In addition, the multiple FFases produced by A. pullulans have distinct properties as suggested by authors. FFase IV has high hydrolytic activity acting as FOS-degrading enzyme at the FOS-degrading period while the participation of FFases II, III and V is uncertain, since they have significant transfructosylating activity and they are present in the FOS-degrading periods (Yoshikawa et al., 2006).
The most of β-fructofuranosidases are dimmers but monomers also can be found. The optimum of temperature and pH of reaction considering all microbial sources are variable. This carbohydrate has a negative influence on the invertase synthesis by A. niger as well as fructose. Only β-fructofuranoside saccharides were able to induce the invertase synthesis (Rubio & Navarro, 2006). It was observed that the A. niger is able to produce two β-fructosidases known as SUC1 and SUC2. Both enzymes catalyzed the sucrose hydrolysis but only SUC 2 was able to act on inulin. Other fungal strains have been used for invertase production as Aspergillus ochraceus (Guimarães et al., 2007), Aspergillus niveus (Guimarães et al., 2009), Aspergillus caespitosus (Alegre et al., 2009), Aspergillus phoenicis (Rustiguel et al., 2011) and Paecylomyces variotii (Giraldo et al., 2012) using both submerged and solid-state fermentation with agro-industrial residues as carbon source/substrate. Thermostable FFases has been obtained by cultivation of A. ochraceus and A. niveus using sugar cane bagasse as carbon source.
At high sucrose concentration, some β-fructofuranosidases are able to catalyze transfructosylation reaction to obtain fructooligosaccharides (FOS) as 1-kestose (GF2), 1-nystose (GF3) and fructofuranosyl nystose (GF4). The molecular structure of these FOS can be observed in the figure 7. The GF2 is constituted by two molecules of fructose binding to the D-glycosyl unit at the non reducing end while the GF3 and GF4 by three and four fructose residues, respectively. These oligosaccharides have functional properties that have attracted the attention of different sectors. FOS are no caloric sugars that can be used by diabetic peoples with security since they are not metabolized by the organism. In addition, FOS can also stimulate the bifidobacteria development in the intestine and minimize the colon tumor. It has been demonstrated that some components of plant sources (biomass) used in pet foods exhibit FOS concentration of GF2, GF3 and GF4, as for example wheat bran, peanut hulls and barley, among others. The hydrolysis of FOS by microbial sources as bacteria using enzymes that act on these saccharides was demonstrated in some reports. Hence, enzymes that are able to act on FOS can be used to obtain saccharides as glucose from the biomass containing GF2, GF3 and/or GF4. On the other hand, different approaches have been used to obtain FOS as the utilization of immobilized enzymes on lignocellulosic materials and by substrate and enzyme engineering. Recently, the one-step FOS production was obtained using Aspergillus phoenicis biofilms in rich-sucrose medium as demonstrated in our laboratory (Aziani et al., 2012).
In the same way, the fuctosyltransferases as levansucrases (sucrose:2,6-β-fructans: 6-β-D-fructosyltransferase; EC 2.4.1.10), inulosucrases (sucrose:2,1-β-D-fructan: 1-β-D-fructosyltransferase; EC 2.4.1.9) and fructosyltransferase (sucrose:2,6-β-fructan:6-β-D-fructosyltranferase; EC 2.4.1.10) should be considered. The former is responsible by the synthesis of microbial levans using glucose or levan as acceptor to the β-D-fructosyl residues while the inulosucrases are able to catalyze the transference of the β-D-fructosyl residues to the sucrose or inulin as acceptors. The later are involved in the levan synthesis but it is not able to catalyze hydrolysis or exchange reactions as observed for the levansucrase (Velázques-Hernandez et al., 2009). These enzymes that catalyze the fructans synthesis are inserted in the GH68 family of glycoside hydrolases. In general, five main domains are recognized in the fructosyltransferases of microorganisms: a signal peptide; an N-terminal domain with variable length; a catalytic domain with around of 500 amino acids; a cell wall binding domain; and a C-terminal domain with variable length (Van Hijum et al., 2006).
Figure 7.
Molecular structure from the fructooligosaccharides nystose (GF2), 1-kestose (GF3) and fructosyl nystose (GF4).
4. Conclusion
In conclusion, the biomass that has been accumulated around the world as residue can be widely used for different applications considering its carbohydrate composition which can be accessed by microbial activity according to the enzymatic potential of each one. Microorganisms show metabolic versatility permitting the carbohydrate utilization and transformation from biomass since they are important sources of enzymes with biotechnological potential. According to this, different products can be obtained from biomass and applied in different industrial sectors. The view of the biomass as an important renewable energy source is very important to the future of the life in our planet, especially if considered the agro-industrial residues. In addition, the environment problems of bioaccumulation of residues can be reduced. Future studies to improve the biomass utilization are important as well as on the carbohydrate-active enzymes produced by microorganisms to optimize this process.
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Introduction",level:"1"},{id:"sec_2",title:"2. Microbial cultivation using biomass",level:"1"},{id:"sec_3",title:"3. Biomass conversion by microbial enzymes",level:"1"},{id:"sec_3_2",title:"3.1. Cellulases and lignocelullosic biomass ",level:"2"},{id:"sec_4_2",title:"3.2. Amylases, starch sources and structure",level:"2"},{id:"sec_5_2",title:"3.3. Fructosidases and other carbohydrates from biomass ",level:"2"},{id:"sec_5_3",title:"3.3.1. The inulin and its utilization ",level:"3"},{id:"sec_6_3",title:"3.3.2. The sucrose and its utilization ",level:"3"},{id:"sec_9",title:"4. Conclusion",level:"1"}],chapterReferences:[{id:"B1",body:'AlegreA. C. PPolizeliM. L. T. MTerenziH. FJorgeJ. AGuimaraesL. H. S2009Production of thermostable invertases by Aspergillus caespitosus under submerged or solid state fermentation using agro-industrial residues as carbon source. Brazilian Journal of Microbiology, 40612622'},{id:"B2",body:'ArandaCRobledoALoeraOContreras-esquiavelJRodríguezRAguilarC. 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In: Methods in Plant Biochemistry, 2323352Academic Press, Inc., New York.'},{id:"B22",body:'ParadaJAguileraJ. M2011Review: starch matrices and the glycemic responseFood Science Technology International, 17187204'},{id:"B23",body:'Pérez-guerraNTorrado-agrasarALópez-maciasCPastranaL2003Main characteristics and applications of solid substrate fermentation. Electronic Journal of Environmental, Agricultural and Food Chemistry, 2343350'},{id:"B24",body:'RiccaECalabroVCurcioSIorioG2007The state of the art in the production of fructose from inulin enzymatic hydrolysis. Critical Reviews in Biotechnology, 27129145'},{id:"B25",body:'RitteGHeydenreichMMahlowSHaebelSKöttingOSteupM2006Phosphorylation of C6- and C3-positions of glucosyl residues in starch is catalysed by distinct dikinasesFEBS Letters580N° 20, 48724876'},{id:"B26",body:'RubioM. CNavarroA. R2006Regulation of invertase synthesis in Aspergillus nigerEnzyme and Microbial Technology39601606'},{id:"B27",body:'RustiguelC. BOliveiraA. H. CTerenziH. FJorgeJ. AGuimaraesL. H. S2011Biochemical properties of an extracellular β-D-fructofuranosidase II produced by Aspergillus phoenicis under solid-state fermentation using soy bran as substrate. Electronic Journal of Biotechnology, 14N° 2 (doi:vol14-2-fulltext'},{id:"B28",body:'SzydlowskiNRagelPHennen-bierwagenT. APlanchotVMyersA. MMéridaAdHulstCWattebledF. (2011Integrated functions among multiple starch synthases determine both amylopectin chain and branch linkage location in Arabidopsis leaf starch.Journal of Experimental Botany62N° 13, 45474559'},{id:"B29",body:'SzydlowskiNRagelPRaynaudSLucasMRoldanIMonteroMMunozF. JOveckaMBahajiAPlanchotVet al2009Starch granule initiation in Arabidopsis requires the presence of either class IV or class III starch synthases. Plant Cell, 2124432457'},{id:"B30",body:'TeixeiraF. APiresA. VNascimentoP. V. N2007Sugarcane pulp in the feeding of bovine. Revista Eletrônica de Veterinária, 819'},{id:"B31",body:'Van Der MaarelM. J. E. CVan Der VeenBUitdehaagJ. C. MLeemhuisHDijkhuisenL2002Properties and applications of starch-converting enzymes of the α-amylase family.Journal of Biotechnology94137155'},{id:"B32",body:'Van HijumS. A. F. TKraljSOzimekL. KDijkhuizenLVan Geel-schuttenI. G. H2006Structure-function relationships og glucasucrase and fructansucrase enzymes from lactic acid bacteria. Microbiology and Molecular Biology Review, 70157176'},{id:"B33",body:'VargasWCuminoASalernoG. L2003Cyanobacterial alkaline/neutral invertases. Origin of sucrose hydrolysis in the plant cytosol?Planta216951 EOF60 EOF'},{id:"B34",body:'Velázquez-hernándezM. LBaizabal-aguirreV. MBravo-patinoACajero-juárezMChávez-moctezumaM. PValdez-alarcónJ. J2009Microbial fructosyltransferases and the role of fructans. Journal of Applied Microbiology, 106N°6, 17631768'},{id:"B35",body:'VijayaraghavanKYaminiDAmbikaVSowdaminiN. S2009Trends in inulinase production- a review. Critical Reviews in Biotechnology, 296777'},{id:"B36",body:'VillenaG. KGutiérrez-correaM2007Morphological patterns of Aspergillus niger biofilms and pellets related to lignocellulosic enzyme productivities. Letters in Applied Microbiology, 45231237'},{id:"B37",body:'WeiseS. EVan WijkK. JSharkeyT. D2011The role of transitory starch in C(3), CAM, and C(4) metabolism and opportunities for engineering leaf starch accumulation. Journal of Experimental Botany, 6231093118'},{id:"B38",body:'WinterHHuberS. C2000Regulation of sucrose metabolism in higher plants: localization and regulation of activity of key enzymes. Critical Review in Plant Science, 193167'},{id:"B39",body:'YoshimotoYTashironJTakenouchiTTakedaY2000Molecular structure and some physicochemical properties of high amylose barley starch.Cereal Chemistry77279285'}],footnotes:[],contributors:[{corresp:null,contributorFullName:"Luis Henrique Souza Guimarães",address:null,affiliation:'
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1. Introduction
1.1 Anatomy
Proprioception was first described by Sir Charles Bell in 1830s as sixth sense coming from Latin word proprius meaning “one’s own” and perception “perceiving one’s own self” [1]. Proprioception is generally defined as either the sense of position or the motion of the limbs and body in the absence of vision [2]. Limb position is a static sense, whereas limb motion is a dynamic sense [3]. It is described as the most important sensorial modality for the internal representation of body map providing static and dynamic proprioceptive systems [4].
Proprioception is a complex system having both conscious and unconscious components involving peripheral and central pathways. The proprioceptive sensations arise from the deeper tissues. The main receptors are muscle spindles, tendons, Ruffini endings in joint capsules ligaments and Pacinian corpuscles reacting pressure, tension, stretching or contraction. The cutaneous receptors of the skin also contribute to joint position and motion sense especially at digits, elbow and knee. The term kinesthesia is generally used to describe the conscious awareness of the body or limb position in space [1, 5, 6, 7]. Conscious proprioceptive impulses elongate along large and myelinated fibers from the peripheral nerves into the dorsal root ganglion of spinal cord (first order neurons) and then via the medial division of the posterior root, via posterior white columns of fasciculi gracilis and cuneatus and ascend to the nuclei gracilis and cuneatus in the lower medulla. Axons of the second-order neuron decussate as internal arcuate fibers (second order neurons), and then ascend in the medial lemniscus to the contralateral somatosensory region of thalamus (Figure 1) [2, 5].
The main pathway for proprioceptive information is via the dorsal column medial lemniscal, posterior and anterior spinocerebellar tracts and spinoreticular tracts [6, 7].
There is a high density of complex spindles in deeper cervical muscles particularly in the intermediate columns, acting as neck prorioceptive receptors. This system is important for head and neck position sense together with the high density muscle spindles of sub-occipital triange. The density of muscle spindles is higher in the upper cervical spine when compared with the lower cervial and cervico-thoracic and thoraco-lumbar junctions [8]. Neck proprioception plays an important role in limb coordination and body-scheme representation [8]. Proprioceptive impulses from the head and neck are supplied by cranial nerves [5].
Contralateral primary and secondary sensorimotor cortex, supplementary motor area and bilateral inferior parietal lobes and basal ganglia (especially nigrostriatal pathways, striatal neurons and putamen) are involved in processing proprioceptive information during passive movement [9, 10]. The cerebellum contributes to proprioception only during movement [3]. Especially deep medial fastigial nucleus of cerebellum converges vestibular and neck proprioceptive sensory signals describing body’s movement in space [11, 12].
1.2 Proprioception and motor control
The sensorimotor system, defined as the sensory, motor, and central integration, is a crucial and intricate component of the motor control system [13]. Motor control is a complex and dynamic process based on the selective integration of sensory information from multiple sources, motor commands, and motor output [13, 14]. There are specific unique roles associated with each sensory source (i.e., somatosensory, visual, vestibular) that cannot be compensated fully with each other [14, 15]. The environment is experienced through sensory systems: exteroception (e.g., sight, hearing, touch), interoception (e.g., arousal, pain, visceral sensations, muscular sensations), and proprioception (e.g., sense of position, motion, and force), which all required for successful motor control [16, 17]. During a task-oriented activity, motor adaptation, defined as a process of modifying the movement based on error feedback [18], skills are needed to cope with the changes occurring in the external and internal environment [2]. Motor adaptation is stimulated with sensorial triggers by using both feedback (reactive: adjust ongoing motor behavior) and feedforward (preparatory: pre-planning and anticipating the motor sequence from the previous experience) mechanism. Proprioceptive information, from proprioceptors found in muscle, tendon, ligament, capsule, skin, and fascial layers, plays an integral role in motor control and considered as multifold [14].
The role of proprioceptive information in motor control can be divided into two categories: external environment (even vs. uneven ground) and internal environment (carrying a load on shoulders vs. hands below knuckle height). The motor programs often need to be adjusted to accommodate unexpected perturbations or changes in the external environment. Although the source of this information is usually associated mainly with visual input, there are many situations where proprioceptive input is the fastest and/or most accurate. Proprioception is necessary during motion execution to update feedforward commands derived from the visual image [14]. Attention to environmental constraints is also required because dealing with complex environments often requires behavioral flexibility to maintain postural balance [19]. Secondly, the central nervous system needs an updated body schema of the biomechanical and spatial properties of body parts to plan and modify internally generated motor commands [20]. Before and during a motor command, the motor control system must consider the current and changing positions of the respective joints to account for the complex mechanical interactions within the musculoskeletal system components [14] . Additionally, proprioception is important after movement to compare the actual movement and intended movement, besides the predicted movement derived from the efference copies (corollary discharge: copying of motor commands based on past events) of motor commands, which has an essential role in motor learning to update the internal forward model of motor command [21].
1.3 Proprioception and postural control
During the execution of all motor tasks, proprioception is required to prepare, maintain, and restore the stability of both the entire body (postural equilibrium) and the segments (joint stability) [14, 15]. Postural control, defined as controlling the position of the body regarding the task in the environment, involves neural control of “postural equilibrium” and “postural orientation”. Postural equilibrium consists of the coordination of sensory and motor strategies to maintain balance by controlling the body’s center of mass (COM) over its base of support (BOS) to maintain postural stability during both intrinsic (self-initiated) and extrinsic (externally triggered) disturbances. The postural equilibrium controls stability during both static (i.e., quiet standing) and dynamic (i.e., walking and reaching) situations. Postural orientation involves positioning body alignment with respect to gravity, the support surface, visual environment, and other sensory reference frames [22].
Postural control is considered as a complex motor skill derived from the interaction of multiple sensorimotor processes, which are; biomechanical constraints (i.e., BOS, degrees of freedom, strength, limits of stability), movement strategies (i.e., reactive, anticipatory, voluntary), sensory strategies (i.e., sensory integration, sensory re-weighting), orientation in space (i.e., perception of visional verticality, perception of postural verticality), control of dynamics (i.e., gait, proactive), cognitive processing (i.e., attention, learning, reaction time), experience and practice [23]. Impairment of the proprioceptive sensation can disrupt any of these six resources, which contributes to postural control (Figure 2). “Sensory strategies” are one of the most critical issues to discuss. Sensory information from somatosensory (tactile sense and proprioception), visual and vestibular systems must be integrated to interpret complex sensory environments for achieving postural control. Depending on the environmental conditions, the relative contribution of each sensory system changes, which is referred to as “sensory re-weighting” [24]. Healthy persons rely on somatosensory (70%), vision (10%), and vestibular (20%) information when standing on a stable surface in a well-lit environment (13). On the other hand, when standing on an unstable surface, due to decreased dependence on surface somatosensory inputs for postural orientation, they need to increase sensory weighting to vestibular and visual information [25]. The dynamic regulation or re-weighting of sensory cues is essential for maintaining postural stability when moving between different environments requiring distinct sensorial systems, such as different surfaces (i.e., walking on the sidewalk, walking on grass) or different lighting (i.e., moving in a well-lit room, moving in a dark room) [23]. The interplay between these three sensory modalities is critical for accurate estimates of self-motion and postural control [26].
Figure 1.
Neuroanatomic pathway adopted from DeJong’s the neurologic examination.
Besides different sensory cues, different mechanical conditions provide significant advantages to humans for maintaining upright standing [27]. Decreased proprioception could lead to “biomechanical constraints” such as abnormal joint biomechanics and decreased muscle strength [28, 29], leading to postural dyscontrol. The “control of dynamics” is defined as the ability to perceive body segments relative to one another to stabilize the COM. Maintaining COM requires input from multiple sensory systems, sensorial re-weighting, and multisensory integration to calculate body state, including the COM and heading [30]. “Movement strategies” (i.e., postural sway, ankle strategy, hip strategy) can be used to return the body to equilibrium in a stance position [23]. Without proprioceptive input from the ankle and knee, ankle muscle responses are delayed suggesting that lower leg balance correcting responses are triggered by hip and, possibly, trunk proprioceptive inputs. Especially hip muscle proprioceptive inputs, considered critical for automatic balance correcting responses [31]. Additionally, cervical proprioception is of particular importance for “orientation in space”. Neck muscle inflow has effects on the perception of body orientation and motion. Prolonged, intense proprioceptive input from neck muscles can induce persistent influences on self-motion perception and cognitive body representation [32]. The loss of proprioception could also impact the “cognitive processing” specifically the reaction time, and other factors such as attention, memory, and visuospatial abilities may contribute to spatial cognitive skills (Figure 2) [23].
Figure 2.
Adapted from the framework of the six important resources required for postural control system by Horak, 2006 [23], the contribution of proprioception sensation to postural control.
2. Clinical implications and evaluation of proprioception
The loss of proprioceptive afferents may affect the control of muscle tone, disrupts postural reflexes, and severely impairs spatial and temporal aspects of movement [33]. Proprioceptive impairments are associated with various neurological conditions such as stroke [34], Parkinson’s disease [35], peripheral neuropathy [36], as well as orthopedic conditions such as low back pain [37], neck pain [38], sports injuries like chronic ankle instability [39], ACL injuries [40], post-operatively such as mastectomy [41], knee arthroplasty [42], and aging [43]. Considering the importance of proprioception for motor control, a detailed evaluation of proprioceptive sense and application of treatment approaches focusing on training the proprioceptive sense is important for restoring motor function. Proprioception can be measured by using specific and non-specific tests in clinical practice.
Specific Tests of Proprioception: assess an individual’s status regarding the joint position sense and kinesthesia [21]. Joint position sense tests assess precision or accuracy in repositioning the joint at a predetermined target angle and can be measured as active joint position detection (AJPD) [e.g., position matching task, position copying task] and passive joint position detection (PJPD) [e.g., thumb finding test, dual-joint position test] [44]. Kinesthesia tests assess the ability to perceive joint movement. For evaluating the perceptual aspect of proprioception, psychophysical thresholds represent the gold standard [33]. These tests are usually performed passively and can be measured by using passive motion detection threshold (PMDT) and passive motion direction discrimination (PMDD) [e.g., distal proprioception test, Rivermead Assessment of Somatosensory Perception] [44].
Non-specific Tests of Proprioception: for determining the contribution of proprioceptive signals on balance control, functional balance tests can be used to provide an estimate of potential proprioceptive disturbances [33]. These tests involve all body and other sensory and motor functions; therefore, they are considered non-specific tests of proprioception [21]. Balance tests can be modified to challenge proprioception, such as unilateral/bilateral stance with eyes open/closed, different supporting surfaces (i.e., stable or unstable), and with/without perturbations [44, 45]. Stereognosis and skilled motor function tests are important as they indicate the contribution of proprioceptive system in the performance of many activities of daily living [46].
3. Neurologic correlation
The complexity of sensorimotor systems requires deep knowledge of anatomy and physiology to analyze and localize the symptoms and the signs of the patients. Joint sense and vibration sense examination is an important component of neurological examination.
The classic diseases causing sensory ataxia are tabes dorsalis, polyneuropathies (especially involving large fibers), dorsal root ganglionopathies and subacute combined degeneration. With parietal lobe lesion, position sense is often impaired and vibration preserved [5]. Vibratory sensation may also be impaired in lesions of the peripheral nerves, plexopathies, radiculopathies, dorsal root ganglion, posterior columns and medial lemniscus. In patients with peripheral neuropathies, vibration sensation is lost in the lower extremities first. Impaired vibration from posterior column disease is more likely to be uniform at all sites in the involved extremities. In spinal cord diseases, detecting a “level” of vibration sensory (segmental demarcation) loss over the spinous processes is crucial for diagnosis [5]. In patients with diabetic neuropathy, the decline in proprioceptive function may be caused by impairment in muscle spindle function and or the spindle receptors itself [47].
In patients with hereditary sensory and autonomic neuropathy type III patients (Riley-Day Syndrome, familial dysautonomia) ataxic gait is explained by poor proprioceptive acuity at the knee joint [48]. In mitochondrial ataxias sensory ataxia (which classically include gait ataxia worsened by loss of visual fixation) is due to the involvement of proprioception, secondary to peripheral neuropathy or neuronopathy [49]. In patients following whiplash type injuries involving soft tissues of cervical spine leads to proprioceptive deficits affecting head and position sense. Also in patients with chronic whiplash associated disorders are reported to have balance and dizziness problems, head and eye movement impairments reflecting mismatch od afferent input from the proprioceptive, visual and vestibular systems [8, 50]. Lesions of the dorsal columns impairs sensation of touch, vibration and proprioception in the ipsilateral side of the body below the injury level [51]. In patients with non-specific low back pain, postural control is impaired during standing and slow performance movements. This is due to an altered use of ankle compared to back proprioception related activity in right primary motor cortex and frontoparietal cortex [52]. Brainstem lesions resemble those in spinal cord disease as it selectively involves spinothalamic tract or medial lemniscus causing contralateral loss of position sense and vibration sense [5].
Neglect is a condition in which patients loose self-spatial awareness opposite to the damaged site of the brain. It is proposed that it is associated with the lesions of the dorsal stream causing dysfunction of proprioceptive space which is encoded in the bilateral parietal cortex [53]. Loss in the position sense may cause pseudochoreoathetosis as well. This abnormal involuntary, spontaneous movements are restricted to the parts with proprioceptive sensory loss. It is proposed that failure to integrate cortical proprioceptive sensory inputs in striatum may explain this situation [5, 54].
There are experimental evidence of proprioception impairments in Parkinson’s disease. Parkinsonian gait is affected by the involvement of lower limb proprioceptive deficits as well as the involvement contralateral somatosensory and premotor lateral cortices and posterior cingulate cortex and basal ganglia and bilateral prefrontal cortex [10, 55, 56]. It was also shown that conscious perception of kinaesthetic stimuli is impaired in Parkinson’s disease as cerebro-basal loops are not intact [9].
Weeks and colleagues showed that patients with cerebellar damage had reduced dynamic proprioceptive acuity which was also parallel to their motor deficits [3]. Diseases of the primary somatosensory cortex do not generally produce sensory symptoms but deteriorate fine and delicate manipulations in the contralateral part depending on position sense [2, 5]. Many patients with stroke experience proprioceptive deficits. Recovery of proprioception increases in the chronic phase [57, 58]. In study by Pope it was shown that proprioceptive input from the neck also may change cerebellar output affecting M1 plasticity [59]. In the study of Vidoni and colleagues preserved motor learning after stroke was related to the degree of proprioceptive deficit suggesting the relation between proprioceptive perception from muscle spindles and motor learning and central neuroplasticity [58, 60].
4. Proprioception after orthopedic surgeries
Studies on changes in joint proprioception after orthopedic surgeries are available in the literature. This section consists of the information in the literature about our five major joints.
4.1 Knee joint
Knee proprioception is necessary to achieve normal joint coordination during movement as well as providing joint stabilization [61, 62]. The anterior cruciate ligament (ACL), posterior cruciate ligament, collateral ligaments and menisci contribute to proprioception with the help of proprioceptors they have [63, 64]. The mechanoreceptors of the cruciate ligaments, together with the mechanoreceptors of the joint capsule, transmit information about the extension and flexion of the knee joint to the brain [65].
The ACL is the most important ligament involved in knee mechanical and neuromuscular stability. It contributes to proprioception in joint movement. However, the ACL is the most frequently injured ligament. After ACL rupture, knee proprioception is disrupted [66, 67].
Various autografts and allografts are used for ACL reconstruction. Patellar tendon or hamstring tendons may be preferred in patients using autografts. In addition, different techniques and materials are used. However, there is no gold standard in graft and technique selection [68]. In order for ACL reconstruction to be successful, not only mechanical but also neuromuscular stability is required. Neuromuscular stability depends on obtaining proprioception [69]. ACL injury leads to degradation of mechanoreceptors and a histologic study revealed that free nerve endings disappear after 1 year [70]. The effectiveness of ACL reconstruction in regaining proprioception has been tried to be revealed by some studies [71, 72, 73, 74]. While some studies argue that ACL reconstruction is not sufficient to restore joint position [71, 72, 73], some studies advocate the adverse opinion [74]. The lack of a test to distinguish about whether the proprioception is derived from the soft tissues around the knee and capsule or from mechanoreceptors on ACL prevents to reach a certain decision about the mechanoreceptors of ACL [75].
Even after total knee arthroplasty, the contribution of the soft tissues around the knee to proprioception continues. In order to take advantage of this effect and ensure satisfactory outcomes in these patients, the soft tissue and gap must be well adjusted. Unicompartmental replacement protecting the ACL may be more advantageous in not reducing proprioception due to the proprioceptive effect of ACL. Also Ishii et al. [76] conclude that balance is improved after the postoperative period in bilateral total knee arthroplasty. It is stated that the first 6-week period is the critical period for adaptation time and proprioceptive loss after total knee replacement, and a new pattern in the knee load distribution occurs with postoperative rehabilitation [77].
4.2 Hip joint
Loss of proprioception, balance, sensation as joint position and kinesthetic are frequently observed in patients with knee osteoarthritis [78, 79]. Shakoor et al. [80] described significant sensory deficits associated with hip osteoarthritis, and these deficiencies involved both upper and lower limbs. The mechanism for this remains unclear; however, it has been suggested that there may be neurological feedback mechanisms or a inherent generalized neurological defect [78].
The greatest portion of mechanoreceptors and free nerve endings and highest concentration of pain receptors are located in the anterosuperior, posterosuperior and anterolateral labrum, respectively [81, 82].
There is no satisfactory information about proprioception impairment after surgeries due to hip pathologies. In the literature on the relationship between arthroplasty and proprioception, there are studies related to the knee rather than the hip. Interestingly, Ishii et al. [83] found no difference in proprioceptive responses among participants in the total hip arthroplasty, hemiarthroplasty and healthy control groups. They thought that the mechanoreceptors in the muscles, tendons and ligaments were responsible for joint proprioception rather than the intracapsular structures. While capsular receptors play a secondary role, muscle receptors play a primary role in hip proprioception. Therefore, it has been suggested that proprioception does not decrease after surgery, despite the capsule being removed during arthroplasty [84].
The effects of FAI and labral tear treatments on proprioception are not well known, but due to their proprioceptive properties, hip musculotendinous and capsuloligamentous tissues contribute to lower limb posture and stabilization through neuromuscular control. Therefore, preserving proprioceptive tissues as much as possible will prevent lower extremity injuries in arthroscopy operations.
4.3 Ankle joint
Ankle injuries are in the first place in sports-related injuries and lateral ankle sprains constitute the majority of this [85]. Unfortunately, many of these acute injuries can become chronic [86, 87]. Training, fatigue, and ankle injuries can affect ankle proprioception. Joint position sense, peroneal reaction time, EMG evaluation of peroneal muscles, and balance tests are tools to evaluate proprioception before and after ankle injuries or surgeries.
There are two important anatomical structures that provide proprioception and are located around the foot and ankle. Superior and inferior extensor retinaculum act as a pulley protecting tendons close to bony structures. The lateral ankle complex is the other anatomical structure with proprioceptive properties [88, 89]. Both acute and chronic injuries of the ankle can predispose the proprioceptors of the ankle. The differentiation in proprioception after these injuries were presented in the literature. While Vries et al. [90] stated that there was no difference between chronic ankle injury, acute trauma and healthy control groups, there are studies suggested that proprioception after acute inversion injuries and chronic ankle injuries are decreased [91, 92, 93]. Recovery of the proprioception is crucial after ankle injuries to maintain balance control. In order to achieve this, rehabilitation should not be neglected, especially after lateral ankle sprains.
A study conducted by Conti et al. [94] found no difference in proprioception between operated and non-operated side in total ankle arthroplasty. However, ankle arthroplasty has the worst outcome in terms of proprioception and balance compared to total hip and knee arthroplasty [95].
4.4 Shoulder joint
Some studies have revealed Pacinian corpuscles and Golgi tendon organ with mechanoreceptors in the shoulder [96, 97]. However, they discovered that while there are free nerve endings in the labrum and subacromial bursa, these structures do not contain mechanoreceptors. It is also thought that the supraspinatus muscle has more receptors than the infraspinatus muscle contains [98].
The pathological conditions of the shoulder joint can affect shoulder proprioception. Surgical shoulder diseases include rotator cuff tears, subcacromial pathologies, biceps tendon diseases and instabilities. Studies comparing pre- and post-surgical proprioception in the shoulder joint are not sufficient. In a study conducted by Aydın et al. [99], it was revealed that there was no difference in terms of proprioception between surgically treated and non-surgically treated shoulders in cases of instability. Duzgun et al. [100] stated a rapid recovery in shoulder joint proprioception after rotator cuff surgery as their experience.
Shoulder arthroplasty is thought to negatively affect proprioception. It has been stated that intervention to the subscapularis muscle and glenohumeral ligaments during shoulder arthroplasty may be effective in this decrease in proprioception [101, 102].
4.5 Elbow joint
Soft tissue damage is significant in elbow arthroplasty. Both flexor and extensor muscles are affected, collateral ligaments are released and capsule is removed. Therefore, the proprioceptive tissues as like skin, capsule, muscle and tendons are damaged. Despite the role of proprioception is still not well-established, one study was found an impairment in proprioception after total elbow arthroplasty [103].
In conclusion, proprioception may be adversely affected after joint surgeries. It should definitely be included in the rehabilitation program considering this situation. Proprioception seems to be an important factor for gaining balance and gait speed, especially after arthroplasties in the lower extremity.
Conflict of interest
The authors declare no conflict of interest.
\n',keywords:"proprioception, neurology, orthopedics",chapterPDFUrl:"https://cdn.intechopen.com/pdfs/75009.pdf",chapterXML:"https://mts.intechopen.com/source/xml/75009.xml",downloadPdfUrl:"/chapter/pdf-download/75009",previewPdfUrl:"/chapter/pdf-preview/75009",totalDownloads:48,totalViews:0,totalCrossrefCites:0,dateSubmitted:"October 22nd 2020",dateReviewed:"January 7th 2021",datePrePublished:"February 5th 2021",datePublished:null,dateFinished:"February 1st 2021",readingETA:"0",abstract:"Proprioception is the sense of position or the motion of the limbs and body in the absence of vision. It is a complex system having both conscious and unconscious components involving peripheral and central pathways. The complexity of sensorimotor systems requires deep knowledge of anatomy and physiology to analyze and localize the symptoms and the signs of the patients. Joint sense and vibration sense examination is an important component of physical examination. This chapter consists anatomy, motor control, postural control related to proprioception with neurologic clinical correlation and also the information about the changes of proprioception after orthopedic surgeries and discuss with the available literature.",reviewType:"peer-reviewed",bibtexUrl:"/chapter/bibtex/75009",risUrl:"/chapter/ris/75009",signatures:"Pinar Gelener, Gözde İyigün and Ramadan Özmanevra",book:{id:"10554",title:"Proprioception",subtitle:null,fullTitle:"Proprioception",slug:null,publishedDate:null,bookSignature:"Prof. José A. Vega and Dr. Juan Cobo",coverURL:"https://cdn.intechopen.com/books/images_new/10554.jpg",licenceType:"CC BY 3.0",editedByType:null,editors:[{id:"59892",title:"Prof.",name:"José A.",middleName:null,surname:"Vega",slug:"jose-a.-vega",fullName:"José A. Vega"}],productType:{id:"1",title:"Edited Volume",chapterContentType:"chapter",authoredCaption:"Edited by"}},authors:null,sections:[{id:"sec_1",title:"1. Introduction",level:"1"},{id:"sec_1_2",title:"1.1 Anatomy",level:"2"},{id:"sec_2_2",title:"1.2 Proprioception and motor control",level:"2"},{id:"sec_3_2",title:"1.3 Proprioception and postural control",level:"2"},{id:"sec_5",title:"2. Clinical implications and evaluation of proprioception",level:"1"},{id:"sec_6",title:"3. Neurologic correlation",level:"1"},{id:"sec_7",title:"4. Proprioception after orthopedic surgeries",level:"1"},{id:"sec_7_2",title:"4.1 Knee joint",level:"2"},{id:"sec_8_2",title:"4.2 Hip joint",level:"2"},{id:"sec_9_2",title:"4.3 Ankle joint",level:"2"},{id:"sec_10_2",title:"4.4 Shoulder joint",level:"2"},{id:"sec_11_2",title:"4.5 Elbow joint",level:"2"},{id:"sec_16",title:"Conflict of interest",level:"1"}],chapterReferences:[{id:"B1",body:'Hillier S, Immink M, Thewlis D. Assessing proprioception: a systematic review of possibilities. Neurorehabilitation and neural repair. 2015;29(10):933-949. DOI:10.1177/1545968315573055'},{id:"B2",body:'Gilman S. 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DOI: 10.1016/j.brainresbull.2007.03.010.'},{id:"B99",body:'Aydin T, Yildiz Y, Yanmiş I, Yildiz C, Kalyon TA. Shoulder proprioception: a comparison between shoulder joint in healthy and surgically repaired shoulders. Arch Orthop Trauma Surg. 2001;121(7):422-425. DOI: 10.1007/s004020000245.'},{id:"B100",body:'Duzgun, I., & Turhan, E. (2017). Proprioception After Shoulder Injury, Surgery, and Rehabilitation. Proprioception in Orthopaedics, Sports Medicine and Rehabilitation, 35-45. DOI:10.1007/978-3-319-66640-2_4.'},{id:"B101",body:'Maier MW, Niklasch M, Dreher T, Wolf SI, Zeifang F, Loew M, Kasten P. Proprioception 3 years after shoulder arthroplasty in 3D motion analysis: a prospective study. Arch Orthop Trauma Surg. 2012;132(7):1003-1010. DOI: 10.1007/s00402-012-1495-6'},{id:"B102",body:'Kasten P, Maier M, Retting O, Raiss P, Wolf S, Loew M. Proprioception in total, hemi- and reverse shoulder arthroplasty in 3D motion analyses: a prospective study. Int Orthop. 2009;33(6):1641-1647. DOI: 10.1007/s00264-008-0666-0.'},{id:"B103",body:'Lubiatowski P, Olczak I, Lisiewicz E, Ogrodowicz P, Bręborowicz M, Romanowski L. Elbow joint position sense after total elbow arthroplasty. J Shoulder Elbow Surg. 2014;23(5):693-700. DOI: 10.1016/j.jse.2014.01.016.'}],footnotes:[],contributors:[{corresp:"yes",contributorFullName:"Pinar Gelener",address:"drpinargelener@gmail.com",affiliation:'
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