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Journal of Cleaner Production 172 (2018) 3713e3720

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Journal of Cleaner Production

journal homepage: www.elsevier .com/locate/ jc lepro

Biotechnological revalorization of Tequila waste and by-productstreams for cleaner production e A review from bio-refineryperspective

Gibr�an S. Alem�an-Nava a, Ilaria Alessandra Gatti a, Roberto Parra-Saldivar a, **,Jean-Francois Dallemand b, Bruce E. Rittmann a, c, Hafiz M.N. Iqbal a, *

a Tecnologico de Monterrey, School of Engineering and Science, Campus Monterrey, Ave. Eugenio Garza Sada 2501, Monterrey, N.L., CP 64849, Mexicob European Commission, Joint Research Centre, Directorate for Energy, Transport & Climate, Via E. Fermi 2749, TP 450, 21027, Ispra, VA, Italyc Biodesign Swette Center for Environmental Biotechnology, Arizona State University, Tempe, PO Box 875701, Tempe, AZ, USA

a r t i c l e i n f o

Article history:Received 28 June 2016Received in revised form17 July 2017Accepted 17 July 2017Available online 24 July 2017

Keywords:AgaveBagasseGreen biotechnologyVinassesWaste valorization

* Corresponding author.** Corresponding author.

E-mail addresses: r.parra@itesm.mx (R. Parrwestminster.ac.uk, hafiz.iqbal@itesm.mx (H.M.N. Iqba

http://dx.doi.org/10.1016/j.jclepro.2017.07.1340959-6526/© 2017 Elsevier Ltd. All rights reserved.

a b s t r a c t

In this paper, industrial processing and biotechnological revalorization of Tequila waste and by-productstreams have been reviewed. Tequila production process generates different kind of waste and by-products with a huge potential to produce value-added products. Therefore, many research projects,scientific investigations and innovative utilizations of such waste and by-product streams have been theobject of recent studies. Moreover, the bio-based transformation from a petrochemical-based economy toa bio-based economy necessitates the novel exploitation of cost-effective natural materials for bothfuture biorefinery development and a range of value-added products of interests. The present reviewarticle focuses on an area not comprehensively reviewed previously, the potential of utilizing waste andby-product streams from current Tequila industry activities. The first part of this review focused onvarious processing aspects and prospects on the fermentative production of Tequila. In the second andthird parts, statistical and sustainable aspects and the generation of waste and by-product streams ofTequila industry are critically reviewed, respectively. In the fourth part, various industrial and biotech-nological applications of Tequila’s wastes are comprehensively discussed from a bio-refinery perspective.In conclusion, it is evident that biotransformation of waste and by-product streams has great potentialand significant prospects for wider industrial and biotechnological applications.

© 2017 Elsevier Ltd. All rights reserved.

1. Introduction

Tequila is a Mexican alcoholic beverage, both production andcommercialization are verified and certified by the Mexican TequilaRegulatory Council (CRT) (L�opez-Alvarez et al., 2012; Nava-Cruzet al., 2015). According to the norm, Tequila has to be preparedfrom the heads of the Agave Tequilana Weber var. azul, hydrolyzedor cooked, and then subjected to alcoholic fermentations withyeast. With 219 producers and 1648 brand names, Tequila wasregistered from the CRT in 2014. Tequila industry signifies animportant economic boost for the 180 municipalities within the

a-Saldivar), hafiz.iqbal@my.l).

Denomination of Origin territory (CRT, 2014). The protected terri-tories by the tequila denomination of origin, Jalisco, Nayarit, Gua-najuato, and Tamaulipas states with 8, 6, 29 and 12 municipalities,respectively, are shown in Fig. 1 (I~niguez-Covarrubias et al., 2001a).The complex cultivation of agave has always complicated supplyand demand patterns. The fact that the plant takes 6e10 years tomature after being planted has repeatedly caused cycles of shortageand surplus of agave, as can be noticed in Fig. 2. This kind of trendhas progressively made it difficult for supply chain actors to suc-cessfully coordinate the supply of agave with the demand forTequila.

The agave waste from the Tequila industry has a great potentialfor biotransformation into value-added products. Awider spectrumof high-added value products with industrial interests e.g. platformchemicals including enzymes, fuels, and electricity, bioactive mol-ecules for nutraceutical, pharmaceutical, biomedical and biotech-nological sectors of the modern world, can be obtained using

Fig. 1. Protected territories by the tequila denomination of origin, Jalisco and Nayarit,Guanajuato, and Tamaulipas states with 8, 6, 29 and 12 municipalities, respectively(Reproduced from I~niguez-Covarrubias et al., 2001a, with permission from Elsevier).

Fig. 2. Tequila production and agave demand from 1995 to 2013.

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naturally abundant materials such as agave and otherlignocellulosic-based materials (Bilal et al., 2017; Arevalo-Gallegoset al., 2017). Therefore, biomass waste (re)-valorization hasrecently emerged. There have been many contributions in utilizingwaste biomass both from plant and animal wastes and reviewedelsewhere (Iqbal et al., 2013; Liguori et al., 2013; Santiba~nez-Aguilaret al., 2014; Sukumara et al., 2014; Xu et al., 2014; Evcan and Tari,2015; Fern�andez-Rodríguez et al., 2016; Gallegos et al., 2016;Masran et al., 2016; Narron et al., 2016; Putro et al., 2016;Rouches et al., 2016; Zhang et al., 2016). However, the present re-view mainly focuses on an area not comprehensively reviewedpreviously, the potential of utilizing waste and by-product streamsfrom current Tequila industry activities. The part of the reviewfocused on various processing aspects and prospects industrial andbiotechnological applications of Tequila’s wastes from a bio-refinery perspective.

2. Tequila production process

The Tequila production process starts with the harvesting of theagave plants considered to be mature enough: the sugar content isat a maximumwhen the plant is approximately 10 years old. Plantswho are not deemed to be ready yet are left to complete thegrowth. The harvesting consists in bluntly cutting the leaves from

the agave, to be able to extract the head (also known as “pi~na”) fromthe ground. The heads are then transported to the distillery, wherea sample of each head is taken and analyzed to determine reducingsugar content (an indicator of the amount of inulin), along withmany other critical parameters e.g. moisture content, ash content,processing temperature and pH. Moreover, to further facilitate auniform cooking and handling during the production process, thehead parts of the agave plant are sliced into small pieces. Agaveleaves represent the 46% of the whole plant weight and usually leftin the field during harvesting process (Cede~no Cruz and AlvarezJacobs, 1991; I~niguez-Covarrubias et al., 2001a,b; Corbin et al.,2015).

The next phase is the cooking, which hydrolyzes the complexcarbohydrates (inulin) of the agave heads into simple sugars(fructose and sucrose) which are suitable for fermentation pro-cesses. It also softens the heads to make the process of sugarextraction easier. The traditional cooking takes place in brick orstone ovens, and it is a process that lasts from 50 to 72 h and in-volves steam injection. More modern versions of this processusually take place in autoclaves of several tons capacity: the highersealed capability of these tanks allows the required time for thisprocess to be reduced to 14 or even 8 h. After a stipulated cookingtime, a sweet liquid i.e. mainly fructose is collected and used later asa source of free sugars.

Fermentation follows the sugar extraction via traditionalextraction method. Fermentation time varies depending on envi-ronmental temperature, but it usually lasts many hours and differsamong factories due to different standards applied. Once thefermentation process is concluded, and the must have reached analcoholic content of 5e7%, it can be left to settle a few hours beforemoving onto the distillation stage. The fermented must was thenused to separate further and concentrate the alcohol contents viaprocess distillation. Tequila is usually distilled twice. The firstdistillation is known as “destrozamiento”: it takes a couple ofhours, and it yields the “Tequila Ordinario”, meaning a liquid withan alcohol level of around 20%. The second distillation, also knownas “rectificaci�on”, takes between 3 and 4 h. The result of this processis a liquid with an alcohol level near 55%, also known as “TequilaBlanco”. This product can be sold, or it can be aged to becomeanother type of Tequila. Distillation phase generates a liquid wastecalled vinasses, which remains in the bottom of the still. In a typicalTequila distillery, 7e10 L of this effluent are produced per liter ofTequila. Due to their low pH, high temperature, and high organicloads, they represent a significant disposal problem. Fig. 3 illus-trates a schematic diagram of the Tequila production process.

3. Sustainability of tequila industry

3.1. Economic and social sustainability

In the 1990s, a fungal infection and an early winter frost, alongwith the usual cycles of surplus and shortage, caused a decrease of50.7% in the blue agave population in Jalisco (Gonz�alez, 2002;Bowen and Zapata, 2009; Figueroa-Castro et al., 2013). Theshortage consequences were amplified by the increased popularityof Tequila in domestic and international markets and pushed manysmall Tequila companies out of the market (Bowen and Zapata,2009). This crisis led to several changes in the production re-lations of the Tequila industry:

� Agave production expanded into new areas, where there was notraditional agave cultivation (Macías, 2001)

� The main tequila producing sectors became more self-sufficientin their agave supply, to avoid and tackle the associated risks ofsurplus and shortage (Bowen, 2008)

Fig. 3. A schematic illustration of Tequila production process using agave as a potentsubstrate.

G.S. Alem�an-Nava et al. / Journal of Cleaner Production 172 (2018) 3713e3720 3715

� Tequila industry became more concentrated, with major firmscontrolling the majority of the market

� Formerly Mexican firms were bought by multinational com-panies (Casas, 2006).

As a result, without a proper intervention, local Mexican tradi-tions, and culture connected to the Tequila production process riskto be prejudiced irreparably.

3.2. Environmental sustainability

From the environmental point of view, the explosion of theTequila market started in the 1990s has caused the need forintensifying and expanding agave cultivations. This situation, alongwith federal government restrictions on the variety of agave to beused to produce Tequila has an adverse effect on other varieties ofagave progressively used previously for the same purpose, leadingto a reduction of the biodiversity in the region. The Agave TequilanaWeber var. azul is a semelparous plant, meaning that once itflowers, it dies. Its reproduction can be sexual, by seeds, or asexual,by offshoots from rhizomes or bulbils from the inflorescence. ForTequila production purposes, rather than allowing the plant togrow the flower to attract pollinating birds, bats, and moths thatfeed on the nectar, the flower stalk is cut as soon as it begins tosprout, interrupting in this way the flowering process. The reason isthat during the flowering process the plant consumes its reserve ofcarbohydrates and then dies. The nineties explosion of the Tequilamarket encouraged growers to continue the traditional practice ofremoving the inflorescence before fertilization and seed formationoccurs and using the vegetation propagation (asexual reproduc-tion) exclusively for producing new plants. This overuse of asexualreproduction has in time created whole fields of genetically iden-tical blue agaves. The cultivation of a single, preferred genotype is avery common practice in commercial agriculture. However, it isusually available a base of genetic variation for the crop species thatcan be exploited if needed. Recent studies have shown that it is avery different case for the Agave Tequilana Weber var. azul: one ofthe lowest levels of polymorphism to date was detected for thisspecies. It, therefore, appears to be no readily available base ofgenetic variation for this variety of agave (Vega et al., 2001).

The Agave Tequilana has been considered to have a minimalimpact on soil fertility due to its unusually long harvesting cycle.The shallow rooting system and succulent morphology also facili-tate its environmental adaptation in desert regions. This is mainlydue to its crassulacean acid metabolism (CAM photosynthesis),which allows a carbon fixation pathway with minimum loss ofwater. These factors have contributed to the success of the culti-vation of the Agave used in Tequila production. In the past 20 years,though, the rising global consumption of Tequila and the conse-quent increase in the cultivation of agave have newly prompted

questions regarding its impact on soil composition and character-istics. Another common practice is to allow livestock to graze onmature fields, as it is supposed to be beneficial for controllingweeds andmanure distribution over the fields as a fertilizer. A thirdcommon practice is to treat the field with the distillery effluent,vinasses. The disposal of this effluent had become difficult andexpensive due to new and stricter regulations. As a result, Tequilacompanies started to use it as an organic fertilizer. It also appearedthat it brought elevated soil calcium and foliar phosphorus andmagnesium (Monroy Reyes, 1999), which was considered to bebeneficial for the agave cultivation. Recent studies have examinedthe effects of the common agricultural practices involved in theblue agave cultivation on soil fertility (Gobeille et al., 2006). Prac-tices of tillage, livestock grazing and field amendment with dis-tillery effluent were studied. The addition of distillery effluent wasfound to increase mean levels of soil phosphorus, potassium, cal-cium, and boron, as well as CEC (cation exchange capacity). Theseresults show that blue agave cultivation stimulates the depletion ofsoil nutrients and alters soil physical properties. Whether a loweravailability of soil nutrients is associated with reduced productivityor not is yet to be ascertained.

4. Generation of wastes e problematic issue

The production process of Tequila generates a considerableamount of waste. Fig. 4 shows the amount of waste generated perliter of Tequila produced. As these numbers want to prove, thedisposal of Tequila industry waste has increasingly become aproblem for Tequila producers, due to the growing market.

Agave Tequilana Weber var. azul leaves typically are 90e120 cmin length and 8e12 cm in width, firm fibrous, rigid, acuminate andconcave, generally blue or gray-green in color (Gentry, 2004;Chattopadhyay and Khan, 2012; Hulle et al., 2015). The parts ofthe leaves are cut off from the base of the plant during the har-vesting and are left in the field to recycle nutrients or amassed inwide spaces, unused. It was found that the wet agave head repre-sents the 54% of the plant in mass, while the remaining 46% is madeof leaves, meaning that almost half of the plant usually remainsunused (I~niguez-Covarrubias et al., 2001a,b).

The residual material left behind after the harvesting andcooking of head part following mining and washing for sugarextraction is usually termed as agave bagasse, which is fibrous innature. It is composed of thick-walled and long fiber (approxi-mately 5e10 cm) and pith (I~niguez-Covarrubias et al., 2001a,b).Table 1 shows physical composition and chemical composition ofdry agave bagasse at 5% water content (I~niguez-Covarrubias et al.,2014). Moreover, most of the bagasse is not utilized at all, causingillegal dumping or improper applications on agricultural land,along with pollution by leachates, odor generation and habitat forpests and diseases (Rodriguez, 2013). The solution to the problem offinal disposal of agave bagasse is to find an appropriate technologyfor indirect assessment and treatment, so that it can be integratedinto the environment (manure, compost), within the food chain(forage, fodder yeast), or in industrial processes of economic in-terest (paper pulp, agglomerated materials).

Vinasses represent significant disposal and treatment problemsdue to their complex physicochemical composition. Table 2 showsthe physio-chemical characteristics of Tequila vinasses in detail.They are usually toxic in natural, particularly for micro-organisms,along with some anti-oxidant features and are among potentialcandidates for waste management (L�opez-L�opez et al., 2010). Withever increasing scientific knowledge, ecological awareness anddemands from the legislative authorities, an eco-friendly remedi-ation treatment is an absolute requirement to save the currentecological system. Fig. 5 illustrates a tentative pilot plant scheme

Fig. 4. Waste generation per liter of Tequila produced.

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for the treatment of Tequila vinasses.

Table 2Physio-chemical characteristics of Tequila vinasses.

Parameter Value

pH 3.4e4.5Oils and fats (mg/L) 10e100Total COD (mg/L) 60,000e100,000Soluble COD (mg/L) 40,000e80,000

5. Biorefinery from Tequila’s waste

5.1. Agave leaves as fiber source for paper products

The paper is considered a ubiquitous product, in nature, andused for many applications in our daily lives (Manda et al., 2012).The pulp & paper industry processes huge quantities ofagricultural-based lignocellulosic materials every year which isharvested either directly or indirectly from various sources. Owingto the cost-effective ratio, improvement in the processing modal-ities along with an ever increasing demand (Singh et al., 2012; Iqbalet al., 2013), pulp & paper can be made from lignocellulosic-basedmaterials including agave leaves. Three main processing steps, i.e.,(1) pulping, (2) bleaching, and (3) production are potentiallyinvolved in the paper manufacturing process (Iqbal et al., 2013).Based on the processing mechanism there is three main types ofpulping i.e. (i) mechanical pulping, (ii) chemical pulping and lastly(iii) chemical and mechanical pulping (combination pulping) (Iqbalet al., 2013; Gallegos et al., 2016).

Recent studies have tried to revalorize the agave leaves, atroublesome waste left behind the field, by their fiber content andquality (I~niguez-Covarrubias et al., 2001a,b). Many researchers havetried to investigate the potential of agave leaf as a source of fibersfor paper production. I~niguez-Covarrubias and Vaca (2001) havecompared the fibrous characteristics of the agave leaves with two

Table 1Physio-chemical composition of dry agave bagasse at 5% water content.Reproduced from Alonso and Rigal (1997) and I~niguez et al. (2014), an openaccess article licensed under the Creative Commons Attribution InternationalLicense (CC BY). http://creativecommons.org/licenses/by/4.0/.

Parameter Characteristic or percent value

Physical compositionTexture Not very rigidColor Brown-yellowFiber length 5-10 cmDiameter 0.3e0.1 mmChemical compositionCellulose 43%Hemicellulose 19%Lignin 15%Nitrogen 3.0%Pectins 1.0%Fats 1.0%Reducing sugar 5.0%Ash 6.0%Others 2.0%

major types of woods i.e. (i) softwood e.g. pine and (ii) hardwoode.g. eucalyptus, which is particularly being used in papermaking. Inthe same study, they have also found that agave fibers have highercellulose content than either type of the woods mentioned above.Owing to this high cellulosic contents, agave leaves have theremarkable potential to provide a pulp with higher yields. Ascompared to the softwood e.g. pine and hardwood e.g. eucalyptus,agave leaves have lower lignin contents which are also an impor-tant property to avoid and reduce chemical consumption duringthe entire pulping process. In summary, the agave-based fibrousmaterial has a large perspective that could be potentially utilizedfor many paper-based products e.g. handicraft, geotextiles, filters,packaging and composites (I~niguez-Covarrubias et al., 2001a,b).

5.2. Agave leaves as a substrate for the production of enzymes

Enzyme production is a growing field of biotechnology and hasbecome an integral part of the current biotechnological sector fromthe modern world. One of the most appropriate approaches toproduce cost-effective, competent, highly active and novel en-zymes for multifunctional purposes is to capitalize thelignocellulosic-based waste materials e.g. agave leaves (Huitronet al., 2008). Such potential materials contain noteworthy concen-trations of soluble carbohydrates and potent inducers of enzymesynthesis ensuring efficient production of enzymes (Reddy et al.,2003; Moldes et al., 2004; Elisashvili et al., 2006; Iqbal et al.,2011a, b; Asgher and Iqbal, 2011; Asgher et al., 2012a, b, c). Inrecent years, many potent technologies ranging from flask shake tolarge scale have been developed and well documented in theliterature for various enzymes ligninases e.g. lignin peroxidase,manganese peroxidase, versatile peroxidase, manganese indepen-dent peroxidase, phenol oxidoreductase i.e. laccases along withmany other like cellulytic mainly cellulases production (Moldeset al., 2004; Elisashvili et al., 2006).

Enzymes like ligninases, cellulases, xylanases, pectinases andinulinases are nowadays used in a variety of sectors, from food and

Total BOD (mg/L) 35,000e60,000Soluble BOD (mg/L) 25,000e50,000Total solids (mg/L) 25,000e50,000Total suspended solids (mg/L) 2000e8000Fixed suspended solids (mg/L) 10e500Volatile suspended solids (mg/L) 1990e7500Total dissolved solids (mg/L) 23,000e42,000Settle-able solids (mg/L) 10e900Total alkalinity (mg/L) <6.00Total acidity (mg/L) 1500e6000Fixed acidity (mg/L) 1480e5800Volatile acidity (mg/L) 20e200Ca (mg/L) 200-1100Mg (mg/L) 100e300K (mg/L) 150e650Phosphates (mg/L) 100e700Total nitrogen (mg/L) 20e50Organic nitrogen (mg/L) 5.0e10Total reducing sugars (%w) 0.5e2.0Direct sugars (%w) 0.4e1.0Cu (mg/L) <3.0Fe (mg/L) <45Ni (mg/L) <0.02Zn (mg/L) <1.0

Fig. 5. A tentative pilot plant scheme for the treatment of Tequila vinasses.

G.S. Alem�an-Nava et al. / Journal of Cleaner Production 172 (2018) 3713e3720 3717

beverage manufacturing to biomass conversion and waste treat-ment. The potential use of Agave TequilanaWeber var. azul has beenexploited as a fermentative substrate for enzyme production. In anearlier study conducted by Huitron et al. (2007), two filamentousfungal strains were found able to simultaneously secrete endo-pectinases, and exopectinases, along with xylanases, and inuli-nases. In this context, agave wastes particularly agave leaves havegained exceptional consideration from both the academic and in-dustrial researchers because of its potential as an inexpensivecarbon and energy sources for the production of ligninolytic andlignocellulolytic enzymes. Likewise, many other research in-vestigations have also proved the potential of using Agave Tequilanawaste as a prospective candidate material for many biotechnolog-ical applications (Huitron et al., 2007; Nava-Cruz et al., 2015; Yanget al., 2015). Ligninolytic, cellulases and hemicellulases are impor-tant industrial enzymes having numerous applications andbiotechnological potential for various industries including chem-icals, fuel, food, brewery and wine, animal feed, textile and laundry,pulp and paper and agriculture (Couto and Sanrom�an, 2006; Levinet al., 2008; Oberoi et al., 2010; Asgher and Iqbal, 2011; Iqbal et al.,2011a, 2013).

5.3. Agave bagasse for animal feeding

In a ruminant’s diet, cellulose is considered a primary carbonand energy source. In this context, agave bagasse utilization foranimal feeding could have a remarkable influence on livestockmanagement. However, the presence of lignin limits the di-gestibility of cellulose thus requires some preferential delignifica-tion treatment before use for animal feeding. To enhance the pre-digestibility and nutritional value, the concept of preferentialdelignification of lignocellulosic materials has been applied (Iqbalet al., 2013). Moreover, to further facilitate this kind of use, it is,therefore, necessary to physically separate the more digestible partof the bagasse, the pith, from the low digestibility fibers. Inparticular, bagasse that came from shredded agave heads beforecooking and sugars extraction in pressing mills yielded the higherpercentage of recovered pith (56%). Feeding trials have been con-ducted on Pelibuey crossbred male sheep, testing 3 comparativediets: 79.3% (on dry basis) ground corn-based diet, 63.2% agavebagasse pith based diet and 63.2% ground corn stubble based diet. Itwas found that daily feed consumption and average weight gains

were statistically the same for the three diets (I~niguez-Covarrubiaset al., 2001a,b). The study also calculated that a Tequila factory isproducing 68 ton/day of agave bagasse, with 36% pith recovered,could feed 24,480 animals daily if using a proper agave bagasse pithbalanced diet. Finally, it is important to underline that agavebagasse could potentially have an economic value with an advan-tage of being available all year around (I~niguez-Covarrubias et al.,2001a,b).

Another study investigated the chemical and physical compo-sition of agave bagasse, along with its potential for ruminantsfeeding material (Rami

rez-Cortina et al., 2012). The authorsunderlined the high content of lignin being a problem for di-gestibility, but also stated the benefit of the high proportion of freesugars (22% in dry basis) for direct use in ruminant food portions.Digestibility value of agave bagassewas comparedwith sunflower’sand straw’s and located between the two. An alternative suitabletechnology to increase its digestibility was also proposed. Alkalinepretreatments, besides of saponifying waxes and cuticles, alsoperform solubilization of lignins and hemicellulose, increasing di-gestibility of lignocellulosic residues. Therefore, in this case, thehigh content of lignin was decreased using a calcium hydroxidetreatment. Moreover, the treatment prevents drying, responsiblefor the decrease of free sugars. Furthermore, Ca(OH)2 concentrationin treatment provides an important contribution of calcium, whichis beneficial for the composition of animal feeding (Rami

rez-Cortina et al., 2012).

5.4. Agave bagasse for fiberboard production

From the last few decades, there has been increasing researchinterests towards the utilization of lignocellulosic-based materialsand by-products as composite materials, in particular, for thermalinsulation, false ceilings, fiberboards and packaging materials.Recent articles have investigated the potential of agave bagasse tobe used for these purposes. In the same study on the use of agavebagasse as feeding material, the agave bagasse fibers separatedfrom the pith were tested for fiberboard production (I~niguez-Covarrubias et al., 2001a,b). A range of medium density and high-density boards samples were prepared and tested by I~niguez-Covarrubias and Vaca, 2001, using short and long agave bagassefibers. Medium specific gravity fiberboards were found to havesimilar moisture andmechanical properties, as compared to similarfiberboards made from aspen fiber. High specific gravity boardswere stronger in bending tests than the ANSI standards (AmericanNational Standards Institute) for hard boards. The comparableproperties and the better bending resistance of fiberboards made ofagave bagasse fibers show that this could be a possibility of cost-efficient use of this low-value waste by-product of the Tequila in-dustry (I~niguez-Covarrubias et al., 2001a,b).

5.5. Agave bagasse for agricultural purposes

Another potential use for agave bagasse has also been proposedfor agricultural purposes as a substrate. A recent study investigatedthe composting process of agave bagasse from two different Tequilacompanies, using ammonium nitrate as a nitrogen source to adjustthe agave bagasse C: N ratio to 25:1, the recommended value for anexcellent biodegradability (I~niguez-Covarrubias et al., 2011).Furthermore, a field study was conducted, using the agave bagassecomposts as substrates for tomato production. Comparisons withcommercial substrates were also carried out. The different com-posts used did not show statistically significant differences at theend of the 21 days of composting: total grams of tomatoes pro-duced per plant and their quality (color, diameter, deformations)were found to be similar. These results show the potential of the use

Fig. 6. PHAs granules (A) and schematic of a PHA granule (B). The core consists of PHApolymer that is enwrapped by a phospholipid monolayer and proteins on the outside.The proteins consist of PHA polymerase, PHA depolymerase, structural proteins, andproteins of unknown function (Reproduced with permission from Iqbal, 2015).

G.S. Alem�an-Nava et al. / Journal of Cleaner Production 172 (2018) 3713e37203718

of agave bagasse as a substrate for agriculture cultivations.Agave bagasse based compost has also been used as a substrate

for new-born agave plants. As it has already been mentioned, agavereproduction and propagation is conducted asexually, which gua-rantees more control, but weakens the new plantations and makesthem more sensitive to pests and infestations. This procedure in-volves seedling and micropropagation in vitro. After that, micro-propagated agave plants must pass a period of adaptation in thenursery, for nine to twelve months. Only after they can be taken tothe fields. This period of acclimatization is usually carried out in agreenhouse, with proper treatments. Canadian peat and coconutpowder substrates are commonly used for this purpose, althoughthey are expensive. On this matter, agave bagasse based substratecould represent a potential cheap substitute. A recent studyinvestigated this potential. In particular, the response of micro-propagated seedlings of agave in four mixtures of agave bagassecompost was analyzed. A comparison with coconut powder, Ca-nadian peat, and the commercial substrate was also carried out, byevaluating the following parameters: diameter of the cone andstem diameter, the length of longest leaf, the width of the longestleaf and number of leaves (Gonz�alez et al., 2013). It was found thattreatments based on agave bagasse compost led to better values ofthe morphological parameters if compared to the coconut powderand the peat results. These results show the possibility of substitutethe commercial substrate with the compost substrates, particularlywith the mixtures 30, 50 and 70%. By making this substitution, ahuge waste of the Tequila industry would be used (bagasse)through composting, avoiding environmental pollution, andreducing production costs, since the compost can be made locally(Gonz�alez et al., 2013).

5.6. Agave bagasse for biosolids treatment and vinasses disposal

Agave bagasse can also potentially be used to solve the problemof vinasses treatment partially. In particular, recent studies inves-tigated the use of bagasse as a final disposal for vinasses. Com-posting of agave bagasse was once again involved, but this timeaddition of nutrients was not participating in the degradation ofagave bagasse (I~niguez-Covarrubias et al., 2005). Only urea andvinasses were added to the composting process to maintainmoisture. Four bagasse piles were considered. During the com-posting process two of them were irrigated with vinasses and theother two with water. One water wetted pile, and one vinassewetted pile was added with urea at the beginning of the process, toadjust the C: N ratio to the optimum 25:1. Every two months thepiles were moved to facilitate aeration and the addition of waterand vinasses. Samples were taken for the analysis of pH, organicmatter, and cellulose. At the end of the composting time, compostswere subjected to analysis of ash, total organic carbon, N, P, K, andconductivity, along with some phytotoxicity analysis. The testperiod for the piles with urea was 228 days. During this time,0.912 L of vinasses were added per kg of wet bagasse. It was alsofound that the obtained compost had similar characteristics to thegarden soil without problems of phytotoxicity: composts from thefour treatments had no adverse effects on seedling emergence,relative growth, germination and root elongation of cucumberseeds (I~niguez-Covarrubias et al., 2005).

5.7. Agave bagasse for slaughterhouses and tanneries wastedisposal

Tanneries waste are classified as hazardous residues and mainlycome from the preparation of the hide for hardening and arecomposed of hair and flesh material. Due to their organic compo-sition and previous experiences in the biodegradation of animal

waste, the agave bagasse residues could potentially be used tocompost slaughterhouses and tanneries waste. Since this is anaerobic process of degradation, in some cases it is necessary tofacilitate the passage of air by adding some material that increasesthe pore structure of the residue susceptible to degradation. Arecent study investigated the use of agave bagasse as a promoter ofthe air passage in the composting process of tanneries waste, aswell as the potential use of the final product for cultivation pur-poses (�I~niguez et al., 2003). Temperature changes in the threadmaterial were daily monitored during biodegradation process.Microbial and chemical analyses were performed on the compost,as well as germination studies. From the microbial analyses, thepresence of Escherichia coli was found.

5.8. Agave bagasse for bioplastic production

There has been considerable interest in agricultural-based ma-terials like agave bagasse in recent years due to their potential as analternative source of the traditional petroleum-based syntheticmaterials. Another possible use for agave bagasse could be for theproduction of bioplastics. A recent study investigated the ability ofSaccharophagus degradans to degrade the major components ofplant cell walls and to synthesize polyhydroxyalkanoates (PHAs,also known as bioplastics) (Alva Munoz and Riley, 2008).Biopolymers-based bioplastic such as PHAs generated fromrenewable natural sources by micro-organisms are often biode-gradable, biocompatible and non-toxic in nature (Iqbal et al.,2014a,b,c; Iqbal, 2015). Therefore, the development of bioplasticsusing one or more individual biopolymers are among the routes toimprove some of the properties of biodegradable polymers (Miaoand Hamad, 2013; Hooshmand et al., 2014; Iqbal et al., 2014a,b,c).PHAs belongs to a family of bio-polyesters produced by microbesunder limited nutritional conditions (e.g. nitrogen or phosphate)(Sudesh et al., 2000; Chen and Wu, 2005), or excess carbon source(Ojumu et al., 2004; Keshavarz and Roy, 2010). The unbalancednutritional supply causes the bacteria to accumulate PHAs in theform of granules as an internal energy storage, as shown in Fig. 6.The main members of the PHAs family are presented in Table 3based on the generic structural formula for the PHAs where x is 1or higher, and R can be either hydrogen or hydrocarbon chains of upto C16 in length (Iqbal, 2015). PHAs offer a broad range of me-chanical properties, are biodegradable and could potentially sub-stitute oil based plastics and polymers. It has already beendemonstrated that S. degradans can attach to cellulosic fibers anddegrade the cellulose to use it as a primary carbon source. Its use isattractive also due to its non-pathogenesis, its capacity of decom-posing and metabolize a wide variety of insoluble complex poly-saccharides, and its production of three key enzymes for PHAsynthesis (Ekborg et al., 2005). Over the past several years, owing tothe above discussed characteristics, many scientists, around the

Table 3Main PHAs structures based on the general structure (Reproduced with permissionfrom Iqbal, 2015).

Name Abbreviation x value R group

Poly(3-hydroxypropionate) P(3HP) 1 HydrogenPoly(3-hydroxybutyrate) P(3HB) 1 MethylPoly(3-hydroxyvalerate) P(3HV) 1 EthylPoly(3-hydroxyhexanoate) P(3HHx) 1 PropylPoly(3-hydroxyheptanoate) P(3HHp) 1 ButylPoly (3-hydroxyoctanoate) P(3HO) 1 PentylPoly (3-hydroxynonanoate) P(3HN) e HexylPoly(3-hydroxydecanoate) P(3HD) 1 HeptylPoly(3-hydroxyundecanoate) P(3HUD) 1 OctylPoly(3-hydroxydodecanoate) P(3HDD) 1 NonylPoly(3-hydroxyoctadecanoate) P(3HOD) 1 PentadecanoylPoly(4-hydroxybutyrate) P(4HB) 2 HydrogenPoly(5-hydroxybutyrate) P(5HB) 2 MethylPoly(5-hydroxyvalerate) P(5HV) 3 Hydrogen

G.S. Alem�an-Nava et al. / Journal of Cleaner Production 172 (2018) 3713e3720 3719

globe, have directed their research interests into the developmentof engineered constructs using PHAs for various applicationsincluding bio-medical, pharmaceutical, drug delivery, antibacterialpackaging or sanitary materials, and household items (Fillat et al.,2012; Iqbal et al., 2014a, 2015a,b).

6. Conclusions

This work presents various alternatives for the disposal of Te-quila industry byproducts, following the concept of the biorefinery.Agave leaves, mainly composed of cellulose, hemicellulose, andlignin could potentially be used as a sugar source for animal feed oralcohol production, as a fiber source for paper products or as asubstrate for enzymes production. Agave bagasse, a fibrous solidresidual, was found to be suitable for animal feeding or fiberboardproduction, as well as composting. It was also considered as anefficient way for slaughterhouses and tanneries waste disposal andbioplastic production. Recent studies also investigate the use ofAgave bagasse for ethanol production. Vinasses, the residualgenerated during distillation, represent significant disposal andtreatment problems due to their complex physiochemical compo-sition. Their high biological oxygen demand, dissolved salts contentand low pH make them a recalcitrant waste that is hardly decom-posed by the usual biological processes. New anaerobic treatmentsfor biogas production are being considered and evaluated at labo-ratory scale. It is firmly believed by the author that, due to the largeamounts of waste produced by the Tequila industry, the best so-lution for the disposal problem presented in this paper does not liein the choice and implementation of a single treatment. On thecontrary, a mix of some of the alternative treatments presentedwould probably represent the most efficient option, from both aneconomical and environmental point of view.

Declaration of interest

The authors report no declarations of interest in any capacity,i.e., competing or financial.

Acknowledgement

This paper was supported by the Emerging TechnologiesResearch Group and the Environmental Bioprocesses of Tecnolo-gico de Monterrey, Mexico. The authors would like to thank Tec-nologico de Monterrey, Mexico for providing literature facilities.

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