artículo de residuos solido

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Review Sustainability of using composting and vermicomposting technologies for organic solid waste biotransformation: recent overview, greenhouse gases emissions and economic analysis Su Lin Lim, Leong Hwee Lee, Ta Yeong Wu * Chemical Engineering Discipline, School of Engineering, Monash University, Jalan Lagoon Selatan, 47500 Bandar Sunway, Selangor Darul Ehsan, Malaysia article info Article history: Received 10 January 2015 Received in revised form 16 August 2015 Accepted 18 August 2015 Available online 28 August 2015 Keywords: Biodegradation Compost Earthworm Organic fertilizer Vermicompost Solid waste management abstract Organic solid waste poses a serious threat to the environment as the world struggles to keep up with its rapid generation. Biological waste treatment technologies such as composting and vermicomposting are widely regarded as a clean and sustainable method to manage organic waste. The focus of this review is to evaluate the feasibility of composting and vermicomposting as a means to recover nutrients from the organic waste and returning them to the environment. The environmental impact and economic po- tential of these processes are also discussed. This review shows that composting and vermicomposting are capable of degrading various types of organic waste, thus enabling them to be adopted widely. The present review also reveals that greenhouse gases are emitted during composting and vermicomposting processes. However, introductions of intermittent aeration, bulking agents and earthworm abundance may reduce the greenhouse gases emissions. Economic assessments of composting and vermi- composting technologies show that these technologies are generally viable except in some cases. The differences are due to the wide range in market value for organic fertilizer and differences in cost for the type of composing or vermicomposting system which could affect its economic feasibility. However, if organic fertilizer value increases and carbon offsets are available for nutrient recycling, it will affect the economic feasibility in a positive way. © 2015 Elsevier Ltd. All rights reserved. Contents 1. Introduction ...................................................................................................................... 262 2. Methods ......................................................................................................................... 264 3. Composting and vermicomposting processes: an introduction, differences and similarities ................................................. 265 3.1. Composting of organic waste .................................................................................................. 266 3.2. Vermicomposting of organic waste ................................................. ........................................... 270 3.3. Integration of composting-vermicomposting process ............................................................................. 271 4. Environmental impact of composting and vermicomposting processes .................................................................. 272 5. Economic analysis of composting and vermicomposting processes ..................................... ................................ 273 6. Conclusion ....................................................................................................................... 274 Acknowledgments ............................................................ .................................................... 275 References ......................................................................................................................... 275 1. Introduction World cities generate approximately 1.3 billion metric tons of solid waste annually, which is almost double the amounts that * Corresponding author. Tel.: þ60 3 55146258; fax: þ60 3 55146207. E-mail addresses: [email protected], [email protected] (T.Y. Wu). Contents lists available at ScienceDirect Journal of Cleaner Production journal homepage: www.elsevier.com/locate/jclepro http://dx.doi.org/10.1016/j.jclepro.2015.08.083 0959-6526/© 2015 Elsevier Ltd. All rights reserved. Journal of Cleaner Production 111 (2016) 262e278

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Page 1: artículo de residuos solido

lable at ScienceDirect

Journal of Cleaner Production 111 (2016) 262e278

Contents lists avai

Journal of Cleaner Production

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

Review

Sustainability of using composting and vermicomposting technologiesfor organic solid waste biotransformation: recent overview,greenhouse gases emissions and economic analysis

Su Lin Lim, Leong Hwee Lee, Ta Yeong Wu*

Chemical Engineering Discipline, School of Engineering, Monash University, Jalan Lagoon Selatan, 47500 Bandar Sunway, Selangor Darul Ehsan, Malaysia

a r t i c l e i n f o

Article history:Received 10 January 2015Received in revised form16 August 2015Accepted 18 August 2015Available online 28 August 2015

Keywords:BiodegradationCompostEarthwormOrganic fertilizerVermicompostSolid waste management

* Corresponding author. Tel.: þ60 3 55146258; fax:E-mail addresses: [email protected], tayeo

http://dx.doi.org/10.1016/j.jclepro.2015.08.0830959-6526/© 2015 Elsevier Ltd. All rights reserved.

a b s t r a c t

Organic solid waste poses a serious threat to the environment as the world struggles to keep up with itsrapid generation. Biological waste treatment technologies such as composting and vermicomposting arewidely regarded as a clean and sustainable method to manage organic waste. The focus of this review isto evaluate the feasibility of composting and vermicomposting as a means to recover nutrients from theorganic waste and returning them to the environment. The environmental impact and economic po-tential of these processes are also discussed. This review shows that composting and vermicompostingare capable of degrading various types of organic waste, thus enabling them to be adopted widely. Thepresent review also reveals that greenhouse gases are emitted during composting and vermicompostingprocesses. However, introductions of intermittent aeration, bulking agents and earthworm abundancemay reduce the greenhouse gases emissions. Economic assessments of composting and vermi-composting technologies show that these technologies are generally viable except in some cases. Thedifferences are due to the wide range in market value for organic fertilizer and differences in cost for thetype of composing or vermicomposting system which could affect its economic feasibility. However, iforganic fertilizer value increases and carbon offsets are available for nutrient recycling, it will affect theeconomic feasibility in a positive way.

© 2015 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2622. Methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2643. Composting and vermicomposting processes: an introduction, differences and similarities . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 265

3.1. Composting of organic waste . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2663.2. Vermicomposting of organic waste . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2703.3. Integration of composting-vermicomposting process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 271

4. Environmental impact of composting and vermicomposting processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2725. Economic analysis of composting and vermicomposting processes . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2736. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 274

Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 275

þ60 3 [email protected] (T.Y. Wu).

1. Introduction

World cities generate approximately 1.3 billion metric tons ofsolid waste annually, which is almost double the amounts that

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Table 1Current and projected waste generation rates and composition by income level (adapted from Hoornweg and Bhada-Tata, 2012).

Income level Urban population (millions) Waste generation rates (kg/capita/d) Solid waste composition (%) Total organic solidwaste volume (t)

Organic Paper Plastic Glass Metal Others

Lower Current 343 0.60 64 5 8 3 3 17 48 � 106

2025 676 0.86 62 6 9 3 3 17 132 � 106

Lower Middle Current 1293 0.78 59 9 12 3 2 15 218 � 106

2025 2080 1.30 55 10 13 4 3 15 526 � 106

Upper Middle Current 572 1.16 54 14 11 5 3 13 131 � 106

2025 618 1.60 50 15 12 4 4 15 180 � 106

High Current 774 2.13 28 31 11 7 6 17 169 � 106

2025 912 2.10 28 30 11 7 6 18 192 � 106

Fig. 1. Global solid waste composition (adapted from Hoornweg and Bhada-Tata,2012).

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 263

were generated a decade ago (Hoornweg and Bhada-Tata, 2012). By2025, solid waste generations will double again (Hoornweg et al.,2013). The annual increase in solid waste generation is inextri-cably link to the rapid rise in global population and rate of urban-ization. As a country urbanizes, its standard of living and incomelevel increases which leads to higher consumption of goods andservices, thereby generating larger amount of solid waste per capita(Hoornweg and Bhada-Tata, 2012). Table 1 shows the current andprojected waste generation rates according to income level. Thewaste generation rates in 2025 are predicted to be 38e67% increaseof the current waste generation rates for the lower to middle in-come countries. In higher income countries, as their total popula-tion are largely urban population (Hoornweg and Bhada-Tata,2012), the waste generation rates have more or less stabilizedduring the last decade (UNEP, 2011). Although higher incomecountries generate more solid waste, they recycle more and havethe resources to deploy new technologies for treating their waste,which eventually decrease waste generation and disposal (Sim andWu, 2010). On the contrary, developing countries generally do nothave the technical skills nor financial capability, leading to limitedresources for safe disposal of final waste. The limitations of re-sources in developing countries to manage organic waste pose asignificant challenge that needs to be resolved (UNEP, 2011).

Among the total solid waste generated globally, organic waste isthe largest proportionwith 46% (Fig. 1) (Hoornweg and Bhada-Tata,2012). The organic waste includes food scraps, yard waste andagricultural waste. The rest of the waste is inorganic like paper,plastic, glass, metal and others (Karak et al., 2012). As the incomelevel of a country increases, the waste stream composition alsochanges and typically has lower proportion of organic waste. Theproportion of organic waste in low income countries is 64% and thisvalue reduces to 28% in higher income countries (Table 1)

(Hoornweg and Bhada-Tata, 2012). Slight reduction in proportion oforganic waste in low to high income countries are projected in2025. However, the amount of the organic waste is increasingtogether with the total amount of solid waste. Solid waste gener-ation rates are predicted to be exceeding 11 million metric tons perday, which are more than three times the current rate of solid wastegeneration using ‘business-as-usual’ projections by the year of 2100(Hoornweg et al., 2013).

Current methods of solid waste managements are landfilling,incineration, recycling, reuse, source reduction and others (Wuet al., 2014). Both landfilling and incineration are characterized aswaste disposals, which are the least preferred options in the wastemanagement hierarchy. In many parts of the world, landfilling re-mains the dominant method for waste disposal as it is the cheapestin terms of capital costs (Laner et al., 2012). In developed countries,the landfills are equipped with a combination of waste contain-ment systems such as leak detection and management systems forcollecting leachates and biogas (Hoornweg and Bhada-Tata, 2012).On the contrary, proper landfilling is often lacking in developingcountries (Hoornweg and Bhada-Tata, 2012). In recent years,controlled landfilling in these countries is increasing (Sim and Wu,2010) but open dumping is still a common practice (Hoornweg andBhada-Tata, 2012). Management of leachate is also a problematicissue because the raw leachate contains high organic load inchemical oxygen demand (Romero et al., 2013), which requiresproper management and disposal that will add cost to the landfilloperation (Z�avodsk�a et al., 2014). Greenhouse gas emissions due tosolid waste decomposition in the landfill is also a cause for concern(Pozza et al., 2015). In addition, most landfills in the developedcountries require proper maintenance and continuous care aftertheir closure. Therefore, extra costs are needed for landfill aftercareuntil no threat to the human health and environment is found(Laner et al., 2012). Furthermore, the limitation of land and thevalue of waste as resources are concrete reasons tomove away fromlandfilling and shift towards more sustainable waste managementstrategy (Marshall and Farahbaksh, 2013). For example, Europeancountries are doing away with the landfill owing to the EU LandfillDirective which requires its member states to reduce landfilling ofbiodegradable waste to less than 35% of the amount produced in1995. Countries such as Austria, Belgium, Denmark, Germany,Luxembourg, Netherlands and Sweden have fulfilled and exceededthe targets of the EU Landfill Directive (EEA, 2009). Currently,Netherlands are landfilling only 2e3% of its total waste (Scharff,2014). In addition, recent study done by Yang et al. (2015) alsoshowed that over the next 10e15 years, an increase in the pro-portions of incineration and composting is more feasible thanlandfilling in municipal solid waste management.

Scarcity of land for landfilling leads to another waste disposaloption like incineration. Waste incineration could be the solutionfor reducing the degradation of land, generation of methane gas

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S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278264

and leachate production caused by improper landfilling. Incinera-tion is suitable for non-biodegradable waste with low moisturecontent (Tan et al., 2014). Besides, reduction of waste volume of upto 90% and recovery of energy are possible during incineration(Hoornweg and Bhada-Tata, 2012). Waste-to-energy incinerationplants in large scale are common in developed countries such asDenmark, Japan, Germany, Sweden, Netherlands and UnitedKingdom (Tan et al., 2014). One of the major drawbacks of theincineration plant is the harmful emissions but technologies areavailable for controlling gaseous emissions to minimize the impacton the environment (Samolada and Zabaniotou, 2014). Incinerationplants in the developed countries consist of environmental controlsystem, in which their governments regulate and monitor theemissions frequently. The drawback of incineration plant is the highcapital, technical and operation costs. This is an issue especially forthe lower to middle income countries whereby these developingcountries usually do not have the economic resources for setting upand maintaining an incineration plant (Sim and Wu, 2010).Furthermore, incineration poses societal and environmental healthrisks if misused and shows a less positive energy balance thantransformingmaterials through recycling (Oliveira and Rosa, 2003).Generally, incineration is not suitable to be introduced in devel-oping countries such as Ethiopia, Nepal, Sri Lanka, Tunisia, Algeriaand others because these countries produce a lot of organic solidwaste which is high in moisture content and has low calorific value(Karak et al., 2012).

Other solid waste management options are 3Rs, consisting ofsource reduction, recycling and reuse (Zaman, 2013). Waste man-agement options using 3Rs are in line with the cleaner productioninitiative which involves continuous application of preventiveenvironmental strategies to all processes in order to maximize theefficiency and minimize the impact on the environment (UNEP,2015). Waste avoidance and reduction technology are consideredto be the prime challenge rather than the development of newwaste treatment technology (Zaman, 2013). Source reduction in-volves redesigning processes and managing products to reduce theamount of generated waste and greenhouse gas emission. If nowaste is generated, there is no need for treatment or disposal.However, waste is bound to be generated despite the efforts tominimize them. Recycling also helps reduce the amount of wastesuch as paper, glass andmetal generated by returning the materialsconsumed to the economy (Shekdar, 2009). Recycling rates arehigher and effective in developed countries as compared todeveloping countries due to the better collection services and fa-cilities for sorting and processing. These facilities are highlyequipped, common and regulated (Hoornweg and Bhada-Tata,2012). Developing countries are often lacking of waste recyclingand treatment facilities, where waste is still dumped in the openenvironment (Song et al., 2015). The recycling process is generallyinformal but is slowly in the process of institutionalization (UNEP,2011).

Reuse is another waste management strategy for waste thatcannot be recycled and helps reduce the amount for disposal(Shekdar, 2009). Examples of reuse of organic solid waste arecomposting and vermicomposting processes. Composting is a bio-logical decomposition of organic waste under either aerobic oranaerobic conditions. Similarly, vermicomposting is also a biolog-ical decomposition process of organic waste but with an addition ofearthworms to speed up the biodegradation process. The compostsand vermicomposts produced from organic waste can be reused asnutrient-rich organic fertilizers or for land application (Wu et al.,2014). These two processes are also highly favored to managesolid waste owing to the high percentage of organic waste in thewaste composition. Moreover, lesser costs are incurred in bothcomposting and vermicomposting process, making them a good

option to be applied in developing countries. Increases in com-posting facilities are mushrooming in developed countries likeBelgium, Denmark, Germany, France, Sweden, Switzerland, UnitedStates and others. From 1995 to 2007, some of the Europeancountries showed an increase of more than 50% in composting rate(Karak et al., 2012). In fact, these biological decomposition pro-cesses can be considered as a sustainable waste managementstrategy, which is in line with the zero waste concept.

In a zerowaste system, the resource flow is circular whereby theresources are conserved and recovered for reuse purposes insimilar or other processes. In other words, what is seen as a wastefrom an industry could be reused or converted into value-addedinputs for other industries or processes (Curran and Williams,2012). Both landfilling and incineration with limited energy re-covery do not fulfill the intentions and goals of ‘zero waste’ concept(Scharff, 2014). Open dumping and landfilling remain the pre-dominant method of solid waste disposal in the lower to middleincome countries. However, cost-benefit analysis of compostingand landfilling reveals that the former is a more attractive optionbased on its lower environmental and social costs (UNEP, 2011).Reusing waste could also reduce management costs due to savingsfrom reducing the amount of organic waste that was sent to landfill(Cabanillas et al., 2013). The efficient treatment and recycling ofvalue-added products such as compost to agricultural land canusually be shown to have lower global warming potential ascompared to other disposal processes (Samolada and Zabaniotou,2014). Life cycle assessment studies also concluded that compost-ing is having lesser environmental impacts as compared to otherorganic waste disposals, such as landfilling and incineration (Saeret al., 2013). In short, composting and vermicomposting could bethe most promising option for organic waste management, espe-cially in lower income countries, because they incur lower cost andhave lesser impact on the environment. Mechanisms of bothcomposting and vermicomposting processes in producing organicfertilizer from the waste show that they are meeting the cleanerproduction concept. Moreover, the driving force behind the intro-duction of composting and vermicomposting (or other reuse pro-cesses) in organic solid wastemanagement is the global recognitionof the need to recover useful organic materials and return them tothe soil. Thus, this review will focus on the potential of introducingcomposting and vermicomposting in bio-transforming organicwaste into fertilizer as a sustainable waste management strategy.

2. Methods

The aim of this review is to provide a detailed account on thefeasibility of composting and/or vermicomposting of organic wasteby analysing its environmental and economic aspects. In this re-view, a summary of the composting and vermicomposting processwas presented. This summary includes the process mechanisms, itsadvantages, disadvantages and limitations as reported by existingresearchers. Composting and vermicomposting literature related toenvironmental and economic aspects were critically evaluatedbased on their significance and relevance. In addition, the reviewaims to provide a comprehensive and balanced portrayal of thecurrent state and feasibility of composting and/or vermicompost-ing process by including all viewpoints and conclusions on thesubject matter obtained by different researchers. The literatureincluded in this review was obtained using databases from majorpublishers. Due to the vast amount of literature available in com-posting and vermicomposting of organic waste, only articles pub-lished in 2010 until nowwere considered. Articles published before2010 were only included if (1) they were deemed necessary tosupport/contradict other studies, or (2) the contents were exclusiveand worth highlighting.

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S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 265

3. Composting and vermicomposting processes: anintroduction, differences and similarities

Composting is a biological decomposition of organic wasteeither in an aerobic (Makan et al., 2014) or anaerobic (Minale andWorku, 2014) environment with the former being more common.The organic matters in the waste are consumed by aerobic ther-mophilic and mesophilic microorganisms as substrates and con-verted into mineralized products such as CO2, H2O, NH4

þ orstabilized organic matters (Qian et al., 2014). The resultant compostis a stable, humus-rich, complex mixture that can improve physicalproperties of the soil (Watteau and Villemin, 2011). Factorsaffecting composting process are temperature, initial C/N ratio,aeration, porosity, moisture content and pH (Shafawati andSiddiquee, 2013). During composting process, these parametersare regulated and controlled to provide an optimum environmentfor the microorganisms to degrade the organic waste (L�opez-Gonz�alez et al., 2015).

Similar to composting, vermicomposting process is also a bio-logical decomposition of organic waste to produce stabilizedorganic fertilizer, namely vermicompost. Unlike composting, ver-micomposting process involves interactions between earthwormsand microorganisms to biodegrade organic waste at a faster rate(Sim and Wu, 2010). Earthworms act as the main drivers in thedecomposition of organic waste by fragmenting and conditioningthe substrate. In doing so, earthworms increase the surface area ofthe organic waste that is exposed to the microorganisms. Thus, themicrobial activity and decomposition process of solid waste areenhanced. Vermicomposting results in the production of vermi-compost or earthworm cast that has low C/N ratio, high porosity,water-holding capacity and available nutrients (Lim et al., 2015b).According to Lim and Wu (2015), scanning electron microscopeimage of the vermicompost showed a distinct physical appearancethat was more scattered and smaller in nature in comparison withthe initial waste. Like composting, efficiency of vermicompostingprocess is also influenced by several factors such as initial C/N ratio,moisture content, pH and nature of the organic waste. In compar-ison with the composting process, all the factors influencing ver-micomposting process are also inextricably linked to theearthworm species which are used during the biodegradationprocess. In addition to the vermicompost, earthworm biomass isalso produced during vermicomposting. After the completion ofvermicomposting process, earthworms were removed from thevermicompost via light, vertical or sideways separation. The excessearthworms after the vermicomposting process ends could be usedto biotransform other organic waste or as a protein source for an-imals and as fishing bait (Edwards et al., 2010).

Earthworms used in the vermicomposting process must possessthe following characteristics: 1) high rates of organic matter con-sumption, digestion and assimilation; 2) high tolerance of envi-ronmental stress; 3) high reproductive rate; 4) rapid growth and

Table 2Characteristics of different epigeic earthworm species for vermicomposting process.

Characteristics Epigeic End

Habitat 3-10 cm, surface dwellers 10-Feeding habit Coarse particulate organic matter, undecomposed litter SubCasting habit Surface casting Mos

deeSize Small, uniformly pigmented MedReproductive rates High LowExample of

earthworm species(life cycle)

Eisenia fetida (45e51 d), Eisenia andrei (45e51 d), Eudriluseugeniae (50e70 d), Perionyx excavates (40e50 d)

Octo

Source: Butt and Briones (2011), Edwards (2004), Edwards et al. (2010), Fern�andez et al

maturation rate of hatchlings (Singh et al., 2011). Earthworms areclassified into three different categories, namely epigeic, endogeicand anecic. Table 2 shows the characteristics of the three differentcategories of earthworms. Among these earthworms, epigeicearthworms are the most suitable earthworms to be used in ver-micomposting process as they live in organic horizons and feedprimarily on decaying organic matter. On the other hand, endogeicearthworms feed on subsurface soil and live below the soil surfacewhile anecic earthworms prefers to feed on soil and lives deep inthe soil (Yadav and Garg, 2011a). Epigeic species are the mostefficient in biodegrading organic waste and releasing nutrients intothe soil. In addition, the latest study revealed that surface-dwellingmode of life guarded the epigeic earthworm against their exposureto pesticide (Suthar, 2014). Among the epigeic earthworms, Eiseniafetida and Eisenia andrei are the most commonly used in vermi-composting because both earthworms are peregrine and ubiqui-tous with a worldwide distribution, resilient and have widetemperature tolerance (Edwards, 2004).

Table 3 shows the differences between composting and vermi-composting process. Vermicomposting process has the advantageover composting process in terms of the length of the biodegra-dation process, whereby the latter generally requires longer time toproduce a good quality fertilizer (Roy et al., 2010). Based on theearthworm species and substrate characteristics, it takes about6e18 h for vermicomposting process to occur as this is the amountof time taken by the earthworm to ingest the substrate and excretethem as vermicast (Abbasi et al., 2015). However, there are in-stances where the composting duration is shorter than vermi-composting due to various factors such as system used, the natureof waste, moisture content, aeration and earthworm species(Edwards et al., 2010). The vermicompost also possesses finertexture and lower heavymetal content as compared to the compost(Wu et al., 2014). On the other hand, composting process can nor-mally decompose a wider range of organic waste without affectingthe efficiency of the process because it does not involve earth-worms, which are delicate to certain chemicals from the waste.Thus, a combination between composting and vermicomposting(as a later stage) is recommended to biodegrade solid waste whichare too oily, salty or have extreme pH. Despite the differences be-tween composting and vermicomposting process, the main pur-pose of these two processes is to recycle nutrients from the organicwaste. Both composting (Albrecht et al., 2011) and vermicompost-ing (Shak et al., 2014) processes also reduce the waste volume afterprocess completion. The recovered nutrients are recycled to the soilas an organic fertilizer (compost and vermicompost), therebyclosing the organic matter cycle (Singh et al., 2011). According toDoan et al. (2013), both compost and vermicompost modified soilchemical properties, leading to higher carbon and nitrogen, higherpH and cationic exchange capacity but lower available P, NH4

þ andNO3

� than mineral fertilizer. In addition, Doan et al. (2014)demonstrated that the nature of the organic amendment from

ogeic Anecic

30 cm, live in soil upper layer 30-90 cm, deep burrowingsurface soil material Surface litter, soiltly underground inside horizontal,p-branching burrow system

Surface casting or at burrow entrance

ium, little pigmentation LargeModerate

lasion cyaneum (~90 d) Lumbricus terrestris (210 d), Lumbricus friendi(231 d), Aporrectodea trapezoids (153 d)

. (2010), Lowe and Butt (2008), Yadav and Garg (2011a).

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Table 3Differences between composting and vermicomposting process.

Parameters Composting Vermicomposting

Type of process 3 stages: Initial activation phase, thermophilicphase and mesophilic phase

Mesophilic stage

Organisms involved in biodegradation Microorganisms Earthworms and microorganismsOrganic waste characteristics Sorted organic waste, combination of waste with

similar decomposition rateNot hard, oily, salty, acidic and alkaline

Initial C/N ratio Between 20 and 50 30:1 (Ideal proportion)pH No requirement Between pH 5 to 8Moisture content Coarse organic waste: 70e75%

Fine organic waste: 55e65%40e55% (Preferable)

Product characteristics Texture is coarser and may contain heavy metals Texture is finer and heavy metals accumulatedin earthworm bodies

Source: Chowdhury et al. (2013), Singh et al. (2011), Wu et al. (2014).

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278266

either compost or vermicompost had important consequences forboth soil and water microbial abundance and diversity. Bothcompost (Fourti, 2013) and vermicompost (Lim et al., 2015b) areknown to positively affect soil structure as well as increasing itsmicrobial population and activity. Due to the characteristicspossessed by the organic fertilizers, Quir�os et al. (2014) concludedthat the organic fertilizers were suitable substitutes for mineralfertilizer. A study conducted by Cabanillas et al. (2013) showed thatbasil plant produced better growth when vermicompost was usedas compared to urea. Furthermore, the use of organic fertilizerreduced the quantity of organic fraction that would end up inlandfills; and optimized the nutrients that were already in usewithout requiring the extraction of more nutrients by not dis-rupting the natural cycle (Quir�os et al., 2014).

3.1. Composting of organic waste

Briefly, composting process can be divided into three phases,namely initial activation, thermophilic and mesophilic or matura-tion phase (Chowdhury et al., 2013). The majority of the organicwaste degradation happens during the thermophilic phase. In thisphase, microorganisms degrade the readily available compounds inthe organic waste. Generally, high microbial activity translates tohigh degradation of organic waste (Fourti, 2013). This phase ischaracterized by high temperature in the composting pile due tothe heat released from the microbial catabolism of organic waste(Singh and Kalamdhad, 2014). The high temperature achieved inthis phase is also crucial for pathogen reduction and sanitization oforganic waste. Temperatures above 55 �C are required to kill thepathogens in the organic waste (Tian et al., 2012). The EPA guide-lines require composting material to maintain a temperature of55 �C for at least 15 days or 5 consecutive days (Jurado et al., 2014a).Some composting piles are known to reach temperatures as high as70 �C during the degradation of animal manure (Tang et al., 2011)and green waste (C�aceres et al., 2015). The end of the thermophilicphase and beginning of the maturation phase is indicated by thetemperature decrease in the composting pile. As the organic wastestabilizes, the temperature will continue to decrease to ambient airtemperature (S�anchez-Monedero et al., 2010). The temperaturedecrease also marks the exhaustion of decomposable organicfraction in the waste (Ravindran and Sekaran, 2010).

Table 4 shows a variety of organic solid waste that has suc-cessfully undergone composting process. The majority of thecomposting process was done under aerobic conditions and theduration of the process was dependent on the composting systemand scale of the process. It was also observed from Table 4 thatdifferent organic waste achieved different peak temperature duringthe thermophilic phase which can be attributed to the differentinitial C/N ratio of the organic waste. Higher temperature in com-posting pile is an indication of higher microbial activities (Yahya

et al., 2010), which in turn is enhanced by the available carbonsources in the organic waste (Raj and Antil, 2011). However, high C/N ratio will limit the composting rate as there is an excess ofdegradable substrate for the microorganisms (Bernal et al., 2009).This was proven by Singh and Kalamdhad (2012) whereby thewaste materials containing the highest amount of available carbonhad lower temperature during the thermophilic phase. On theother hand, with lower C/N ratio there is an excess of nitrogen perdegradable carbon and inorganic nitrogen is produced in excesswhich can be lost through ammonia volatilization or by leaching(Bernal et al., 2009). Thus, an optimum initial C/N ratio of organicwaste is necessary for the growth of microorganisms. Different typeof organic waste can be combined to obtain the desired initial C/Nratio for higher composting efficiency (Table 4). Besides, themixture of organic waste also helps adjust moisture content(Tsutsui et al., 2013) and provide structural support to create inter-particle void for enhancing composting process (C�aceres et al.,2015).

Some composting studies that were reported did not achievethe thermophilic temperature. For example, Paradelo et al. (2013)noted that the temperatures were in the mesophilic range duringcomposting of lignocellulosic winery waste, but an evidence oforganic waste decomposition was found. Low temperature duringcomposting process could be caused by low ambient temperatureor heat retention properties of the compostingmaterials (Singh andKalamdhad, 2014). In fact, low temperature is typical for homecomposting because the layer for decomposing material is too thinto retain a significant amount of heat and the heat is quicklytransferred out from the pile. Although organic waste could bedecomposed in low temperature conditions, the end product is notguaranteed to be free of pathogens or weed seeds (Faverial andSierra, 2014).

Composting is typically a time consuming process, butadvancement in composting technology has reduced the durationof composting process. Gabhane et al. (2012) showed that additives,such as jaggery and polyethylene glycol, helped hasten the com-posting process as well as produce superior quality compost. Theonly downside was that the additives were not cost effective. Apartfrom additives, microbial inoculums were also used to reduce theduration of composting process. For example, an addition of spe-cific strain of fungal consortium like Trichoderma viride MTCC 793,Aspergillus niger MTCC 1344 and Aspergillus flavus MTCC 1425increased the composting rate of municipal solid waste. Theresultant compost had lower C/N ratio and germination indexvalues of 84e93% as compared to municipal solid waste withoutintroducing fungal inoculation (Awasthi et al., 2014). Microbescould also be added to the composting process by an addition ofanother type of organic waste, which contained indigenous mi-crobes. For example, Zainudin et al. (2013) used palm oil milleffluent as microbial seeds to increase the composting rate of oil

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Table 4Composting of different types of organic waste.

Organic waste Amendment/Bulking agent Type ofcompostingsystem

Compostingduration (d)

Comments References

Animal waste:Anaerobic digestate of pig

slurryWheat straw, vine shootprunings, pepper plantprunings, almond shellpowder

Aerobic,thermos-composters(350L)

~42 - Peak temperature: >50 �C within the first week- Maturation period: 1 month

Bustamanteet al. (2013)

Beef manure Sawdust Aerobic, pile 28 (self-heatingperiod)

- Peak temperature: 70 �C after 2 d- Temperature of pile at 50 �C after 28 d

Millner et al.(2014)

Cattle manure Sawdust Aerobic,reactor

31.75 Tsutsui et al.(2013)

Cattle slurry and hen manure Barley straw Aerobic, lab-scale reactor

31 - Peak temperature: 55e68 �C within 2.5e3.3 d Chowdhuryet al. (2014b)

Cow manure Sawdust Aerobic,bench-scalereactors

63 - Mesophilic composting- Addition of CaCN2 to reach sanitary standard rapidly.

Simujide et al.(2013)

Pig manure Aerobic, pile 91 - Addition of maggots- Two-stage composting phases: i) Maggot treatment (days1e9); ii) Thermophilic (days 10e18); iii) Mesophilic(days 19e43) and iv) Thermostable (days 44e92)

Zhu et al.(2012)

Pig manure Woodchips Aerobic,windrow

91e105 - Peak temperature: 63.8e63.9 �C average- Thermophilic phase duration: 4e6 weeks withtemperature >40 �C

- Maturation period: 2 months

V�azquez et al.(2015)

Pig manure and corn stalk Mature compost Forced-draftaeration,vessel

30 - Peak temperature: >55 �C for 12 d.- Converged to ambient temperature on day 29.

Luo et al.(2014)

Sheep bedding Cattle manure Aerobic,windrow

82e96 - Thermophilic phase duration: 10e25 d at temperature>50 �C

Costa et al.(2015)

Swine manure Sawdust Aerobic, lab-scale reactor

- Peak temperature: >40 �C for 2 d- Final compost did not meet the sanitation requirements.

Kang et al.(2014)

Swine manure Mushroom residues Aerobic,openwindrow

52 - Peak temperature: ~55 �C for the whole compostingperiod.

Wu et al.(2011)

Swine manure and rice husk Bacteria and fungi Aerobic,windrow

69 - Thermophilic phase duration: 44 d with peak temperatureat 72 �C

- Cooling duration: 25 d

Tang et al.(2011)

Agro-industrial waste:Apple and tobacco waste e Forced-

aeration, in-vessel

22 - Peak temperature: 54.7 �C- Temperature >45 �C for 8 d

Kop�ci�c et al.(2014)

Chicken feathers from poultryprocessing company

Pine bark; rye straw Aerobic, bins 210 Korniłłowicz-Kowalska andBohacz (2010)

Empty fruit bunch, palm oil milleffluent and decanter cakeslurry

Aerobic,turningfurrow

51 - Peak temperature: 79 �C- Temperature > 50 �C for ~45 d

Yahya et al.(2010)

Hydrolyzed grape marc andvinification lees

Aerobic, in-vessel

150 - Temperatures reached were in the mesophilic range butlow C/N ratio was achieved.

Paradelo et al.(2013)

Oil palm empty fruit bunch 40 - Palm oil mill effluent anaerobic sludge added continuouslyat 3 d interval

Zainudin et al.(2013)

Olive mill waste (alperujo) Poultry manure; sheepmanure

Aerobic, pile 266 - Peak temperature: >50 �C from week 2 to 14 Tortosa et al.(2012)

Pressmud from sugar mill Mixed farm waste Aerobic,cementedpits

150 - Peak temperature: >45 up to 61e68 d Raj and Antil(2011)

Spent grape marc; vinificationlees and hydrolyzed grapemarc from winery industry

Aerobic,compostingvessels

150 - Temperatures in mesophilic range Paradelo et al.(2013)

Two-phase olive mill waste Sheep manure; olive treepruning; horse manure

Aerobic,windrow

182 - Peak temperature: 50e70 �C for 10 weeks S�anchez-Monedero et al.(2010)

Wet husks from olive mill Aerobic, pile 200 - Peak temperature: 45 �C for 80 d Agnolucci et al.(2013)

Municipal organic waste:Banana peel Poultry litter Aerobic;

anaerobic84 - Peak temperature (aerobic): 69.5 �C

- Peak temperature (anaerobic): 58.5 �CKalemelawaet al. (2012)

Digested sewage sludge Green waste and pine bark Forcedaeration,windrow

180 - Initial phase (4 to 50e60 d) was characterized by intensivedegradation.

- Stabilization phase: up to 146 d

Albrecht et al.(2011)

Wood shaving 35 - Temperature: >55 �C

(continued on next page)

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 267

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Table 4 (continued )

Organic waste Amendment/Bulking agent Type ofcompostingsystem

Compostingduration (d)

Comments References

Food, vegetable, garden andoffice waste

Aerobic,windrow

Awasthi et al.(2014)

Green waste Thermocolboxes

21 - Additives used: jaggary, polyethylene glycol, lime,phosphogypsum, fly ash)

- Peak temperature: >50 �C for 3e4 d

Gabhane et al.(2012)

Greenhouse waste Cattle manure Aerobic, lab-scale reactor

21 - Peak temperature:>50 �C for ~11 d Külcü andYaldiz (2014)

Kitchen and garden waste Aerobic,homecomposter

84 - Peak temperature: 30e43 �C Faverial andSierra (2014)

Kitchen bio-waste; anaerobicsludge; aerobic sludge

Peat Passiveaerationcomposter

441 - Peak temperature:i) Kitchen bio-waste e 63 �C (4 weeks)ii) Anaerobic sludge - 57 �C (2 weeks)iii) Aerobic sludge e 44 �C (mesophilic)

- After 84 d, all waste reached ambient temperature

Himanen andH€anninen(2011)

Municipal solid waste; driedsewage sludge

Aerobic,windrow

200 - Temperature: >50 �C between 30 and 130 d Fourti (2013)

Post-harvest tomato plants andpine chips

Wood chips Forcedaeration, pile

136 - Temperature: 65e70 �C after 24e48 h Jurado et al.(2014b)

Shredded green waste (GW) Cattle slurry (CS) Forcedaeration,static pile

196 - Peak temperature:i) 1GW:3CS e 76 �C (98 d intensive composting; 98 d

stabilization)ii) 3GW:1CS e 79.9 �C (168 d intensive composting; 28 d

stabilization)

C�aceres et al.(2015)

Tomato plant waste Sawdust Forcedaeration, pile

189 - Bio-oxidative phase: 63 d- Maturation phase: 123 d- Temperature: >60 �C after 48 h

Jurado et al.(2014a)

Industrial waste:Digested solids from biogas

plantPlastic tube pieces,woodchips, bio-char, barleystraw, lupin residues

Aerobic,cylindricalreactors

28 - Thermophilic conditions: >45 �C within 2 d Chowdhuryet al. (2014a)

Dregs from pulp mill industry Pine bark; wood chips;glucose

Aerobic,reactor

70 - Temperature: 40e57 �C for 15 d Zambrano et al.(2010)

Limed animal fleshing fromtannery industry

Cow dung, leaf litter Aerobic,compostbioreactor

49 - Peak temperature: 59 �C on day 28 Ravindran andSekaran (2010)

Oiled bleaching earth fromvegetable fats manufacturer

Dewatered sewage sludge;maize straw

Aerobic, two-chamberbioreactor

45 - Peak temperature: 64 �C on day 4 Piotrowska-Cyplik et al.(2013)

Paint sludge frommanufacturing industry

Waste paper; plant residue;mature compost

Aerobic,middle-scalevessel

84 - Temperature: <40 �C Tian et al.(2012)

Others:Opium poppy processing waste Aerobic, pile 55 - Temperature: >50 �C after 14 d Wang et al.

(2014b)Phumdi (combination of

different type of weeds)Cattle manure, rice husk Aerobic, pile 30 - Peak temperature: 46.8 �C on the 8th day (5 phumdi: 4

cattle manure: 1 rice husk)Singh andKalamdhad(2014)

Tanned leather waste Food waste Aerobic,compostingtank

20e45 - Peak temperature: ~40 �C- Composting tank equipped with hot water circulationinside (35 �C)

Zuriaga-Agustíet al. (2015)

Water hyacinth Cow dung; sawdust; lime Agitated pile 30 - Thermophilic conditions: ~57 �C for 15 d Singh andKalamdhad(2013)

Water hyacinth (Eichhorniacrassipes)

Cow manure, sawdust Agitated pile 30 - Temperature ranged during composting phases: 26e56 �C Singh andKalamdhad(2012)

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278268

palm empty fruit bunch. The continuous addition of palm oil milleffluent shortened the composting duration from 60e90 d to 40 d.

The intention of composting process is to convert organic wasteinto fertilizer for agricultural or land use. However, certain organicwaste contains high concentrations of heavy metal contents thatare not removed during composting process. Generally, total heavymetal contents will increase after composting process owing to thereduction of organic matter but it is the bioavailability and mobilityof heavy metals that provide more significant information oftoxicity (Singh and Kalamdhad, 2013b). Singh and Kalamdhad

(2012) used Tessier sequential extraction method to trackchanges in heavy metal speciation during composting process.Their study concluded that with an addition of appropriate pro-portion of cattle manure, available fractions of heavymetal could besignificantly reduced due to better humification. The acidic func-tional groups in humic substances had high complexity capacitieswith metal ions, thus heavy metals could be bound to them easily(Güng€or and Bekb€olet, 2010). Lime, an alkaline material was alsoproven to help reduce the heavy metal bioavailability significantlyduring composting process (Singh and Kalamdhad, 2013b). Besides

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Table 5Vermicomposting of different types of organic waste.

Organic waste Amendment/Bulking agent Earthworms Pre-treatment(duration, d)

Vermicompostingduration (d)

References

Animal Waste:Animal waste: Cow, sheep, pig,

chickenE. eugeniae Yes (15) 147 Coulibaly and Zoro Bi (2010)

Cattle dung E. fetida Yes (7) 90 Lv et al. (2013)Cattle manure Soil Metaphire posthuma; Lampito

mauritii; Allolobophora parvae 60 Suthar (2014)

Cattle manure Rock powders E. andrei e 60 de Souza et al. (2013)Cattle manure Sugarcane bagasse;

sunflower cakeE. foetida Yes (30) 120 Aguiar et al. (2013)

Cattle manure E. fetida Yes (30) 120 Martinez-Balmori et al. (2013)Cow dung P. excavatus e 75 Suthar (2012)Cow dung Allobophora parva 147 Suthar (2011)Pig manure Vermicompost E. fetida e 252 Monroy et al. (2011)Pig slurry E. fetida e 252 G�omez-Brand�on et al. (2011a)

Agro-industrial waste:Biosolid vinasse and vine shoots Vermicompost E. fetida Yes (14) 105 Castillo et al. (2013)Empty fruit bunches from palm oil mill Cow dung E. eugeniae e 84 Lim et al. (2015a)Filter cake from sugarcane factory E. fetida Yes (30) 120 Martinez-Balmori et al. (2013)Grape marc from winery industry Mature vermicompost E. andrei 15 G�omez-Brand�on et al. (2011b)Lees cake vinasse from winery-

distillery industriesPre-composted/vermicomposted rabbitmanure

E. fetida e 56 Molina et al. (2013)

Palm oil mil effluent (POME) Rice straw; soil E. eugeniae Yes (14) 42 Lim et al. (2014)Pressmud from sugarcane industry Cow dung E. fetida Yes (10) 120 Bhat et al. (2014)Pressmud from sugar industries Cow dung P. ceylanensis e 60 Prakash and Karmegam

(2010)Press-mud, bagasse and sugarcane

trash from sugar mill industriesDrawida willsi Yes (30) 40 Kumar et al. (2010)

Rice husk Market refused fruits E. eugeniae e 63 Lim et al. (2012)Rice husk, rice straw Cow dung E. eugeniae e 60 Shak et al. (2014)Sago industry waste Cow dung; poultry manure E. foetida Yes (21) 45 Subramanian et al. (2010)Soybean husk Papaya E. eugeniae e 63 Lim et al. (2011)Wet olive cake and goat manure Vermicompost E. fetida Yes (14) 126 Castillo et al. (2013)

Municipal organic waste:Fresh fruit and vegetable waste Soil; vermicompost E. foetida e 35 Huang et al. (2014)Fresh sewage sludge Cow dung; straw E. foetida Yes (14) 90 Li et al. (2011)Fresh water weeds (macrophytes) Cow dung E. fetida e 60 Najar and Khan (2013)Greenhouse vegetable residues Cow dung; straw E. andrei Yes (7) 84 Fern�andez-G�omez et al.

(2010)Leaf litters Cow dung E. fetida Yes (21) 70 Suthar and Gairola (2014)Municipal sewage sludge Powdered oyster shell E. andrei e 25 Kwon et al. (2009)Municipal solid waste Cow dung P. ceylanensis Yes (1) 50 John Paul et al. (2011)Pre-consumer processing vegetable

wasteCow dung E. fetida Yes (21) 105 Garg and Gupta (2011)

Sewage sludge Cattle dung; sawdust E. fetida Yes (14) 120 Lv et al. (2014)Sewage sludge Rice straw E. fetida 21 Yang et al. (2014)Sewage sludge Cow dung; straw E. fetida Yes (14) 60 Xing et al. (2012)Sewage sludge Pre-composted/

vermicomposted rabbitmanure

E. fetida e 56 Molina et al. (2013)

Sewage sludge Fly ash; phosphoric rock E. fetida Yes (15) 60 Wang et al. (2013c)Sewage sludge Fly ash; phosphatic rock E. fetida Yes (20) 70 Wang et al. (2013b)Tomato plant waste Paper-mill sludge; Cattle

manureE. fetida e 105 Fern�andez-G�omez et al.

(2011)Tomato-plant waste Paper-mill sludge E. fetida Yes (14) 168 Fern�andez-G�omez et al.

(2013, 2015)Vegetable waste Vermicompost (from food

waste and cow dung)E. foetida Yes (7) 60 Huang et al. (2013)

Industrial waste:Animal fleshing from leather

industriesCow dung, leaf litter E. eugeniae Yes (3) 25 Ravindran et al. (2014);

Ravindran et al. (2013)Bio sludge from beverage industries Cattle dung E. fetida Yes (15) 120 Singh et al. (2010)Dye laden slurry Cow dung E. fetida Yes (15) 45 Kaushik et al. (2012)Dyeing sludge from textile mill

industriesCattle dung E. fetida Yes (15) 90 Bhat et al. (2013)

Fly ash from thermal plant and vinassefrom distillery industry

E. fetida, E. eugeniae e 63 Pramanik and Chung (2011)

Herbal pharmaceutical industrialwaste

Cow dung E. fetida Yes (7) 60 Singh and Suthar (2012a);Singh and Suthar (2012b)

Paper mill sludge from paper millindustries

Cow dung E. fetida Yes (7) 56 Negi and Suthar (2013)

(continued on next page)

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 269

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Table 5 (continued )

Organic waste Amendment/Bulking agent Earthworms Pre-treatment(duration, d)

Vermicompostingduration (d)

References

Pulp sludge from paper manufacturingcompany

Powdered oyster shell E. andrei e 25 Kwon et al. (2009)

Shredded waste paper Cow dung; rock phosphate E. fetida e 42 Unuofin and Mnkeni (2014)Tannery sludge Cattle dung E. fetida Yes (20) 120 Vig et al. (2011)Wastewater sludge from paper and

pulp industryCow dung E. fetida Yes (7) 60 Suthar et al. (2014)

Wood waste from timber industries D. willsi Yes (30) 40 Kumar and Shweta (2011)

Others:Water hyacinth (Eichhornia crassipes) Cow manure, sawdust E. fetida 45 Singh and Kalamdhad

(2013a); (2013c)Water hyacinth (Eichhornia crassipes) Cow dung E. eugeniae Yes (30) 40 Subhash Kumar et al. (2015)Weed (Parthenium hysterophorus L.) Cow dung E. eugeniae Yes (60) 45 Rajiv et al. (2013); Rajiv et al.

(2014)

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278270

heavy metal, composting could also degrade resistant compoundssuch as phenols (S�anchez-Monedero et al. (2010), morphine (Wanget al., 2014b) and melamine resins (Tian et al., 2012).

3.2. Vermicomposting of organic waste

Vermicomposting has been attempted on many types of organicsolid waste such as animal manure, sewage sludge, vegetablewaste, industrial sludge and agriculture waste (Table 5). Vermi-composting, similar to composting process, is also an organic wastedecomposition process but with an addition of earthworms to aidand hasten the waste stabilization process (Lim et al., 2015b).Therefore, suitable organic waste or feedstock for earthworms iscrucial to ensure a successful and efficient vermicomposting pro-cess (Yadav and Garg, 2011a). Earthworms can consume mostorganic materials that have pH in the range from 5 to 8, moisturecontent between 40 and 55% and initial C/N ratio around 30(Table 3). However, not all organic waste fall within these param-eters. Therefore, to make the organic waste more suitable for ver-micomposting, the waste should be: i) amended with bulkingagents/organic waste (or amendments) or ii) undergone some formof pre-treatment process.

During vermicomposting process, bulking agents or amend-ments are used to make the organic waste more palatable for theearthworms. For example, cow dung is commonly used as anamendment in vermicomposting process because it is the easiestanimal waste for growing the earthworms (Edwards, 2004). Fruitwaste could also be used in some instances as amendments duringvermicomposting of soybean husk (Lim et al., 2011) and rice husk(Lim et al., 2012). Some organic waste that have high moisturecontent are amended with bulking agents (or amendments) toreduce the moisture content. In fact, liquid waste like palm oil milleffluent was absorbed onto a bulkingmaterial for vermicompostingprocess (Lim et al., 2014). Other amendments used are soil andmatured vermicompost (Huang et al., 2014). Vermicompost is usedto provide an initial habitat for earthworms and as a source ofmicrobial inoculums (Castillo et al., 2013). Lignocellulosic organichas high carbon content, hence this waste could be mixed withother organic waste that has low carbon content to improve theinitial C/N ratio of the waste mixtures (Castillo et al., 2013). Otherexample includes animal fleshing waste from tannery industrywhich had low C/N ratio, thus it was suitable to be amended withleaf litter and cow dung (Ravindran et al., 2014). Optimum initial C/N ratio of feedstock for vermicomposting is around 30, but it ispossible to vermicompost organic waste which has higher C/N ratio(Pramanik and Chung, 2011). For example, Lim et al. (2015a) suc-cessfully vermicomposted empty fruit bunches and cow dung that

had initial C/N ratio >50. After 12 weeks of vermicomposting, the C/N ratio of the waste mixture dropped to <20.

Some organic waste could be vermicomposted without usingbulking materials but some form of pre-treatment process shouldbe introduced prior to vermicomposting process. For example,dried cow dung is commonly used as an amendment but fresh cowdung is unfavorable for the growth of earthworms (Edwards, 2004).Thus, cow dungwas dried under natural sunlight for oneweekwithperiodic turning as a pre-treatment process (Lv et al., 2013). Pre-treated cow dung could be used alone (Suthar, 2012) or mixedwith other organic waste (Aguiar et al., 2013) for vermicompostingprocess. Therefore, in most vermicomposting studies, it is a com-mon practice to pre-treat the organic waste by at least turning thewaste manually to eliminate the volatile gases which are toxic tothe earthworms (Lim et al., 2014) and reduce highmoisture contentin some organic waste (Yang et al., 2014). Pre-treatment also en-courages initial microbial degradation and softening of the waste(Suthar and Gairola, 2014).

Similar to the compost, the presence of heavy metals in thevermicompost poses a serious threat to human and environmentowing to its agricultural application. Singh and Kalamdhad(2013a) found that vermicomposting process was effective inreducing most of the bioavailable fractions of heavy metals. Theheavy metal ions could form complexes with humic substancespresent in the vermicompost. Various organic functional groupsin the humic compounds could bind with metal ions throughionic forces. Singh and Kalamdhad (2013c) confirmed that theleachable concentration of heavy metals in the vermicompostwas under the threshold limit. Moreover, earthworms were ableto accumulate heavy metals in the organic waste via skin ab-sorption or in their intestine (Lim et al., 2015b). Suthar et al.(2014) found that some available fractions of heavy metalswere removed by the earthworms through gut/skin absorption.Heavy metal content found in the worm tissues confirmed thetheory that earthworms had the capability to regulate metals.Additives like fly ash and phosphatic rock functions could also beused as an immobilizing amendment to reduce the heavy metalsavailability (Wang et al., 2013b).

One of the major concerns using vermicomposting process isthat it does not involve a thermophilic stage. However, limitedstudies showed that vermicomposting could reduce pathogens inthe organic waste. Yadav et al. (2010) detected no coliforms in themature vermicompost derived from source-separated human fecal.It was suggested that pathogens were killed or reduced through theaction of intestinal enzymes in the earthworms as well as thecompetition between pathogens and microbes for the limited re-sources that earthworms left behind (Sim and Wu, 2010). Thisresult was supported by Hill and Baldwin (2012) who proved the

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S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 271

viability of using vermicomposting to convert fecal matter andtoilet paper into vermicompost which had lesser Escherichia coli.

3.3. Integration of composting-vermicomposting process

Organic waste stabilization through composting or vermi-composting is well established and proven to be feasible. However,each of this process has its own disadvantages. In the compostingprocess, longer duration is needed for waste stabilization and theorganic waste requires frequent aeration to maintain aerobic con-ditions (Hait and Tare, 2011b). The major drawback during vermi-composting process is the low temperature required for theduration of the process due to the presence of earthworms. Thewaste might not be sanitized at low temperature and the vermi-compost could not meet the required level of pathogen in theorganic fertilizer (Fornes et al., 2012). Thus, an integrated com-postingevermicomposting process is suggested to overcome thedisadvantages of each stabilization process. The composting stagein the integrated system will ensure that the produced fertilizer isfree from pathogens due to the presence of thermophilic stage,while the vermicomposting stage reduces the particle size andincreases available nutrient recovery at a much higher rate with thepresence of earthworms. In addition, earthworms can help to turnand mix the organic waste which will help reduce the cost neededto maintain aerobic conditions during organic matter stabilization(Dominguez and Edwards, 2011). Besides, the integrated systemallows for awider range of organic waste to be treated. For example,highmoisture content of faecal slurry was not suitable to be used asa direct feedstock for vermicomposting process. Therefore,

Table 6Integration compostingevermicomposting of organic waste.

Organic waste Amendment/Bulking agent Composting

Duration(days)

Comm

Activated sewage sludge Corn stalk, compost, cowmanure, paper

30 e

Animal manure Mushroom residues 20 - ManApple pomace Straw 14 - Mec

Biogas digestate Wheat straw 14 - MecBiogas slurry Wheat straw, sugarcane

trash, guar bran21 - The

Cattle manure Sunflower cake 60 - The- Mec

Citronella plant (Cymbopogonwinterianus Jowitt.)

Cow dung 15

Dewatered sludge Horse manure, saw dust,grass clippings

90 - Pea

Duck manure Reed straw; zeolite 45 - Pea4 d

Food industry sludge Cow dung, poultry dropings 28 - Semther

Food industry sludge, biogas plantslurry, animal manure

28 - Semther

Milk processing industry sludge Cow dung, sugarcane trash,wheat straw

21 - The

Pig manure Rice straw 15 e

Primary sewage sludge; wasteactivated sludge

Matured vermicompost � 20rec

Sewage sludge Spent mushroom compost 21 - The- Man

Temple floral offerings Mature cow dung 15 - TheTomato crop residues Almond shells 63 - PeaWeed (Lantana camara) Cow dung 21 - The

Weed (Parthenium hysterophorus) Cow dung 21 - Sem- Man

composting stage could be introduced before the pre-treated wastewas subjected to vermicomposting process (Yadav et al., 2012).

Table 6 shows the integrated compostingevermicompostingsystem applied on different types of organic waste. Most studiesindicated that organic waste went through composting first andthen followed by vermicomposting. Ndegwa and Thompson (2001)compared the product obtained from two combined systems,namely vermicomposting followed by composting and compostingfollowed by vermicomposting. The conclusion from their studyshowed that composting followed by vermicomposting yieldedbetter end product. In most cases, a short period of composting canbe applied to pre-treat the waste before the pre-treated waste isundergone vermicomposting process at the later stage (Wu et al.,2014). Pre-treatment via pre-composting of organic waste usuallylasts for about 2e3 weeks and involves thermal stabilization,initiation of microbial degradation and softening of organic waste,making the pre-treated waste more palatable for earthworm con-sumption (Deka et al., 2011b). During pre-composting, organicwaste is turned periodically to ensure continuous aerobic conditionand remove any odor (Suthar and Sharma, 2013). After thecompletion of composting, earthworms are added to the com-posted organic waste for further stabilization and degradation. Theresultant vermicompost from the integrated system usually hasfinal C/N ratio of less than 20 and higher in available nutrients (Garget al., 2012).

A comparison between composting process alone and the in-tegrated system revealed higher organic matter stability and nu-trients (P, Mg and Ca) in the latter (Sierra et al., 2013). Ma�n�akov�aet al. (2014) showed that higher reduction of arsenic mobility andavailability in the integrated system as compared to composting or

Vermicomposting References

ents Duration(days)

Earthworms

40 E. fetida Kharazzi et al. (2014)

ually aerated every 2 d 100 E. fetida Song et al. (2014)hanically aerated 30 Eisenia Hanc and Chadimova

(2014)hanically aerated 150 Eisenia Hanc and Vasak (2015)rmal stabilization 105 E. fetida Suthar (2010)

rmophilic conditionshanically aerated

30 E. foetida Busato et al. (2012)

105 E. eugeniae; P.excavatus

Deka et al. (2011a,2011b)

k temperature: 50 �C 90 E. fetida Ma�n�akov�a et al. (2014)

k temperature: >55 �C for 32 E. fetida Wang et al. (2014a)

i-decomposition andmal stabilization

91 E. fetida Yadav and Garg (2011b)

i-decomposition andmal stabilization

105 E. fetida Garg et al. (2012)

rmal stabilization 90 E. fetida Suthar et al. (2012)

45 E. fetida Zhu et al. (2014)cycles of mixing and

ycling28 E. fetida Hait and Tare (2011a,

2011b, 2012)rmophilic conditionsual turning

105 L. rubellus Azizi et al. (2013)

rmophilic conditions 120 E. fetida Singh et al. (2013)k temperature: 70 �C 198 E. fetida Fornes et al. (2012)rmal stabilization 60 E. fetida Suthar and Sharma

(2013)i-compostingually aerated

126 E. fetida Yadav and Garg (2011c)

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vermicomposting process alone. Similarly, Soobhany et al. (2015)reported lower Cd, Cr, Cu, Co, Zn and Ni content in the integratedsystem as compared to composting process alone, suggesting thatearthworms reduced the heavy metals in the organic fertilizer byaccumulating the metals in their bodies during vermicompostingprocess. According to Wang et al. (2014a), lower greenhouse gasemissions were produced in the integrated system. Therefore, itwould seem that the integration of composting and vermi-composting process results in a higher quality organic fertilizer andposes lesser negative impact on the environment. Furthermore, thethermophilic composting stage in the integrated system also en-sures the fertilizer fulfilling the pathogen reduction requirements.

4. Environmental impact of composting andvermicomposting processes

Emissions of significant amount of greenhouse gases (GHGs)during composting and vermicomposting processes are leading tosecondary pollution such as greenhouse effect, thus mortifying theenvironmental benefits of both processes. As stated by Hao et al.(2004), losses of carbon (C) and nitrogen (N) during compostingprocess will reduce the agronomic value of the compost. GHGs arereleased due to the energy needed by the composting facility (i.e.machinery used) and by the biodegradation process itself whichproduces CO2, methane and nitrous oxide (Friedrich and Trois,2013). Most C is lost as CO2 while methane accounting for <6%(Hao et al., 2004), which are two of the most important GHGs in theatmosphere (Majumbar et al., 2006). Himanen and H€anninen(2011) stated that the emissions of CO2 implied the mineraliza-tion and degradation of organic matters. This statement corre-sponded well to the studies reported by Hao et al. (2004), Tsutsuiet al. (2013) and Luo et al. (2014), where they correlated theemissions of CO2 with a consumption of O2 in biodegradationprocess as the decomposition of organic matters consumed O2 andreleased CO2. Table 7 shows the GHG emissions for different typesof feedstock used in composting and/or vermicomposting.

Aeration and turning are known to be important factorsaffecting the emissions of GHGs, including CO2 during composting

Table 7GHGs emission for different types of feedstock.

Feedstock Amendment/Bulking agent Method

Straw-bedded cattle feedlot manure e CompostingWood chip-bedded cattle feedlot manure e CompostingDairy manure e CompostingAnimal manure e CompostingAnimal manure Plastic tube CompostingAnimal manure Woodchips CompostingAnimal manure Bio-char CompostingAnimal manure Barley straw CompostingAnimal manure Lupin residues CompostingCattle slurry High flow CompostingCattle slurry Low flow CompostingHen manure High flow CompostingHen manure Low flow CompostingHen manure Bio-char, high flow CompostingHen manure Bio-char, low flow CompostingHousehold waste e CompostingHousehold waste e VermicompostiDuck manure e VermicompostiDuck manure Reed straw VermicompostiDuck manure Reed straw, zeolite VermicompostiDuck manure e Combined pre-cDuck manure Reed straw Combined pre-cDuck manure Reed straw, zeolite Combined pre-c

process. Based on the experiment conducted by Chowdhury et al.(2014b), they concluded that low aeration was more effective inreducing GHG emissions, while Wang et al. (2013a) indicated thatintermittent aeration was better than continuous aeration inmitigating CO2 emissions. Turning enhanced air exchange in thepiles, thus decreasing methane emission and shortening thematuring period (Jiang et al., 2013). Experiment carried out by Luoet al. (2014) concluded that the emissions of GHGs during com-posting process could be efficiently controlled by turning andcovering pig manure with mature compost. For the composting ofGanqinfen pig manure, Jiang et al. (2013) also suggested that atreatment with turning twice weekly without covering wouldresult in compost that was sufficiently matured after six weekswith the lowest emissions of GHGs. Between aeration and turning,a study conducted by Friedrich and Trois (2013) reveled that duringcomposting of gardenwaste, turned windrow composting released8.14% higher GHGs than aerated dome composting. Their findingsmay prove that the use of aeration in composting could reduce theGHGs emissions as compared to composting with turning orwithout turning. To reduce GHGs emissions such as CO2, some re-searchers suggested that mature compost (Luo et al., 2014), bio-char (Chowdhury et al., 2014b) and C-bulking agent, such aswoodchips (Chowdhury et al., 2014b), sawdust or crop residues(Maeda et al., 2013), could be used tomix withmanure to adjust thecondition of the waste mixture prior to composting process. Li et al.(2013) showed that ammonia emission could be mitigated byadding a mixture of sucrose and straw powder at the beginningstage of composting process.

Until now, only handful of studies have been carried out toexamine the emission of GHGs during vermicomposting process.An earlier experiment done by Luth et al. (2011) showed that theemission of CO2 was increased by an elevation of manure input.However, decreases in emissions of ammonia and nitrous oxide aswell as a sink of methane in treatments with earthworms wereobserved, suggesting that earthworm abundance could be used todiscourage the production of GHGs (Luth et al., 2011). Further-more, results obtained by Chan et al. (2010) indicated that thetotal GHGs emissions, including both nitrous oxide and methane,

GHGs emission (gCO2-eq/kg waste)

Reference

CO2 N2O CH4

165.0 10.2 187.3 Hao et al. (2004)145.6 11.2 188.6587.0 48.0 153.0 Mulbry and Ahn (2014)62.3 2.81 1.39 Chowdhury et al. (2014a)63.2 1.97 0.7348.0 3.62 1.0841.2 1.79 0.1150.3 1.06 0.7461.2 1.29 6.3193.0 12.0 12.0 Chowdhury et al. (2014b)85.0 12.2 24.879.0 12.75 4.2570.0 14.63 4.3762.0 11.96 1.0454.0 12.22 0.78

e 4.27 0.43 Chan et al. (2010)ng e 3.37 0.93ng 26.6 53.67 0.12 Wang et al. (2014a)ng 27.8 16.39 0.06ng 23.9 15.02 0.1omposting and vermicomposting 264.4 77.69 0.26omposting and vermicomposting 308.7 27.65 0.15omposting and vermicomposting 312.5 32.75 0.15

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S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 273

were the lowest during vermicomposting of household waste inBrisbane, followed by methods using aerobic composting andanaerobic digestion. The lower emission of nitrous oxide from thevermicomposting system was probably offset by the reduction ofanaerobic denitrification, due to the burrowing action of theearthworms (Chan et al., 2010). Also, moisture content and tem-perature are two crucial factors that would affect the emission ofammonia and methane during vermicomposting process. Velasco-Velasco et al. (2011) reported that water content of 80% and 15 �Cwould produce lesser ammonia than 70% water content and 22 �C.Chan et al. (2010) further observed a reduction in methaneemission during vermicomposting process at lower temperature.On the other hand, a recent experiment using combined pre-composting and vermicomposting was carried out by Wanget al. (2014a). Wang et al. (2014a) showed that CO2 emissionwas not affected by the presence of the earthworms but therelease of CO2 was significantly increased by about 20% with anaddition of reed straw. This phenomenon could be due to theaddition of reed straw which helped promote the decompositionof duck manure at higher temperature in longer duration duringpre-composting process (Wang et al., 2014a). Wang et al. (2014a)concluded that the combined pre-composting and vermi-composting with additions of reed straw and zeolite not onlysuccessfully bio-transformed duck manure into organic fertilizerbut also reducing the emissions of ammonia, nitrous oxide andmethane significantly during biodegradation of duck manure.

Life cycle assessment (LCA) could be used in analyzing theenvironmental impacts of composting and vermicomposting pro-cess. According to Seo et al. (2004), global warming, eutrophicationand acidification were the main factors of causing impact to theenvironment. Global warming, the greatest contributor, was causedby CO2 and methane emissions (Seo et al., 2004), followed byacidification which was due to the emissions of NOx, SOx andammonia while eutrophication which was due to the emissions ofammonia and SOx (Cadena et al., 2009). Lou (2008) found that theGHG emissions during composting process was estimated to be0.284 ton CO2-eq/ton-of-mixed waste, with emissions from theoperational activities taken into account. Composting of municipalsolid waste produced lower GHGs as compared to the conventionallandfill in which 1.287 ton CO2-eq/ton-of-waste was emitted in theformer (Lou and Nair, 2009). Lou and Nair (2009) further justifiedthat the emissions from landfilling activities, such as trans-portation, excavation, compaction and soil spreading, would alsocontribute to overall GHG emissions. Similar results could beobserved from the study done by Banar et al. (2009), where land-filling was a greater contributor to global warming with an emis-sion of 6990 kg CO2-eq/ton-of-waste managed, as compared to thecomposting with an emission of 1370 kg CO2-eq/ton-of-wastemanaged. In addition, Lee et al. (2007) compared the environmentimpacts of landfill, incineration and composting. The resultsdemonstrated that incineration process was the main source ofglobal warming, with emissions of 580,317 g CO2-eq/ton-of-waste,followed by landfill and composting, with emissions of 409,433 and269,647 g CO2-eq/ton-of-waste, respectively (Lee et al., 2007).However, Güereca et al. (2006) found that the global warming wasmainly contributed by the emission of GHGs from landfilling, fol-lowed by incineration and composting. Yay (2015) furtherconcluded that among the waste management methods, com-posting demonstrated better performance, as compared to land-filling and incineration. On the other hand, between compostingand vermicomposting of biodegradable waste, Komakech et al.(2015) found that vermicomposting process caused 78.19% lesserGHG emission as compared to composting process which released80.9 kg CO2-eq/ton-of-waste. The huge variation in the GHGsemission observed was due to the different amount of solid waste

involved in the waste treatment processes as well as the durationand conditions of the processes.

Generally, reuse of solid waste through composting and ver-micomposting processes provide positive impact on the environ-ment. An application of compost or vermicompost on land, couldreduce the amount of chemical fertilizers and pesticides needed inagriculture, thus reducing possible environmental pollution (Louand Nair, 2009). Moreover, an application of compost and vermi-compost could enhance carbon sequestration in the soil, thusreducing the release of GHGs into the environment (Luth et al.,2011). Ruggieri et al. (2009) stated that the compost could act asa suppressor agent against different diseases occurred in the cropor plantation. Besides, the thermophilic condition in the com-posting process was able to prevent the threat of pathogen in-fections (Ruggieri et al., 2009). On the other hand, Chan et al. (2010)reported that the earthworms were able to reduce the volatilesulfur compounds emission, which would in turn decreased theenvironmental pollution.

5. Economic analysis of composting and vermicompostingprocesses

Thus far, composting and vermicomposting processes arefeasible organic waste management strategies because both pro-cesses are able to transform a wide variety of waste and withrelatively low environmental impact as compared to other man-agement options. It is also well-known that composting and ver-micomposting are sustainable processes in terms of economicaspects as they involve lower operating cost as compared to otherwaste management options (Ruggieri et al., 2009). The low costinvolved in composting system is due to low technical complexityand capital requirements (Galgani et al., 2014). Studies on economicanalysis of composting and vermicomposting process are scarceand to the best of our knowledge, no economic analysis was donepreviously on integrated composting-vermicomposting process.

Table 8 shows the economic assessment for composting andvermicomposting technology. Generally, the economic analysis incomposting system encompasses capital, labor, biomass, process-ing energy, repair and maintenance costs, revenue from compostproduction and disposal credit (Blumenstein et al., 2012). Ananaerobic sludge composting plant with a capacity of 7.12 � 106 kgrequired investment costs of approximately V462,646 and annualcost between V250,000 and V360,000. The composting plant wasequipped with an aeration system or/and turning vehicle andassuming 50% load for each composting type. Housing and gasemission treatment facilities were included for aerated compostingwhilst only roofing for composting with pile turning. The plant alsoincluded either asphalt or concrete platform to collect any leachateand precipitation. The revenue for the composting plant came fromselling 60% of the compost (V0.041 per kg) while the remainingcompost was used as a landfill cover. This set-up of compostingsystem and final use of compost was economically viable with apayback period of 2.9 years (Cukjati et al., 2012). Other studies alsoshowed economic viability of composting system as compared toother organic waste management method. Ruggieri et al. (2009)made a comparison between external management costs andcomposting costs of organic waste produced in wine industries.This study showed a savings of V19.56 per ton of organic waste ifcomposting was used to manage wine industries waste in com-parison with external management. Cost benefit analysis formunicipal solid waste management in Africa also showed thataerated openwindrow composting systemwas the better option ascompared to controlled landfilling (Couth and Trois, 2012).

Nevertheless, Blumenstein et al. (2012) highlighted that com-posting of semi-natural grassland was not profitable from an

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Table 8Economic assessment of several composting and vermicomposting technologies.

Treatment technology Capacity(t/y)

Life timescenarioanalysis (y)

Totalcost(USDmillion)

Totalrevenue(USDmillion/y)

Net presentvalue, NPV(USD million)

Internalrate ofreturn, IRR(%)

Paybackperiod,PBP (y)

Return oninvestment,ROI (%)

Remarks References

Integrated biogas andcompostingtechnology

218,570 10 6.29a 2.38 9.53 32 2.9 e - Clean Development Mechanism(CDM) was taken intoconsideration of economicanalysis

Yoshizakiet al.(2013)

Compostingtechnology

276,000 10 ~4.37a ~1.10 3.91 31 2.9 e - Clean Development Mechanism(CDM) was taken intoconsideration of economicanalysis

Yoshizakiet al.(2012)

Composting toilets ec 50 0.22b e 0.49 e 6e7 e - PBP at discount rates 0e12% Anand andApul(2011)

Vermicompostingsystem for urbansmall-holderfarmer

0.6e1.2 5 e e e e e 170e200 - Profit: USD 100e280 per annum Lalanderet al.(2015)

Composting plant inGhana

1500 10 ~0.24 ~0.13 e e e �16.25 - Economic analysis includesrevenue through carbon credits

Galganiet al.(2014)

Continuous-flowreactorvermicompostingsystem

36,500 e ~2.38 ~2.28 e e e e - Profit: USD ~2.06 million perannum

Edwardset al.(2010)

a Total cost ¼ Investment cost þ Annual operation and maintenance cost.b Total cost ¼ Lifetime manufacturing cost þ Lifetime operational cost.c Composting system similar to Sun Mar's Centrex 3000 A/F extra high capacity composting toilet systems. Composting tanks (0.8 � 0.7 � 1.8 m) were placed in the

basement of building (comprises approximately 2200 people) and every two toilets were connected to one single composting chamber.

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278274

investors' point of view as compared to producing solid fuel andbiogas from the biomass. Profitability could only be obtained whengrassland disposal costs were increased due to no other manage-ment options were available in a specific locality and shortages offossil fuels which led to higher fertilizer values (Blumenstein et al.,2012). Yoshizaki et al. (2012, 2013) showed that composting systemand integrated system of biogas plus composting had similar in-ternal rate of return and payback period but the net present valuewas higher in the integrated system (Table 8). Both of these studiesrevealed that composting system had lower investment and capitalcost but it brought in lesser revenue as compared to integratedsystemwith biogas generation (Blumenstein et al., 2012; Yoshizakiet al., 2013). Galgani et al. (2014) also reported that composting wasnot viable without external subsidies in a case study conducted atNorthern Ghana. However, composting was economically feasiblewithout any subsidies in Bangladesh and Indonesia (Galgani et al.,2014). Thus, the economic viability of composting system is hardto be determined as it depends on the cost of many parameterssuch as type of composting system, production volume, existingfacilities and equipment, feedstocks, compost prices and moreimportantly how the estimates were calculated (Rynk, 2001). Forexample, investment costs from different composting farms andcompost prices could be ranged from $20e40 and $15e35 per cubicyard compost, respectively (Rynk, 2001).

The capital cost of an indoor continuous-flow reactor vermi-composting system was estimated to be $2,159,000 and the oper-ating cost was $220,000 with an annual return of $2,275,000. Therevenue was inclusive of the sales of vermicompost and landfillsavings. Therefore, the potential annual profit was around$2,055,000. The price of vermicompost varies from $200 to $1000per ton, depending on its quality, unit size and packaging (Edwardset al., 2010). In Uganda, the market price for vermicompost was$0.08 per kg (Lalander et al., 2015), indicating that the vermicom-post revenue also depended on the location. Excess earthwormbiomass from the vermicomposting process can also generaterevenue. Market value for earthworm biomass can be ranged from

$5 to $35 per pound (Edwards et al., 2010). Similar to the com-posting system, the economic potential of a vermicompostingsystem is dependent on the initial costs as well as vermicompostand earthworm revenues at a particular location, making the ver-micomposting system not entirely feasible in certain scenarios.

Carbon markets also play a role in the economic feasibility ofcomposting system. Although composting contributes to lowerGHG emissions in comparison with landfilling, carbon offsets arenot considered for recycling of nutrients to produce compost fromorganic waste thus far. The carbon offsets have only be approved foravoiding methane formation from landfilling waste (Galgani et al.,2014). Until now, no economic analyses are attempted on inte-grated composting-vermicomposting system. Thus, one can onlyestimate the total cost of the process based on the individualcomposting and vermicomposting process. It can be postulated thatthe cost of an integrated compostingevermicomposting systemcontributed higher capital and annual costs than using compostingsystem alone. However, an integrated system could also bring inmore revenues due to the higher quality of organic fertilizer andsale of earthworm biomass.

6. Conclusion

The available literature proves that composting and vermi-composting technologies are able to degrade a variety of organicsolid waste and convert them into value-added product(s). Theintegration of composting-vermicomposting system was alsoproven to be more efficient than individual composting or vermi-composting process. This review also shows that during compost-ing and vermicomposting processes, the emitted GHGs would leadto secondary pollution which in turn mortifies the environmentalbenefits of both processes, but it can be mitigated. Mature compostand C-bulking agent could be used tomixwith the solid waste priorto composting or vermicomposting process to reduce the emissionsof GHGs. Economic assessment of composting and vermicompost-ing process are limited and those available are generally positive

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with some studies showing the opposite. The differences in eco-nomic potential is due to the differences in type of compostingsystem, market value of organic fertilizer, production volume andetc. Also, solid fuel and biogas generation systems are generallymore established and profitable than composting system, makingthe latter less desirable. Despite that, it is commonly known thatcomposting or vermicomposting system has low investment costthan other waste treatment methods. Additionally, both compost-ing and vermicomposting are considered as clean and sustainabletechnologies because they reuse waste to produce organic fertilizerwhich could be applied to agricultural lands.

Acknowledgments

The research was funded by Ministry of Higher Education,Malaysia under Fundamental Research Grant Scheme (FRGS/1/2013/STWN03/MUSM/02/1). In addition, the authors would like tothank Monash University Malaysia for providing both S.L. Lim andL.H. Lee with postgraduate scholarships.

References

Abbasi, S.A., Nayeem-Shah, M., Abbasi, T., 2015. Vermicomposting of phytomass:limitations of the past approaches and the emerging directions. J. Clean. Prod.93, 103e114.

Agnolucci, A., Cristani, C., Battini, F., Palla, M., Cardelli, R., Saviozzi, A., Nuti, M., 2013.Microbially-enhanced composting of olive mill solid waste (wet husk): bacterialand fungal community dynamics at industrial pilot and farm level. Bioresour.Technol. 134, 10e16.

Aguiar, N.O., Olivares, F.L., Novotny, E.H., Dobbss, L.B., Balmori, D.M., Santos-Júnior, L.G., Chagas, J.G., Façanha, A.R., Canellas, L.P., 2013. Bioactivity of humicacids isolated from vermicomposts at different maturation stages. Plant Soil362, 161e174.

Albrecht, R., Petit, J.L., Terrom, G., Perissol, C., 2011. Comparison between UVspectroscopy and nirs to assess humification process during sewage sludge andgreen wastes co-composting. Bioresour. Technol. 102, 4495e4500.

Anand, C., Apul, D.S., 2011. Economic and environmental analysis of standard, highefficiency, rainwater flushed and composting toilets. J. Env. Manag. 92,419e428.

Awasthi, M.K., Pandey, A.K., Khan, J., Bundela, P.S., Wong, J.W.C., Selvam, A., 2014.Evaluation of thermophilic fungal consortium for organic municipal solid wastecomposting. Bioresour. Technol. 168, 214e221.

Azizi, A.B., Lim, M.P.M., Noor, Z.M., Abdullah, N., 2013. Vermiremoval of heavy metalin sewage sludge by utilising Lumbricus reubellus. Ecotoxicol. Environ. Saf. 90,13e20.

Banar, M., Cokaygil, Z., Ozkan, A., 2009. Life cycle assessment of solid waste man-agement options for Eskisehir, Turkey. Waste Manag. 29, 54e62.

Bernal, M.P., Alburquerque, J.A., Moral, R., 2009. Composting of animal manures andchemical criteria for compost maturity assessment. A review. Bioresour. Tech-nol. 100, 5444e5453.

Bhat, S.A., Singh, J., Vig, A.P., 2013. Vermiremediation of dyeing sludge from textilemill with the help of exotic earthworm Eisenia fetida Savigny. Environ. Sci.Pollut. Res. 20, 5975e5982.

Bhat, S.A., Singh, J., Vig, A.P., 2014. Genotoxic assessment and optimization ofpressmud with the help of exotic earthworm Eisenia fetida. Environ. Sci. Pollut.Res. 21, 8112e8123.

Blumenstein, B., Bühle, L., Wachendorf, M., M€oller, D., 2012. Economic assessment ofthe integrated generation of solid fuel and biogas from biomass (IFBB) incomparison to different energy recovery, animal-based and non-refiningmanagement systems. Bioresour. Technol. 119, 312e323.

Busato, J.G., Lima, L.S., Aguiar, N.O., Canellas, L.P., Olivares, F.L., 2012. Changes inlabile phosphorus forms during maturation of vermicompost enriched withphosphorus-solubilizing and diazotrophic bacteria. Bioresour. Technol. 110,390e395.

Bustamante, M.A., Restrepo, A.P., Alburquerque, J.A., P�erez-Murcia, M.D., Paredes, C.,Moral, R., Bernal, M.P., 2013. Recycling of anaerobic digestates by composting:effect of the bulking agent used. J. Clean. Prod. 47, 61e69.

Butt, K.R., Briones, M.J.I., 2011. Life cycle studies of the earthworm Lumbricus friendi(Cognetti, 1904). Pedobiologia 54S, S27eS29.

Cabanillas, C., Stobbia, D., Ledesma, A., 2013. Production and income of basil in andout of season with vermicomposts from rabbit manure and bovine ruminalcontents alternatives to urea. J. Clean. Prod. 47, 77e84.

C�aceres, R., Coromina, N., Mali�nska, K., Marf�a, O., 2015. Evolution of process controlparameters during extended co-composting of green waste and solid fraction ofcattle slurry to obtain growing media. Bioresour. Technol. 179, 396e406.

Cadena, E., Col�on, J., Artola, A., S�anchez, A., Font, X., 2009. Environmental impact oftwo aerobic composting technologies using life cycle assessment. Int. J. LifeCycle Assess. 14, 401e410.

Castillo, J.M., Romero, E., Nogales, R., 2013. Dynamics of microbial communitiesrelated to biochemical parameters during vermicomposting and maturation ofagroindustrial lignocellulose wastes. Bioresour. Technol. 146, 345e354.

Chan, Y.C., Sinha, R.K., Wang, W.J., 2010. Emission of greenhouse gases from homeaerobic composting, anaerobic digestion and vermicomposting of householdwastes in Brisbane (Australia). Waste Manag. Res. 29, 540e548.

Chowdhury, A.K.M.M.B., Akratos, C.S., Vayenas, D.V., Pavlou, S., 2013. Olive millwaste composting: a review. Int. Biodeterior. Biodegr. 85, 108e119.

Chowdhury, M.A., Neergaard, A., Jensen, L.S., 2014a. Composting of solid separatedfrom anaerobically digested animal manure: effect of bulking agents andmixing ratios on emissions of greenhouse gases and ammonia. Biosyst. Eng.124, 63e77.

Chowdhury, M.A., Neergaard, A., Jensen, L.S., 2014b. Potential of aeration flow rateand bio-char addition to reduce greenhouse gas and ammonia emissions duringmanure composting. Chemosphere 97, 16e25.

Costa, M.S.S.M., Cestonaro, T., Costa, L.A.M., Rozatti, M.A.T., Carneiro, L.J.,Pereira, D.C., Lorin, H.E.F., 2015. Improving the nutrient content of sheepbedding compost by adding cattle manure. J. Clean. Prod. 86, 9e14.

Coulibaly, S.S., Zoro Bi, I.A., 2010. Influence of animal wastes on growth andreproduction of the African earthworm species Eudrilus eugeniae (Oligochaeta).Eur. J. Soil Biol. 46, 225e229.

Couth, R., Trois, C., 2012. Cost effective waste management through composting inAfrica. Waste Manag. 32, 2518e2525.

Cukjati, N., Zupan�ci�c, G.D., Ro�s, M., Grilc, V., 2012. Composting of anaerobic sludge:an economically feasible element of a sustainable sewage sludge management.J. Environ. Manag. 106, 48e55.

Curran, T., Williams, I.D., 2012. A zero waste vision for industrial networks inEurope. J. Hazard. Mater 207e208, 3e7.

Deka, H., Deka, S., Baruah, C.K., Das, J., Hoque, S., Sarma, N.S., 2011a. Vermi-composting of distillation waste of citronella plant (Cymbopogon winterianusJowitt.) employing Eudrilus eugeniae. Bioresour. Technol. 102, 6944e6950.

Deka, H., Deka, S., Baruah, C.K., Das, J., Hoque, S., Sarma, H., Sarma, N.S., 2011b.Vermicomposting potentiality of Perionyx excavates for recycling of wastebiomass of java citronella-an aromatic oil yielding plant. Bioresour. Technol.102, 11212e11217.

de Souza, M.E.P., de Carvalho, A.M.X., Deliberali, D.C., Jucksch, I., Brown, G.G.,Mendonca, E.S., Cardoso, I.M., 2013. Vermicomposting with rock powder in-creases plant growth. Appl. Soil Ecol. 69, 56e60.

Doan, T.T., Bouvier, C., Bettarel, Y., Bouvier, T., Henry-des-Tureaux, T., Janeau, J.L.,Lamballe, P., Nguyen, B.V., Jouquet, P., 2014. Influence of buffalo manure,compost, vermicompost and biochar amendments on bacterial and viral com-munities in soil and adjacent aquatic systems. Appl. Soil Ecol. 73, 78e86.

Doan, T.T., Ngo, P.T., Rumpel, C., Nguyen, B.V., Jouquet, P., 2013. Interactions betweencompost, vermicompost and earthworms influence plant growth and yield: aone-year greenhouse experiment. Sci. Hortic. 160, 148e154.

Dominguez, J., Edwards, C.A., 2011. Relationships between composting and vermi-composting. In: Edwards, C.A., Arancon, N.Q., Sherman, R. (Eds.), VermicultureTechnology. CRC Press, Boca Raton, USA, pp. 11e25.

Edwards, C.A., 2004. Earthworm Ecology, second ed. CRC Press LLC, Boca Raton,USA.

Edwards, C.A., Arancon, N.Q., Sherman, R., 2010. Vermiculture Technology: Earth-worms, Organic Wastes, and Environmental Management. CRC Press LLC, BocaRaton, USA.

European Environmental Agency (EEA), 2009. Diverting Waste from Landfill,Effectiveness of Waste-management Policies in the European Union. Report No7/2009. Office for the Official Publications of the European Communities,Luxembourg. http://dx.doi.org/10.2800/10886.

Faverial, J., Sierra, J., 2014. Home composting of household biodegradable wastesunder tropical conditions of Guadeloupe (Frence Antilles). J. Clean. Prod. 83,238e244.

Fern�andez-G�omez, M.J., Díaz-Ravi~na, M., Romero, E., Nogales, R., 2013. Recycling ofenvironmentally problematic plant wastes generated from greenhouse tomatocrops through vermicomposting. Int. J. Environ. Sci. Technol. 10, 697e708.

Fern�andez-G�omez, M.J., Nogales, R., Plante, A., Plaza, C., Fern�andez, J.M., 2015.Application of a set of complementary techniques to understand how varyingthe proportion of two wastes affects humic acids produced by vermicompost-ing. Waste Manag. 35, 81e88.

Fern�andez, R., Novo, M., Guti�errez, M., Almod�ovar, A., Cosín, D.J.D., 2010. Life cycleand reproductive traits of the earthworm Aporrectodea trapezoides (Dug�es,1828) in laboratory cultures. Pedobiologia 53, 295e299.

Fern�andez-G�omez, M.J., Romero, E., Nogales, R., 2010. Feasibility of vermi-composting for vegetable greenhouse waste recycling. Bioresour. Technol. 101,9654e9660.

Fern�andez-G�omez, M.J., Romero, E., Nogales, R., 2011. Impact of imidacloprid resi-dues on the development of Eisenia fetida during vermicomposting of green-house plant waste. J. Hazard. Mater 192, 1886e1889.

Fornes, F., Mendoza-Hern�andez, D., García-de-la-Fuente, R., Abad, M., Belda, R.M.,2012. Composting versus vermicomposting: a comparative study of organicmatter evolution through straight and combined processes. Bioresour. Technol.118, 296e305.

Fourti, O., 2013. The maturity tests during composting of municipal solid wastes.Resour. Conserv. Recycl. 72, 43e49.

Friedrich, E., Trois, C., 2013. GHG emission factors developed for the recycling andcomposting of municipal waste in South African municipalities. Waste Manag.33, 2520e2531.

Page 15: artículo de residuos solido

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278276

Gabhane, J., William, S.P.M.P., Bidyadhar, R., Bhilawe, P., Anand, D., Vaidya, A.N.,Wate, S.R., 2012. Additives aided composting of green waste: effects on organicmatter degradation, compost maturity, and quality of the finished compost.Bioresour. Technol. 114, 382e388.

Galgani, P., van der Voet, E., Korevaar, G., 2014. Composting, anaerobic digestion andbiochar production in Ghana. Environmental-economic assessment in thecontext of voluntary carbon markets. Waste Manag. 34, 2454e2465.

Garg, V.K., Gupta, R., 2011. Optimizing of cow dung spiked pre-consumer processingvegetable waste for vermicomposting using Eisenia fetida. Ecotoxicol. Env. Saf.74, 19e24.

Garg, V.K., Suthar, S., Yadav, A., 2012. Management of food industry wasteemploying vermicomposting technology. Bioresour. Technol. 126, 437e443.

G�omez-Brand�on, M., Aira, M., Lores, M., Domínguez, J., 2011a. Changes in microbialcommunity structure and function during vermicomposting of pig slurry. Bio-resour. Technol. 102, 4171e4178.

G�omez-Brand�on, M., Lazcano, C., Lores, M., Domínguez, J., 2011b. Short-term sta-bilization of grape marc through earthworms. J. Hazard. Mater 187, 291e295.

Güereca, L.P., Gass�o, S., Baldasano, J.M., Jim�enez-Guerrero, P., 2006. Life cycleassessment of two biowaste management systems for Barcelona, Spain. Resour.Conserv. Recycl. 49, 32e48.

Güng€or, E.B.€O., Bekb€olet, M., 2010. Zinc release by humic and fulvic acid as influ-enced by pH, complexation and DOC sorption. Geoderma 159, 131e138.

Hait, S., Tare, V., 2012. Transformation and availability of nutrients and heavy metalsduring integrated composting-vermicomposting of sewage sludges. Ecotoxicol.Environ. Saf. 79, 214e224.

Hait, S., Tare, V., 2011a. Optimizing vermistabilization of waste activated sludgeusing vermicompost as bulking material. Waste Manag. 31, 502e511.

Hait, S., Tare, V., 2011b. Vermistabilization of primary sewage sludge. Bioresour.Technol. 102, 2812e2820.

Hanc, A., Chadimova, Z., 2014. Nutrient recovery from apple pomace waste byvermicomposting technology. Bioresour. Technol. 168, 240e244.

Hanc, A., Vasak, F., 2015. Processing separated digestate by vermicompostingtechnology using earthworms of the genus Eisenia. Int. J. Environ. Sci. Technol.12, 1183e1190.

Hao, X.Y., Chang, C., Larney, F.J., 2004. Carbon, nitrogen balances and greenhousegas emission during cattle feedlot manure composting. J. Environ. Qual. 33,37e44.

Hill, G.B., Baldwin, S.A., 2012. Vermicomposting toilets, an alternative to latrinestyle microbial composting toilets, prove far superior in mass reduction,pathogen destruction, compost quality, and operational cost. Waste Manag. 32,1811e1820.

Himanen, M., H€anninen, K., 2011. Composting of bio-waste, aerobic and anaerobicsludges e effect of feedstock on the process and quality of compost. Bioresour.Technol. 102, 2842e2852.

Hoornweg, D., Bhada-Tata, P., Kennedy, C., 2013. Waste production must peak thiscentury. Nature 502, 615e617.

Hoornweg, D., Bhada-Tata, P., 2012. What a Waste: a Global Review of Solid WasteManagement. World Bank, Washington, DC, USA.

Huang, K., Li, F., Wei, Y., Chen, X., Fu, X., 2013. Changes of bacterial and fungalcommunity compositions during vermicomposting of vegetable wastes byEisenia foetida. Bioresour. Technol. 150, 235e241.

Huang, K., Li, F., Wei, Y., Fu, X., Chen, X., 2014. Effects of earthworms on physi-ochemical properties and microbial profiles during vermicomposting of freshfruit and vegetable wastes. Bioresour. Technol. 170, 45e52.

Jiang, T., Schuchardt, F., Li, G.X., Guo, R., Luo, Y.M., 2013. Gaseous emission duringthe composting of pig feces from Chinese Ganqinfen system. Chemosphere 90,1545e1551.

John Paul, J.A., Karmegam, N., Daniel, T., 2011. Municipal solid waste (MSW) ver-micomposting with an epigeic earthworm P. ceyleanensis Mich. Bioresour.Technol. 102, 6769e6773.

Jurado, M.M., Su�arez-Estrella, F., Vargas-García, M.C., L�opez, M.J., L�opez-Gonz�alez, J.A., Moreno, J., 2014a. Evolution of enzymatic activities and carbonfractions throughout composting of plant waste. J. Env. Manag. 133, 355e364.

Jurado, M.M., Su�arez-Estrella, F., Vargas-García, M.C., L�opez, M.J., 2014b. Increasingnative microbiota in lignocellulosic waste composting: effects on process effi-ciency and final product maturity. Process Biochem. 49, 1958e1969.

Kang, W., Kim, I., Lee, T., Kim, K., Kim, D., 2014. Effect of temperature on bacterialemissions in composting of swine manure. Waste Manag. 34, 1006e1011.

Kalemelawa, F., Nishihara, E., Endo, T., Ahmad, Z., Yeasmin, R., Tenywa, M.M.,Yamamoto, S., 2012. An evaluation of aerobic and anaerobic composting ofbanana peels treated with different inoculums for soil nutrient replenishment.Bioresour. Technol. 126, 375e382.

Karak, T., Bhagat, R.M., Bhattacharyya, P., 2012. Municipal solid waste generation,composition, and management: the world scenario. Crit. Rev. Environ. Sci.Technol. 42, 1509e1630.

Kaushik, P., Malik, A., Sharma, S., 2012. Vermicomposting: an eco-friendly option forfermentation and dye decolourization waste disposal. Clean. e Soil Air Water41, 616e621.

Kharazzi, S.M., Younesi, H., Abedini-Torghabeh, J., 2014. Microbial biodegradation ofwaste materials for nutrients enrichment and heavy metals removal: an inte-grated composting-vermicomposting process. Int. Biodeterior. Biodegr. 92,41e48.

Komakech, A.J., Sundbery, C., J€onsson, H., Vinnerås, B., 2015. Life cycle assessment ofbiodegradable waste management treatment systems for sub-Saharan Africancities. Resour. Conserv. Recycl 99, 100e110.

Korniłłowicz-Kowalska, T., Bohacz, J., 2010. Dynamics of growth and succession ofbacterial and fungal communities during composting of feather waste. Bio-resour. Technol. 101, 1268e1276.

Kop�ci�c, N., Domanovac, M.V., Ku�ci�c, D., Bri�ski, F., 2014. Evaluation of laboratory-scalein-vessel co-composting of tobacco and apple waste. Waste Manag. 34,323e328.

Külcü, R., Yaldiz, O., 2014. The composting of agricultural wastes and the newparameter for the assessment of the process. Ecol. Eng. 69, 220e225.

Kumar, R., Shweta, 2011. Enhancement of wood waste decomposition by micro-bial inoculation prior to vermicomposting. Bioresour. Technol. 102,1475e1480.

Kumar, R., Verma, D., Singh, B.L., Kumar, U., Shweta, 2010. Composting of sugar-canewaste by-products through treatment with microorganisms and subsequentvermicomposting. Bioresour. Technol. 101, 6707e6711.

Kwon, Y.T., Lee, C.W., Yun, J.H., 2009. Development of vermicast from sludge andpowdered oyster shell. J. Clean. Prod. 17, 708e711.

Lalander, C.H., Komakech, A.J., Vinnerås, B., 2015. Vermicomposting as manuremanagement strategy for urban small-holder animal farms e Kampala casestudy. Waste Manag. 39, 96e103.

Laner, D., Crest, M., Scharff, H., Morris, J.W.F., Barlaz, M.A., 2012. A review of ap-proaches for the long-term management of municipal solid waste landfills.Waste Manag. 32, 498e512.

Lee, S.H., Choi, K.I., Osako, M., Dong, J.I., 2007. Evaluation of environmental burdenscaused by changes of food waste management systems in Seoul, Korea. Sci.Total Environ. 387, 42e53.

Li, X., Xing, M., Yang, J., Huang, Z., 2011. Compositional and functional features ofhumic acid-like fractions from vermicomposting of sewage sludge and cowdung. J. Hazard. Mater. 185, 740e748.

Li, Y.B., Li, W.G., Wu, C.D., Wang, K., 2013. New insights into the interactions be-tween carbon dioxide and ammonia emissions during sewage sludge com-posting. Bioresour. Technol. 136, 385e393.

Lim, P.N., Wu, T.Y., Sim, E.Y.S., Lim, S.L., 2011. The potential reuse of soybean husk asfeedstock of Eudrilus eugeniae in vermicomposting. J. Sci. Food Agric. 91,2637e2642.

Lim, P.N., Wu, T.Y., Clarke, C., Daud, N.N.N., 2015a. A potential bioconversion ofempty fruit bunches into organic fertilizer using Eudrilus eugeniae. Int. J. En-viron. Sci. Technol. 12, 2533e2544.

Lim, S.L., Wu, T.Y., 2015. Determination of maturity in the vermicompost producedfrom palm oil mill effluent using spectroscopy, structural characterization andthermogravimetric analysis. Ecol. Eng. http://dx.doi.org/10.1016/j.ecoleng.2015.09.050.

Lim, S.L., Wu, T.Y., Clarke, C., 2014. Treatment and biotransformation of highlypolluted agro-industrial wastewater from palm oil mill into vermicompostusing earthworms. J. Agric. Food Chem. 62, 691e698.

Lim, S.L., Wu, T.Y., Lim, P.N., Shak, K.P.Y., 2015b. The use of vermicompost in organicfarming: overview, effects on soil and economics. J. Sci. Food Agric. 95,1143e1156.

Lim, S.L., Wu, T.Y., Sim, E.Y.S., Lim, P.N., Clarke, C., 2012. Biotransformation ofrice husk into organic fertilizer through vermicomposting. Ecol. Eng. 41,60e64.

L�opez-Gonz�alez, J.A., Su�arez-Estrella, F., Vargas-García, M.C., L�opez, M.J.,Jurado, M.M., Moreno, J., 2015. Dynamics of bacterial microbiota during ligno-cellulosic waste composting: studies upon its structure, functionality andbiodiversity. Bioresour. Technol. 175, 405e416.

Lou, X.F., 2008. A Mathematical Estimation of the Impact of Landfilling, Compostingand Anaerobic Digestion on Greenhouse Gas Emissions e the Total EmissionsAccountability Mode. Honours Thesis. Murdoch University, Australia.

Lou, X.F., Nair, J., 2009. The impact of landfilling and composting on greenhouse gasemissions-A review. Bioresour. Technol. 100, 3792e3798.

Lowe, C.N., Butt, K.R., 2008. Life cycle traits of the parthenogenetic earthwormOctolasion cyaneum (Savigny, 1826). Eur. J. Soil Biol. 44, 541e544.

Luo, W.H., Yuan, J., Luo, Y.M., Li, G.X., Nghiem, L.D., Price, W.E., 2014. Effects ofmixing and covering with mature compost on gaseous emissions duringcomposting. Chemosphere 117, 14e19.

Luth, Robin, P., Germain, P., Lecomte, M., Landrain, B., Li, Y.S., Cluzeau, D., 2011.Earthworm effects on gaseous emissions during vermifiltration of pig freshslurry. Bioresour. Technol. 102, 3679e3686.

Lv, B., Xing, M., Yang, J., Qi, W., Lu, Y., 2013. Chemical and spectroscopic charac-terization of water extractable organic matter during vermicomposting of cattledung. Bioresour. Technol. 132, 320e326.

Lv, B., Xing, M., Zhao, C., Yang, J., Xiang, L., 2014. Towards understanding the sta-bilization process in vermicomposting using PARAFAC analysis of fluorescencespectra. Chemosphere 117, 216e222.

Maeda, K., Hanajima, D., Morioka, R., Toyoda, S., Yoshida, N., Osada, T., 2013. Miti-gation of greenhouse gas emission from the cattle manure composting processby use of a bulking agent. Soil Sci. Plant Nutr. 59, 96e106.

Majumbar, D., Patel, J., Bhatt, N., Desai, P., 2006. Emission of methane and carbondioxide and earthworm survival during composting of pharmaceutical sludgeand spent mycelia. Bioresour. Technol. 97, 648e658.

Makan, A., Assobhei, O., Mountadar, M., 2014. Initial air pressure influence on in-vessel composting for the biodegradable fraction of municipal solid waste inMorocco. Int. J. Environ. Sci. Technol. 11, 53e58.

Ma�n�akov�a, B., Kuta, J., Svobodov�a, M., Hofman, J., 2014. Effects of combined com-posting and vermicomposting of waste sludge on arsenic fate and bioavail-ability. J. Hazard. Mater 280, 544e551.

Page 16: artículo de residuos solido

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278 277

Marshall, R.E., Farahbaksh, K., 2013. Systems approaches to integrated solid wastemanagement in developing countries. Waste Manag. 33, 988e1003.

Martinez-Balmori, D., Olivares, F.L., Spaccini, R., Aguiar, K.P., Araújo, M.F.,Aguiar, N.O., Guridi, F., Canellas, L.P., 2013. Molecular characteristics of vermi-compost and their relationship to preservation of inoculated nitrogen-fixingbacteria. J. Anal. Appl. Pyrolysis 104, 540e550.

Millner, P., Ingram, D., Mulbry, W., Arikan, O.A., 2014. Pathogen reduction in mini-mally managed composting of bovine manure. Waste Manag. 34, 1992e1999.

Minale, M., Worku, T., 2014. Anaerobic co-digestion of sanitary wastewater andkitchen solid waste for biogas and fertilizer production under ambient tem-perature: waste generated from condominium house. Int. J. Environ. Sci.Technol. 11, 509e516.

Molina, M.J., Soriano, M.D., Ingelmo, F., Llinares, J., 2013. Stabilization of sewagesludge and vinasse bio-wastes by vermicomposting with rabbit manure usingEisenia fetida. Bioresour. Technol. 137, 88e97.

Monroy, F., Aira, M., Domínguez, J., 2011. Epigeic earthworms increase soilarthropod populations during first steps of decomposition of organic matter.Pedobiologia 54, 93e99.

Mulbry, W., Ahn, H., 2014. Greenhouse gas emissions during composting of dairymanure: influence of the timing of pile mixing on total emissions. Biosyst. Eng.126, 117e122.

Najar, I.A., Khan, A.B., 2013. Management of fresh water weeds (macrophytes) byvermicomposting using Eisenia fetida. Environ. Sci. Pollut. Res. 20, 6406e6417.

Ndegwa, P.M., Thompson, S.A., 2001. Integrating composting and vermicompostingin the treatment and bioconversion of biosolids. Bioresour. Technol. 76,107e112.

Negi, R., Suthar, S., 2013. Vermistabilization of paper mill wastewater sludge usingEisenia fetida. Bioresour. Technol. 128, 193e198.

Oliveira, L.B., Rosa, L.P., 2003. Brazilian waste potential: energy, environmental,social and economic benefits. Energy Policy 31, 1481e1491.

Paradelo, R., Moldes, A.B., Barral, M.T., 2013. Evolution of organic matter duringmesophilic composting of lignocellulosic winery wastes. J. Env. Manag. 116,18e26.

Piotrowska-Cyplik, A., Chrzanowski, L., Cyplik, P., Dach, J., Olejnik, A., Staninska, J.,Czarny, J., Lewicki, A., Marecik, R., Powierska-Czarny, J., 2013. Composting ofoiled bleaching earth: fatty acids degradation, phytotoxicity and mutagenicitychanges. Int. Biodeterior. Biodegr. 78, 49e57.

Pozza, S.A., Penteado, C.S.G., Criscuolo, V.G., 2015. A greenhouse gas inventroy in themunicipal landfill of the City of Limeira, Brazil. Chem. Eng. Trans. 43,2083e2088.

Prakash, M., Karmegam, N., 2010. Vermistabilization of pressmud using Perionyxceylanensis Mich. Bioresour. Technol. 101, 8464e8468.

Pramanik, P., Chung, Y.R., 2011. Changes in fungal population of fly ash and vinassemixture during vermicomposting by Eudrilus eugeniae and Eisenia fetida:documentation of cellulase isozymes in vermicompost. Waste Manag. 31,1169e1175.

Qian, X., Shen, G., Wang, Z., Guo, C., Liu, Y., Lei, Z., Zhang, Z., 2014. Co-composting oflivestock manure with rice straw: characterization and establishment ofmaturity evaluation system. Waste Manag. 34, 530e535.

Quir�os, R., Villalba, G., Mu~noz, P., Font, X., Gabarrell, X., 2014. Environmental andagronomical assessment of three fertilization treatments applied in horticul-tural open field crops. J. Clean. Prod. 67, 147e158.

Raj, D., Antil, R.S., 2011. Evaluation of maturity and stability parameters of compostsprepared from agro-industrial wastes. Bioresour. Technol. 102, 2868e2873.

Rajiv, P., Rajeshwari, S., Venckatesh, R., 2014. Impact of Parthenium weeds onearthworms (Eudrilus eugeniae) during vermicomposting. Environ. Sci. Pollut.Res. 21, 12364e12371.

Rajiv, P., Rajeshwari, S., Yadav, R.H., Venckatesh, R., 2013. Vermiremediation:detoxification of parthenin toxin from Parthenium weeds. J. Hazard. Mater 262,489e495.

Ravindran, B., Contreras-Ramos, S.M., Wong, J.W.C., Selvam, A., Sekaran, G., 2014.Nutrient and enzymatic changes of hydrolysed tannery solid waste treated withepigeic earthworm Eudrilus eugeniae and phytotoxicity assessment on selectedcommercial crops. Environ. Sci. Pollut. Res. 21, 641e651.

Ravindran, B., Sekaran, G., 2010. Bacterial composting of animal fleshing generatedfrom tannery industries. Waste Manag. 30, 2622e2630.

Ravindran, B., Sravani, R., Mandal, A.B., Contreras-Ramos, S.M., Sekaran, G., 2013.Instrumental evidence for biodegradation of tannery waste during vermi-composting process using Eudrilus eugeniae. J. Therm. Anal. Calorim. 111,1675e1684.

Romero, C., Ramos, P., Costa, C., M�arquez, M.C., 2013. Raw and digested municipalwaste compost leachate as potential fertilizer: comparison with a commercialfertilizer. J. Clean. Prod. 59, 73e78.

Roy, S., Arunachalam, K., Dutta, B.K., Arunachalam, A., 2010. Effect of organicamendments of soil on growth and productivity of three common crops viz. Zeamays, Phaseolus vulgaris and Abelmoschus esculentus. Appl. Soil Ecol. 45, 78e84.

Ruggieri, L., Cadena, E., Martínez-Blanco, J., Gasol, C.M., Rieradevall, J., Gabarrell, X.,Gea, T., Sort, X., S�anchez, A., 2009. Recovery of organic waste in the Spanishwine industry. Technical, economic and environmental analyses of the com-posting process. J. Clean. Prod. 17, 830e838.

Rynk, R., 2001. Exploring the economics of on-farm composting Part II. Biocycle 42,62e70.

Saer, A., Lansing, S., Davitt, N.H., Graves, R.E., 2013. Life cycle assessment of a foodwaste composting system: environmental impact hotspots. J. Clean. Prod. 52,234e244.

Samolada, M.C., Zabaniotou, A.A., 2014. Comparative assessment of municipalsewage sludge incineration, gasification and pyrolysis for a sustainable sludge-to-energy management in Greece. Waste Manag. 34, 411e420.

S�anchez-Monedero, M.A., Serrami�a, N., Civantos, C.G., Fern�andez-Hern�andez, A.,Roig, A., 2010. Greenhouse gas emissions during composting of two-phase olivemill wastes with different agroindustrial by-products. Chemosphere 81, 18e25.

Scharff, H., 2014. Landfill reduction experience in The Netherlands. Waste Manag.34, 2218e2224.

Seo, S., Aramaki, T., Hwang, Y., Hanaki, K., 2004. Environmental impact of solidwaste treatment methods in Korea. J. Environ. Eng. 130, 81e89.

Shafawati, S.N., Siddiquee, S., 2013. Composting of oil palm fibres and Trichodermaspp. as the biological control agent: a review. Int. Biodeterior. Biodegr. 85,243e253.

Shak, K.P.Y., Wu, T.Y., Lim, S.L., Lee, C.A., 2014. Sustainable reuse of rice residues asfeedstocks in vermicomposting for organic fertilizer production. Environ. Sci.Pollut. Res. 21, 1349e1359.

Shekdar, A.V., 2009. Sustainable solid waste management: an integrated approachfor Asian countries. Waste Manag. 29, 1438e1448.

Sierra, J., Desfontaines, L., Faverial, J., Loranger-Merciris, G., Boval, M., 2013. Com-posting and vermicomposting of cattle manure and greenwastes under tropicalconditions: carbon and nutrient balances and end-product quality. Soil Res. 51,142e151.

Sim, E.Y.S., Wu, T.Y., 2010. The potential reuse of biodegradable municipal solidwastes (MSW) as feedstocks in vermicomposting. J. Sci. Food Agric. 90,2153e2162.

Simujide, H., Aorigele, C., Wang, C.J., Lina, M., Manda, B., 2013. Microbial activitiesduring mesophilic composting of manure and effect of calcium cyanamideaddition. Int. Biodeterior. Biodegr. 83, 139e144.

Singh, A., Jain, A., Sarma, B.K., Abhilash, P.C., Singh, H.B., 2013. Solid waste man-agement of temple floral offerings by vermicomposting using Eisenia fetida.Waste Manag. 33, 1113e1118.

Singh, D., Suthar, S., 2012a. Vermicomposting of herbal pharmaceutical industrysolid wastes. Ecol. Eng. 39, 1e6.

Singh, D., Suthar, S., 2012b. Vermicomposting of herbal pharmaceutical industrywaste: earthworm growth, plant-available nutrient and microbial quality of endmaterials. Bioresour. Technol. 112, 179e185.

Singh, J., Kalamdhad, A.S., 2014. Potential for composting of green phumdi biomassof Loktak lake. Ecol. Eng. 67, 119e126.

Singh, J., Kalamdhad, A.S., 2013a. Effect of Eisenia fetida on speciation ofheavy metals during vermicomposting of water hyacinth. Ecol. Eng. 60,214e223.

Singh, J., Kalamdhad, A.S., 2013b. Effects of lime on bioavailability and leachabilityof heavy metals during agitated pile composting of water hyacinth. Bioresour.Technol. 138, 148e155.

Singh, J., Kalamdhad, A.S., 2013c. Reduction of bioavailability and leachability ofheavy metals during vermicomposting of water hyacinth. Environ. Sci. Pollut.Res. 20, 8974e8985.

Singh, J., Kalamdhad, A.S., 2012. Concentration and speciation of heavy metalsduring water hyacinth composting. Bioresour. Technol. 124, 169e179.

Singh, J., Kaur, A., Vig, A.P., Rup, P.J., 2010. Role of Eisenia fetida in rapid recycling ofnutrients from bio sludge of beverage industry. Ecotoxicol. Env. Saf. 73,430e435.

Singh, R.P., Singh, P., Araujo, A.S.F., Ibrahim, M.H., Sulaiman, O., 2011. Managementof urban solid waste: vermicomposting a sustainable option. Resour. Conserv.Recycl. 55, 719e729.

Song, Q., Li, J., Zeng, X., 2015. Minimizing the increasing solid waste through zerowaste strategy. J. Clean. Prod. 104, 199e210.

Song, X., Liu, M., Wu, D., Qi, L., Ye, C., Jiao, J., Hu, F., 2014. Heavy metal and nutrientchanges during vermicomposting animal manure spiked with mushroom res-idues. Waste Manag. 34, 1977e1983.

Soobhany, N., Mohee, R., Garg, V.K., 2015. Comparative assessment of heavy metalcontent during the composting and vermicomposting of municipal solid wasteemploying Eudrilus eugeniae. Waste Manag. 39, 130e145.

Subhash Kumar, M., Rajiv, P., Rajeshwari, S., Venckatesh, R., 2015. Spectroscopicanalysis of vermicompost for determination of nutritional quality. Spectrochim.Acta Pt. A-Mol. Biomol. Spectr. 135, 252e255.

Subramanian, S., Sivarajan, M., Saravanapriya, S., 2010. Chemical changes duringvermicomposting of sago industry waste. J. Hazard. Mater 179, 318e322.

Suthar, S., 2010. Potential of domestic biogas digester slurry in vermitechnology.Bioresour. Technol. 101, 5419e5425.

Suthar, S., 2011. Production of earthworm Allolobophora parva (Eisen) in cattledung. Ecol. Eng. 37, 644e647.

Suthar, S., 2012. Earthworm production in cattle dung during vermicompostingsystem under different stocking density loads. Environ. Sci. Pollut. Res. 19,748e755.

Suthar, S., Mutiyar, P.K., Singh, S., 2012. Vermicomposting of milk processing in-dustry sludge spiked with plant wastes. Bioresour. Technol. 116, 214e219.

Suthar, S., 2014. Toxicity of methyl parathion on growth and reproduction of threeecologically different tropical earthworms. Int. J. Environ. Sci. Technol. 11,191e198.

Suthar, S., Gairola, S., 2014. Nutrient recovery from urban forest leaf litter wastesolids using Eisenia fetida. Ecol. Eng. 71, 660e666.

Suthar, S., Sharma, P., 2013. Vermicomposting of toxic weed e Lantana camarabiomass: chemical and microbial properties changes and assessment of toxicityof end product using seed bioassay. Ecotoxicol. Environ. Saf. 95, 179e187.

Page 17: artículo de residuos solido

S.L. Lim et al. / Journal of Cleaner Production 111 (2016) 262e278278

Suthar, S., Sajwan, P., Kumar, K., 2014. Vermiremediation of heavy metals inwastewater sludge from paper and pulp industry using earthworm Eiseniafetida. Ecotoxicol. Environ. Saf. 109, 177e184.

Tan, S.T., Hashim, H., Lim, J.S., Ho, W.S., Lee, C.T., Yan, J., 2014. Energy and emissionsbenefits of renewable energy derived from municipal solid waste: analysis of alow carbon scenario in Malaysia. Appl. Energy 136, 797e804.

Tang, Z., Yu, G., Liu, D., Xu, D., Shen, Q., 2011. Different analysis techniques forfluorescence excitation-emission matrix spectroscopy to assess compostmaturity. Chemosphere 82, 1202e1208.

Tian, Y., Chen, L., Gao, L., Michael Jr., F.C., Keener, H.M., Klingman, M., Dick, W.A.,2012. Composting of waste paint sludge containing melamine resin and thecompost's effect on vegetable growth and soil water quality. J. Hazard. Mater243, 28e36.

Tortosa, G., Alburquerque, J.A., Ait-Baddi, G., Cegarra, J., 2012. The production ofcommercial organic amendments and fertilisers by composting of two-phaseolive mill waste (“alperujo”). J. Clean. Prod. 26, 48e55.

Tsutsui, H., Fujiwara, T., Matsukawa, K., Funamizu, N., 2013. Nitrous oxide emissionmechanisms during intermittently aerated composting of cattle manure. Bio-resour. Technol. 141, 205e211.

United Nations Environment Programme (UNEP), 2015. Cleaner and Safer Produc-tion. www.unep.org/resourceefficiency/Business/CleanerSaferProduction/tabid/55543/Default.aspx (assessed 15.04.15.).

United Nations Environment Programme (UNEP), 2011. Towards a Green Economy:Pathways to Sustainable Development and Poverty Eradication. www.unep.org/greeneconomy (assessed 15.04.15.).

Unuofin, F.O., Mnkeni, P.N.S., 2014. Optimization of Eisenia fetida stocking densityfor the bioconversion of rock phosphate enriched cow dung-waste papermixtures. Waste Manag. 34, 2000e2006.

V�azquez, M.A., de la Varga, D., Plana, R., Soto, M., 2015. Integrating liquid fraction ofpig manure in the composting process for nutrient recovery and water re-use.J. Clean. Prod. 104, 80e89.

Velasco-Velasco, J., Parkinson, R., Kuri, V., 2011. Ammonia emissions during ver-micomposting of sheep manure. Bioresour. Technol. 102, 10959e10964.

Vig, A.P., Singh, J., Wani, S.H., Dhaliwal, S.S., 2011. Vermicomposting of tannerysludge mixed with cattle dung into valuable manure using Eisenia fetida(Savigny). Bioresour. Technol. 102, 7941e7945.

Wang, J., Hu, Z., Xu, X., Jiang, X., Zheng, B., Liu, X., Pan, X., Kardol, P., 2014a. Emis-sions of ammonia and greenhouse gases during combined pre-composting andvermicomposting of duck manure. Waste Manag. 34, 1546e1552.

Wang, Y.Q., Zhang, J.L., Schuchardt, F., Wang, Y., 2014b. Degradation of morphine inopium poppy processing waste composting. Bioresour. Technol. 168, 235e239.

Wang, J.J., Sun, X.J., Zhou, H.T., Zhang, J., 2013a. Influences of different aerationpatterns on the composting of green waste and rice straw with sewage sludges.Appl. Mech. Mater 295e298, 1725e1728.

Wang, L., Zhang, Y., Lian, J., Chao, J., Gao, Y., Yang, F., Zhang, L., 2013b. Impact of flyash and phosphatic rock on metal stabilization and bioavailability duringsewage sludge vermicomposting. Bioresour. Technol. 136, 281e287.

Wang, L., Zheng, Z., Zhang, Y., Chao, J., Gao, Y., Luo, X., Zhang, J., 2013c. Bio-stabilization enhancement of heavy metals during the vermiremediation ofsewage sludge with passivant. J. Hazard. Mater 244e245, 1e9.

Watteau, F., Villemin, G., 2011. Characterization of organic matter microstructuredynamics during co-composting of sewage sludge, barks and green waste.Bioresour. Technol. 102, 9313e9317.

Wu, X., Wei, Y., Zheng, J., Zhao, X., Zhong, W., 2011. The behavior of tetracyclines andtheir degradation products during swine manure composting. Bioresour.Technol. 102, 5924e5931.

Wu, T.Y., Lim, S.L., Lim, P.N., Shak, K.P.Y., 2014. Biotransformation of biodegradablesolid wastes into organic fertilizers using composting or/and vermicomposting.Chem. Eng. Trans. 39, 1579e1584.

Xing, M., Li, X., Yang, J., Huang, Z., Lu, Y., 2012. Changes in the chemical charac-teristics of water-extracted organic matter from vermicomposting of sewagesludge and cow dung. J. Hazard. Mater 205e206, 24e31.

Yadav, A., Garg, V.K., 2011a. Industrial wastes and sludges management by vermi-composting. Rev. Environ. Sci. Biotechnol. 10, 243e276.

Yadav, A., Garg, V.K., 2011b. Recycling of organic waste by employing Eisenia fetida.Bioresour. Technol. 102, 2874e2880.

Yadav, A., Garg, V.K., 2011c. Vermicomposting-an effective tool for the managementof invasive weed Parthenium hysterophorus. Bioresour. Technol. 102,5891e5895.

Yadav, K.D., Tare, V., Ahammed, M.M., 2012. Integrated composting-vermicomposting process for stabilization of human faecal slurry. Ecol. Eng.47, 24e29.

Yadav, K.D., Tare, V., Ahammed, M.M., 2010. Vermicomposting of source-separatedhuman faeces for nutrient recycling. Waste. Manag. 30, 50e56.

Yahya, A., Sye, C.P., Ishola, T.A., Suryanto, H., 2010. Effect of adding palm oil milldecanter cake slurry with regular turning operation on the composting processand quality of compost from oil palm empty fruit bunches. Bioresour. Technol.101, 8736e8741.

Yang, J., Lv, B., Zhang, J., Xing, M., 2014. Insight into the roles of earthworm invermicomposting of sewage sludge by determining the water-extracts throughchemical and spectroscopic methods. Bioresour. Technol. 154, 94e100.

Yang, Z., Zhou, X., Xu, L., 2015. Eco-efficiency optimization for municipal solid wastemanagement. J. Clean. Prod. 104, 242e249.

Yay, A.S.E., 2015. Application of life cycle assessment (LCA) for municipal solid wastemanagement: a case study of Sakarya. J. Clean. Prod. 94, 284e293.

Yoshizaki, T., Shirai, Y., Hassan, M.A., Baharuddin, A.S., Abdullah, N.M.R.,Sulaiman, A., Busu, Z., 2012. Economic analysis of biogas and compost projectsin a palm oil mill with clean development mechanism in Malaysia. Environ.Dev. Sustain 14, 1065e1079.

Yoshizaki, T., Shirai, Y., Hassan, M.A., Baharuddin, A.S., Abdullah, N.M.R.,Sulaiman, A., Busu, Z., 2013. Improved economic viability of integrated biogasenergy and compost production for sustainable palm oil management. J. Clean.Prod. 44, 1e7.

Zainudin, M.H.M., Hassan, M.A., Tokura, M., Shirai, Y., 2013. Indigenous cellulolyticand hemicellulolytic bacteria enhanced rapid co-composting of lignocelluloseoil palm empty fruit bunch with palm oil mill effluent anaerobic sludge. Bio-resour. Technol. 147, 632e635.

Zaman, A.U., 2013. Identification of waste management development drivers andpotential emerging waste treatment technologies. Int. J. Environ. Sci. Technol.10, 455e464.

Zambrano, M., Pichún, C., Alvear, M., Villarroel, M., Vel�asquez, I., Baeza, J., Vidal, G.,2010. Green liquor dregs effect on Kraft mill secondary sludge composting.Bioresour. Technol. 101, 1028e1035.

Z�avodsk�a, A., Bene�sov�a, L., Smyth, B., Morrissey, A.J., 2014. A comparison ofbiodegradable municipal waste (BMW) management strategies in Ireland andthe Czech Republic and the lessons learned. Resour. Conserv. Recycl 92,136e144.

Zhu, F.X., Wang, W.P., Hong, C.L., Feng, M.G., Xue, Z.Y., Chen, X.Y., Yao, Y.L., Yu, M.,2012. Rapid production of maggots as feed supplement and organic fertilizerby the two-stage composting of pig manure. Bioresour. Technol. 116,485e491.

Zhu, W., Yao, W., Zhang, Z., Wu, Y., 2014. Heavy metal behavior and dissolvedorganic matter (DOM) characterization of vermicomposted pig manure amen-ded with rice straw. Environ. Sci. Pollut. Res. 21, 12684e12692.

Zuriaga-Agustí, E., Galiana-Aleixandre, M.V., Bes-Pi�a, A., Mendoza-Roca, J.A.,Risue~no-Puchades, V., Segarra, V., 2015. Pollution reduction in and eco-friendlychrome-free tanning and evaluation of the biodegradation by composting of thetanned leather wastes. J. Clean. Prod. 87, 874e881.