azo dye- past present future

Azo dyes: past, present and the future

Amit Bafana, Sivanesan Saravana Devi, and Tapan Chakrabarti

Abstract: Dyes have a long history and constitute an important component in our daily lives. The dye industry began by us-ing natural plant and insect sources, and then rapidly turned to synthetic manufacturing processes. Unfortunately, several ofthe synthetic dyes, especially azo dyes, have been found to be toxic and mutagenic, and are banned throughout the world.However, because of their low cost and other desirable properties, the use and manufacture of azo dyes continues even to-day. Removal and treatment of azo dyes from wastewater presents a very special challenge. Since azo dyes are recalcitrantto the conventional aerobic biological treatment, and physical/chemical treatment processes are neither ecofriendly nor eco-nomical, innovative remediation approaches need to be explored. In the current scenario, a combination of biological andadvanced oxidation processes seem to be the most desired solution. Moreover, mechanistic studies of the pathways and en-zymes involved in dye degradation and detoxification need to be undertaken for process optimization. This paper criticallyand comprehensively reviews recent research advances and the knowledge-base of the previously mentioned areas, includinghistory and chemistry of dyes, mechanistic studies on their persistence, ecotoxicity, and carcinogenicity, and potential reme-diation methods. Particular emphasis has been given towards critical evaluation of the existing dye wastewater treatmentmethods and their full-scale applications; based on which recommendations have been made for future developments of thetreatment technologies and their assessment methods. In the Authors' opinion, a more holistic and large-scale approach is re-quired to tackle the chronic problem of dye pollution.

Key words: persistence, carcinogenicity, toxicity, legislation, treatment.

Résumé : Les teintures ont une longue histoire et constituent une composante importante de notre vie quotidienne. L'indus-trie des teintures a commencé avec des sources naturelles provenant de plantes et d'insectes, pour rapidement se tourner versdes procédés de fabrication industriels. Malheureusement, on a constaté que plusieurs des teintures synthétiques, surtout detype azoïque, sont toxiques et mutagènes, et défendues partout au monde. Cependant, dû à leur faible coût et autres proprié-tés désirables, l'utilisation et la production des teintures azoïques se poursuivent, même aujourd'hui. La récupération et letraitement des teintures azoïques des eaux usées présentent un défi très spécial. Puisse que les teintures azoïques résistent autraitement conventionnel biologique aérobie, et que les procédés physico-chimiques ne sont pas respectueux de l'environne-ment, on doit explorer des approches innovatrices de remédiation. Selon le scénario actuel, une combinaison de procédésbiologiques et d'oxydations avancés semble constituer la solution la plus souhaitable. De plus, afin d'optimiser les procédés,on doit entreprendre des études mécanistiques sur les enzymes et les sentiers métaboliques impliqués dans la dégradation etla détoxification des teintures. Les auteurs revoient de façon critique et globale les récentes avancées de la recherche et labase de connaissances sur les sujets discutés plus haut, incluant l'histoire et le chimie des teintures, les études mécanistiquessur leurs persistances, l'écotoxicité et la cancérogénicité, ainsi que sur les méthodes potentielles de remédiation. On met unaccent particulier sur les évaluations critiques des méthodes actuelles de traitement des teintures dans les eaux usées et leursapplications à grande échelle, en se basant sur les recommandations ayant été faites pour le développement futur des techno-logies de traitement et leurs méthodes d'évaluation. Selon les auteurs, on doit utiliser une approche plus holistique et àgrande échelle afin de cerner le problème chronique de la pollution par les teintures.

[Traduit par la Rédaction]

Introduction

Dyes may be defined as substances which, when applied toa substrate, impart colour to the substrate by a process that,at least temporarily, destroys any crystal structure of the col-oured substances. They adhere on compatible surfaces byphysical adsorption, mechanical retention, formation of cova-lent bond or of complexes with salts or metals, or by solution(Kirk-Othmer 2004). The colour of dyes depends on their

ability to absorb light in the visible range of electromagneticradiation (400–700 nm). According to Witt theory, a col-oured dye must have a chromophore group and an auxo-chrome group. Chromophores impart colour to the dyebecause they are capable of absorbing light in the visible re-gion (e.g., nitro, azo, quinoid groups), while auxochromesdeepen the colour when introduced into a coloured molecule.Witt theory has now been replaced by the modern electronictheory. According to this theory, colour is caused by the ex-

Received 12 September 2010. Accepted 24 November 2010. Published at www.nrcresearchpress.com/er on 28 September 2011.

A. Bafana. Biotechnology Division, Institute of Himalayan Bioresource Technology (IHBT), Council of Scientific and Industrial Research(CSIR), Palampur-176061.S.S. Devi and T. Chakrabarti. Sivanesan Saravana Devi, and Tapan Chakrabarti: National Environmental Engineering Research Institute(NEERI), Council of Scientific and Industrial Research (CSIR), Nagpur, India-440020.

Corrsponding author: Amit Bafana (e-mail: [email protected]).

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Environ. Rev. 19: 350–370 (2011) doi:10.1139/A11-018 Published by NRC Research Press

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citation of valance p electrons by visible light (Murrell1973). Dyes are widely used in textile dyeing, paper printing,colour photography, pharmaceutical, food, cosmetics, andother industries.Until the middle of 19th century, all dyes came from natu-

ral sources. Most of these were vegetable extracts and a fewwere animal products. The range of colours was limited aswas the utility of dyes. The history of natural dyes is veryinteresting. The earliest written record of the use of naturaldyes was found in China dated 2600 BC. Egyptian mummieshave been found wrapped in cloth dyed from the madderplant. Alexander the Great is thought to have deceived thePersians into thinking that his army was wounded, by sprin-kling his soldiers with a red dye, probably madder juice,which contains the dye alizarin (Garfield 2002).The limited range of natural dyes prompted chemists to

synthesize dyes with new colours. In 1771, Woulfe preparedpicric acid by the action of nitric acid on indigo and showedthat it dyed silk in bright yellow shades. However, the syn-thetic dye industry began only in 1856 when William HenryPerkin prepared mauve from coal-tar chemicals. He built afactory near London to supply the world's first synthetic dye.The late 1870s saw another dramatic development when OttoWitt synthesized an azo dye, which was marketed as LondonYellow. Although England had the early lead, Germany soonbecame the leading global supplier of a rainbow of brilliantcolours. In the early 1900s, about 85% of world dye require-ments were manufactured in Germany, with other Europeancountries (Switzerland, England, and France) accounting for afurther 10%. Dye manufacturing in the US was hampered byseveral reasons such as the Civil War, limited availability ofintermediates derived from coal tar, and tariff regulations thatfavoured imports. When World War I erupted in 1914, theGerman dye factories had to switch to making explosives,which resulted in a dye famine that quickly drove the pricesup. Dye manufacture suddenly became an attractive invest-ment and many large and small dye manufacturing companiesproliferated in several countries (Morris and Travis 1992).Currently, the world market of dyes and pigments is esti-

mated to be around 1.3 million tons, valued at US$16 billion.European countries, such as Italy, France, Spain, Germany,and England, and Asian countries, such as China, Taiwan,India, Japan, Korea, and Pakistan, represent the major dye-stuff producing countries. In terms of market share, Europeis the leading producer with 40% of the global dyestuff pro-duction, because of its commitment towards specialty prod-ucts. However, the industry has slowly shifted towards Asiaover the past years because of the much lower costs of pro-duction in this region. Chinese and Indian shares in the worlddyestuff market have been estimated to be 25% and 6%, re-spectively (Iris 2008).Dye industry in India grew very rapidly following the

country's independence. Atul Products Ltd. was formed inGujarat in 1949, and created joint enterprises with ICI (AticIndustries) in 1955, and CIBA (Cibatui) in 1960. Indian Dye-stuffs Industries, situated in Bombay is the second major pro-ducer, and was formed in the 1950s (Morris and Travis1992). The Indian market for dyes is estimated at US$768million and has been growing at 2%–3%. Textile industry ac-counts for the largest consumption of dyestuffs (nearly 80%)in India. With excess capacity in the domestic market, the

emphasis is on exports, which grew from US$111 million in1990–91 to US$489 million in 1997–98 (Iris 2008; Morrisand Travis 1992).

Types of dyesNatural dyes were the first dyes used by humans. How-

ever, with the introduction of their synthetic counterpart, theiruse has almost been discontinued. Synthetic dyes are basedmainly on aniline, the only source of which was originallycoal tar; hence the name coal-tar dyes. In terms of chemicalstructure, dyes may either be inorganic or organic com-pounds. Sometimes pigments are differentiated from dyes,although the former are currently considered to be a groupof dyes. Pigments are practically insoluble in the media inwhich they are applied. They have to be attached to a sub-strate by means of additional compounds; for example, poly-mers in paints. Dyes are typically classified in two ways:chemical composition and application class or end use (Gar-field 2002). Based on the application method, dyes can bedivided into acid, azoic, basic, direct, disperse, mordant, re-active, sulphur, and vat dyes. Alternatively, dyes may bechemically divided into azo, nitro, nitroso, diarylmethane, tri-arylmethane, xanthene, anthraquinoid, acridine, cyanine,quinone-imine, pthalocyanine, and thiazole dyes. Unfortu-nately, there is no systematic nomenclature of dyes. Hence, asingle dye may have many different names. For example,Rose Red dye has three names viz. Rosaniline, Magenta, andFuchsine. To avoid this difficulty, the Society of Dyers andColourists and the American Association of Textile Chemistsand Colorists have compiled a Colour Index in which eachdye is assigned its individual CI number (Colour Index2001).

Azo dyesWith respect to both number and production volume, azo

dyes are the largest group of colourants constituting 70% ofall organic dyes produced in the world (Carliell et al. 1998).The success of azo dyes is due to the simple synthetic proce-dures involved, their great structural diversity, high molar ex-tinction coefficient, and medium-to-high fastness propertieswith respect to both light and wetness. They are used in sev-eral applications such as dying of natural and synthetic mate-rials, medicine, ink, cosmetics, food, and paints.The first azo dyes were manufactured by Mene in 1861

(Aniline Yellow) and by Martius in 1863 (Bismarck Brown;Fig. 1). The first dye production by diazotization and azocoupling, as carried out in the modern industry, was per-formed in 1875 by Caro and Witt at BASF (Badische Anilin& Soda-Fabrik), Germany (Morris and Travis 1992). Due tothe complexity of the chemical names, azo colourants areonly rarely referred to using the IUPAC (International Unionof Pure and Applied Chemistry) or CAS (Chemical AbstractsService) nomenclatures. Technical literature has adopted theclassification of azo colourants either by the chemical consti-tution or by the colour. In the Colour Index system (ColourIndex 2001), azo colourants are provided with numbers rang-ing from 11000 to 39999 in correspondence with the chemi-cal class (Table 1).

Persistence of azo dyesDyes must have a high degree of chemical and photolytic

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stability to be useful. Subsequently, photolysis is not consid-ered to be an important degradation pathway for azo dyes.Stability against microbial attack is also a required feature ofazo dyes, because it may prolong the lifetime of the products.Pagga and Brown (1986) tested 87 dyestuffs in short-termaerobic biodegradation tests and confirmed that azo dyes areunlikely to show any significant biodegradation in such tests.The recalcitrance of azo dyes has been attributed to the pres-ence of sulphonate groups and azo bonds, two features gener-ally considered as xenobiotic (Fig. 1). Kulla et al. (1983)showed that substitution with sulphonate group interferedwith the degradation of Orange I and Orange II azo dyes bya Pseudomonas strain that was otherwise capable of mineral-izing these dyes. Similarly, the electron-withdrawal characterof azo groups generates electron deficiency and makes azocompounds less susceptible to oxidative catabolism. Indeedmost of the azo dyes are metabolized under anaerobic condi-tions. Wuhrmann et al. (1980) studied decolourization of dif-ferent textile dyes by several microorganisms and found that

decolourization occurred exclusively in anaerobic conditions.In a study, Bafana et al. (2007) utilized a Pseudomonas strainwith high respiration rate, which lowered the oxidation/reduc-tion potential of the medium, to promote anaerobic dye de-colourization by another culture. Liu et al. (2007) alsoshowed that photosynthetic bacteria like Rhodobacter sphaer-oides and Rhodopseudomonas palustris, and recombinant Es-cherichia coli strain over-expressing azoreductase coulddecolourize sulphonated azo dyes only under anaerobic con-ditions. Additionally, substitution with electron-withdrawinggroups enhances the electrophilicity and, hence, the reductivemetabolism of azo dyes (Hsueh et al. 2009). Thus, azo dyeswith electron-withdrawing groups (e.g., sulphonate group inReactive Black 5) are more easily decolourized than thosewith electron-releasing groups (e.g., –NH-triazine in ReactiveBlue 171). Further, the isomers with electron-withdrawinggroups at ortho position relative to the azo bond, are moreslowly decolourized as compared to those with electron-with-drawing group at para position. This is probably because ofsteric hindrance by the substituent near the azo linkage.Reduction of azo bond frequently releases aromatic amines

from azo dyes, which resist further degradation under anaero-bic condition (Fig. 2; Pinheiro et al. 2004). In a study, aro-matic amine metabolites of five azo dyes were found to bepersistent under anaerobic condition, even after long-term in-cubations (Işik and Sponza 2007). These amines have beenreported to undergo slow degradation under aerobic condi-

Fig. 1. Structure of certain representative azo dyes (a) Aniline Yellow, (b) Bismarck Brown, (c) Direct Black 38, and (d) Direct Red 28(Congo Red).

Table 1. Classification of azo dyes in Colour Index.

Chemical Class CI no.Mono azo 11000-19999Bis-azo 20000-29999Tris-azo 30000-34999Polyazo 35000-36999Azoic 37000-39999

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tions only. It has been shown that aromatic amines like sul-phanilic acid and aniline can be mineralized aerobically byany inoculum with significant microbiological diversity, evenwith the domestic effluent (Carvalho et al. 2008). Thus, com-plete mineralization of azo dyes generally requires sequentialanaerobic–aerobic conditions, which further adds to their re-calcitrance.

Toxicity and carcinogenicity of azo dyesThe acute toxicity of azo dyes, as defined by the European

Union criteria for classification of dangerous substances, israther low. The majority of azo dyes show LD50 values be-tween 250–2000 mg/kg body weight (Clarke and Anliker1980). Azo dyes can also cause a variety of other chronic ef-fects. Reactive Brilliant Red can inhibit functioning of humanserum albumin by binding to it and causing a conformationalchange or even precipitation (Li et al. 2010a). Sudan Reddyes are essentially hydrophobic, but contain azo and hy-droxyl groups, which make them amphiphilic. These dyeshave been shown to get sequestered in the membrane phos-pholipid bilayer of E. coli, which may result in toxic effectslike membrane blocking and membrane expansion (Li et al.2007). Several dyes have been shown to cause contact der-matitis in the local lymph node assays (Ahuja et al. 2010).The toxicity is generally not because of the dye itself, but

because of its degradation products. The azo linkage is themost labile portion of an azo dye molecule and may easilyundergo breakdown by an enzyme named azoreductase foundin various microorganisms and in all tested mammals, includ-

ing humans (Fig. 2; Bafana and Chakrabarti 2008). This re-sults in the release of constituent aromatic amines, many ofwhich show very high level of acute and chronic toxicity, andcarcinogenicity (Table 2; IARC 1987). Acid Violet 7 can in-duce chromosome aberrations, lipid peroxidation, and acetyl-cholinesterase inhibitory effect upon intraperitoneal injectionin mice. Ben Mansour et al. (2010) showed that amines (4'-aminoacetanilide and 5-acetamido-2-amino-1-hydroxy-3,6-naphtalene disulphonic acid) resulting from azoreduction ofthe dye were responsible for the toxicity. Humans are exposedto azo dye-derived toxic aromatic amines in a variety of ways.Azo dyes present in food products or clothes can be metabo-lized by intestinal or skin microbiota, leading to exposure totoxic amines. Stingley et al. (2009) showed that majority ofthe skin bacteria could reduce Methyl Red and Orange IIdyes to release aromatic amines. Similarly, Xu et al. (2009)demonstrated reduction of Sudan azo dyes by the human co-lon bacteria. The toxic aromatic amines may also be presentin dye preparations as residual impurities. The InternationalAgency for Research on Cancer (IARC 1987) reported pres-ence of 4-aminobiphenyl and 2,4-diaminoazobenzene as im-purities in Direct Black 38 dye. A survey of textile productsin Japan revealed presence of aromatic amines, including ben-zidine, above the regulatory limits in several fabrics (Kawa-kami et al. 2010). Aromatic amines have also been shown tomigrate from dyed food packaging materials into food prod-ucts (Kolado and Balcerzak 2009). A study in Brazil showedmutagenic activity in treated drinking water, which was tracedto contamination from the effluents of a textile azo dye proc-

Fig. 2. Biological dye degradation. (a) Aerobic dye decolourization by peroxidase and laccase. Enzymes and their substrates are colour-coded.Degradation pathway of Disperse Orange 3 by Pleurotus ostreatus (adapted from Zhao et al. 2006) is shown as an example; (b) a typicalazoreductase-catalyzed reaction; (c) anaerobic decolourization of azo dyes. LiP, lignin peroxidase; MnP, Mn peroxidase; VA, veratryl alcohol;ABTS, 2,2’-azinobis-(3-ethylbenzthiazoline-6-sulphonate); AQDS, anthraquinone-2,6-disulphonate.

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Table 2. Aromatic amines, known or suspected of being human carcinogens, that are banned by European Union.

Amine CAS No.a IARC classificationb Structure4-aminodiphenyl 92-67-1 Group 1

benzidine 92-87-5 Group 1

4-chloro-o-toluidine 95-69-2 Group 2A

2-naphthylamine 91-59-8 Group 1

4-amino-2',3-dimethylazobenzene 97-56-3 Group 2B

2-amino-4-nitrotoluene 99-55-8 Group 3

4-chloroaniline 106-47-8 Group 2B

2,4-diaminoanisole 615-05-4 Group 2B

4,4'-diaminodiphenylmethane 101-77-9 Group 2B

3,3'-dichlorobenzidine 91-94-1 Group 2B

3,3'-dimethoxybenzidine 119-90-4 Group 2B

3,3'-dimethylbenzidine 119-93-7 Group 2B

3,3'-dimethyl-4,4'diaminodiphenylmethane 838-88-0 Group 2B

4-cresidine 120-71-8 Group 2B

4,4'-methylene-bis-(2-chloroaniline) 101-14-4 Group 2A

4,4'-oxydianiline 101-80-4 Group 2B

4,4'-thiodianiline 139-65-1 Group 2B

2-aminotoluene 95-53-4 Group 2B

2,4-diaminotoluene 95-80-7 Group 2B



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essing plant (Alves de Lima et al. 2007). The aromatic aminescan get absorbed into the body through lungs, gastrointestinaltract or skin, and are excreted in the urine (ECDIN 1993).Dewan et al. (1988) demonstrated presence of benzidine andits metabolites in the urine of workers exposed to DirectBlack 38 dye. Polarity of azo dyes influences the metabolismand consequently the excretion. Sulphonation of azo dyes ap-pears to decrease toxicity by enhancing urinary excretion ofthe dye and its metabolites (Chung and Cerniglia 1992).Hence, sulphonated dyes, such as amaranth, sunset yellow,and tartrazine, are permitted worldwide for use in food, cos-metics, and drugs (Poul et al. 2009).About 2000 azo dyes have so far been synthesized and of

these more than 500 are based on carcinogenic amines (Table2), benzidine itself constituting more than 250 azo dyes (Plat-zek 1995). There is sufficient evidence of carcinogenicity ofbenzidine, its congeners (e.g., o-dianisidine), and other aro-matic amines (IARC 1987). A long-term epidemiologicalstudy in the US showed that workers exposed to benzidineand 3,3-dichlorobenzidine had increased risk of bladder canceralong with cancers of the brain, central nervous system, andtongue (Brown and Schoenberg 2008). The evidence forbenzidine-induced cancer in sites other than the bladder, how-ever, is not as strong as for bladder cancer. Some studies haveshown benzidine-induced carcinomas in other organs such asliver, biliary system, and sebaceous glands in mice, rats, andhamsters (Kellner et al. 1973). The aromatic amines cause sev-eral adverse effects in the cells that may lead to cancer. Analy-sis of serum from 331 benzidine-exposed workers in Chinarevealed that incidences of p53 mutations increased with ben-zidine exposure (Xiang et al. 2007). A 10-fold increase in thenumber of peripheral lymphocytes displaying chromosomalaberrations was observed in workers exposed to benzidine andbenzidine-based dyes at a manufacturing plant in Bulgaria(Mirkova and Lalchev 1990). Bone marrow micronuclei (Mir-kova 1990), sister chromatid exchanges, DNA strand breaks(Das et al. 1994), unscheduled DNA synthesis (Ashby et al.1990) and cell transformation were induced by benzidine inthe cells of rodents treated in vivo or in vitro. Several aromaticamines have been shown to induce frame-shift, base-pair andcomplex mutations in Salmonella typhimurium in the Amestest (Claxton et al. 2001). Aromatic amines have also been re-ported to exert high level of acute and chronic toxicity. Symp-toms include allergy, ataxia, anaemia, methemoglobinaemia,

reticulocytosis, hematuria, kidney and liver damage, and poi-soning causing fatality (Patnaik 2007). The acute oral LD50 ofbenzidine is 309 and 214 mg/kg in rat and mouse, respectively(Haley 1975). Pathak and Khuda-Bukhsh (2007) showed thatchronic feeding of p-dimethylaminoazobenzene in mice in-duced considerable toxicity and palpable hepatocellular inju-ries along with carcinogenetic in liver. Similarly, treatment ofMardin–Darby canine kidney cells with p-phenylenediamineinduced apoptotic cell death (Chen et al. 2006). Benzidinewas found to induce contact dermatitis in several patients in astudy (Grimalt and Romaguera 1981).Since metabolism of azo dyes to release the constituent

carcinogenic amines is a generalized phenomenon in all thespecies studied including humans, such dyes are also consid-ered as carcinogens (IARC 1987). Thousands of workers in-volved in the production of dyes, textile, paper, and leathergoods are potentially exposed to carcinogenic dyes. An epi-demiologic study by Yoshida et al. (1971) reported an associ-ation between employment in the dye industry and urinarybladder cancer. In an Italian study of workers exposed tobenzidine-based dyes, there was 30.4-fold increase in thecases of bladder cancer. There was also smaller increase inthe upper digestive and respiratory tract cancers (Piolatto etal. 1991). Carcinogenicity of many of the azo dyes has beendemonstrated experimentally. In a 13-week subchronic feed-ing study, Direct Black 38 induced both hepatic neoplasticnodules and hepatocellular carcinomas in male and femaleFischer 344 rats within 5 weeks (NCI 1978). This is reportedto be the shortest latency period for tumor development byany chemical studied in the NCI (National Cancer Institute)bioassay program. Direct Black 38 was originally listed as“reasonably anticipated to be human carcinogen” in the ThirdAnnual Report on Carcinogens in 1983, and then changed to“known to be human carcinogen” in the Ninth Edition in2000 (NTP 2000). Many azo dyes are also mutagenic in theAmes S. typhimurium test. While some dyes, such as DirectBlue 15, are directly mutagenic, others require metabolic ac-tivation through sequential reduction and oxidation (Reid etal. 1984). Reductive or partially reductive conditions are re-quired initially to reduce the azo dyes and release carcino-genic aromatic amines. Most investigators have employed asuspension of rat coecal flora, or hamster S9 mix supple-mented with flavin mononucleotide for this (Prival et al.1984). The second step of activation generally involves oxi-

Table 2 (concluded).

Amine CAS No.a IARC classificationb Structure

2,4,5-trimethylaniline 137-17-7 Group 3

2-methoxyaniline 90-04-0 Group 2B

4-aminoazobenzene 60-09-3 Group 2B

aCAS, Chemical Abstracts ServicebIARC, International Agency for Research on Cancer, France-classification of agents based on carcinogenic hazards to humans: Group 1: carcinogenic;

2A: probably carcinogenic; 2B: possibly carcinogenic; 3: not classifiable as to its carcinogenicity; 4: probably not carcinogenic.

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dative metabolism of the aromatic amines by Aroclor-inducedrat liver S9 or hamster liver S9. Reid et al. (1984) used thissequential reduction and oxidation protocol to reveal signifi-cant mutagenicity in several azo dyes, which were otherwisenon-mutagenic or less mutagenic. Mutagenicity of benzidine-based azo dyes has been correlated with their structures.Methylation, methoxylation, halogenation, or substitution ofan acetyl group for hydrogen in the amino group do not af-fect mutagenicity, but complexation with Cu ion diminishesmutagenicity. Also, the mutagenicity of benzidine or its de-rivatives is decreased in the form of a hydrochloride salt(Chung and Cerniglia 1992).There is strong evidence that the majority of the aromatic

amines require metabolic activation for carcinogenicity (Skip-per et al. 2010). The first step in activation involves N-hy-droxylation and the second step involves O-acylation,yielding acyloxy amines (Fig. 3). In probably the first everrecognition of a proximate carcinogenic metabolite, N-hy-droxy-2-acetylaminofluorene proved to be more carcinogenicthan 2-acetylaminofluorene in a number of rat tissues (Milleret al. 1961). Conversely, reduction of the N-hydroxy deriva-tives of several aromatic amines led to their detoxification(King et al. 1999). In an in vitro study, Chinese hamsterovary cells transfected with genes catalyzing metabolic acti-vation of aromatic amines showed increase in cell death, mu-tagenesis, and DNA adduct levels in response to 2-amino-1-methyl-6-phenylimidazo [4,5-b] pyridine, as compared to un-transfected cells (Metry et al. 2007). Metabolic activation hasalso been found to be necessary in in vivo studies. 2-acetyla-minofluorene was not carcinogenic in female Fischer rats dueto their low capacity for N-hydroxylation. However, N-hy-droxy-2-acetylaminofluorene administered intraperitoneallyyielded malignant hepatic lesions (Gutmann et al. 1972). Ar-omatic amines also undergo N-acetylation by the enzymes N-acetyltransferases. This plays the role of detoxification sinceit lowers the concentration of N-hydroxylamine, which is re-sponsible for the genetic toxicity. In accordance with it, nu-merous studies have shown that benzidine-exposedindividuals with slow acetylation phenotype are at an in-creased risk of bladder cancer (Carreón et al. 2006). The N-hydroxylamines and their acyloxy derivatives can degrade toform highly reactive nitrenium and carbonium ions. Free rad-ical scavengers, including catalase and superoxide dismutase,have been shown to reduce the mutagenicity of benzidine,which suggests that reactive oxygen species (ROS) may alsobe generated as downstream effectors (Chen et al. 2003).These electrophilic reactants readily damage the cellularDNA and RNA molecules (Brown and DeVito 1993). Bag-nyukova et al. (2008) detected N-(deoxyguanosine-8-yl)-2-aminofluorene as the major adduct in the liver and kidney ofSprague–Dawley rats fed with 0.02% of 2-acetylaminofluor-ene. N-hydroxylamines also react with proteins like hemoglo-bin to form adducts that may persist for as long as theadducted hemoglobin remains in circulation. Hence, hemo-globin adducts are very useful in the evaluation of exposureto aromatic amines (Skipper et al. 2010). A study of Indianworkers exposed to benzidine showed positive correlation ofbenzidine–DNA adduct levels in the white blood cells and inthe exfoliated urothelial cells with the exposure status and in-ternal dose of benzidine metabolites (Zhou et al. 1997).

Ecotoxicity of azo dyesSince dye-containing effluents are normally discharged

into water bodies, toxicity of dyes has mainly been studiedagainst aquatic organisms. Azo dyes have been found to betoxic towards several aquatic organisms including algae, fish,and crustaceans like daphnids. Their acute toxicity is gener-ally very low. A survey of fish toxicity for 3000 azo dyesshowed that LD50 values were higher than 1 mg/L for 98%of the products (Clarke and Anliker 1980). Azo dyes havebeen shown to reduce viability, reproduction, rate of filtrationfeeding, and O2 consumption in the freshwater cladoceranMoina macrocopa (Wong et al. 2006). Birhanli and Ozmen(2005) found many azo dyes to be teratogenic in the frog em-bryo teratogenesis assay–Xenopus. Azo dyes also inhibit sev-eral biological processes, which are ecologically veryimportant. For example, they can inhibit algal photosynthesisby reducing the penetration of light. Similarly, dyes havebeen reported to inhibit COD (chemical oxygen demand) re-duction and respiratory activities of microbial populations.This may result in inhibition of microbial processes likewastewater treatment systems and natural biogeochemicalcycles (Chung and Stevens 1993). Novotný et al. (2006)studied toxicity of azo dyes in various microorganisms andfound that azo dyes can cause inhibition of luminescence inVibrio fischeri, growth inhibition in the microalga Selenas-trum capricornutum, and variety of effects on the viability,growth, grazing and morphometry of the ciliate Tetrahymenapyriformis. Reactive Black 5 and sulphanilic acid have beenshown to decrease the urease activity, arginine ammonifica-tion rate, nitrification potential and ammonium oxidizing bac-teria in soil. This may restrict the nitrogen-use-efficiency ofplants, thus reducing the productivity of terrestrial ecosys-tems (Topaç et al. 2009). Azo dyes can also directly affectplant growth by inhibiting seed germination, seedling sur-vival, and elongation of shoot and root (Puvaneswari et al.2006). Similarly, benzidine has been found to inhibit DNAsynthesis in the nucleus and deregulate calcium homeostasis,resulting in complete destruction of the maize root tip cells(Zaalishvili et al. 2000).Majority of the toxic effects of azo dyes are exerted

through aromatic amines produced by their degradation. Thearomatic amines exhibit very high level of ecotoxicity inaquatic organisms like daphnids, fish, and snails. Sensitivityof different groups of aquatic organisms towards aniline hasbeen reviewed by Ramos et al. (2002). Jiangning et al.(2004) showed that 4-aminobiphenyl affects motility ofDaphnia magna, and development of zebrafish embryos.Similarly, chronic dietary exposure of the fish Gambusia affi-nis to benzidine and 2-aminofluorene resulted in increasedcellular proliferation and apoptosis (Lentz et al. 2010). Aro-matic amines can inhibit bacterial and algal growth and activ-ity also. Dom et al. (2010) found that aniline and chloro-substituted anilines were more toxic to the alga Pseudokirch-neriella subcapitata than to E. coli. Azotobacter chroococ-cum cells showed lower nitrogenase activity, growth andATP levels in the presence of 4-aminobiphenyl or 3–3′-dia-minobenzidine (Pozo et al. 2000).Azo dyes and aromatic amines undergo bioaccumulation

and biomagnification along the food chain (Weisburger2002). This is affected by physico-chemical and toxicokineticproperties of the compounds, such as partition coefficient,



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molecular size, and respiratory volume and gill perfusion inaquatic organisms. The hydrophobic dyes, i.e., disperse andsolvent, and many aromatic amines have high values of parti-tion coefficient, and therefore, pose a high risk of bioaccumu-lation. 3,4-dichloroaniline was found to have an unusuallyhigh bioconcentration factor (BCF) up to 800 in the sedimentdweller Lumbriculus variegates (Schupp and West 2007). An-liker et al. (1981) analyzed 50 azo dyes for their partition co-efficient and BCF in fish. With a few exceptions, hydrophilicdyes had a low BCF. Disperse dyes also had lower BCF thanexpected, probably because of their high molecular weight oraggregation, making the transport across membranes difficult.Several studies have been carried out to determine the fate ofaromatic amines in the environment. Harden et al. (2006)showed that benzidine gets readily adsorbed on sediments,which limits its bioavailability and mobility. However, a 211-day incubation of benzidine in sediment-water system resultedin microbial degradation products like aniline, which hadhigher mobility in the water phase.

Legislations governing azo dyesDue to their toxicity, several azo dyes, especially

benzidine-based dyes, have been banned in many countries.Carcinogenic arylamines, such as 2-naphthylamine, and azodyes based on them have been banned in the UK since 1967and in US subsequently (Vineis and Pirastu 1997). The Euro-pean Union banned azo dyes based on 22 aromatic aminesby its directive 76/769/EEC relating to “restrictions on themarketing and use of certain dangerous substances and prep-arations” (Table 2). It was later amended to include two moreazo dyes and testing methods for the banned compounds,through the directives 2002/61/EC 2003/3/EC, and 2004/21/EC (European Commission 1976, 2002, 2003, 2004). TheMinistry of Environment and Forests in India, also called fora 3-year phase-out of the use of benzidine-based dyes in anotification published in the Gazette in January 1990 (ERM1998). As per this notification, handling of 42 benzidine-based dyes was prohibited from 1993 onwards. Handling of70 more azo dyes was further prohibited as per the notifica-tion published in the Gazette in March 1997.However, switching to non-benzidine dyes implied higher

costs. A study estimated that the cost of Direct Black 38 wasabout US$3.00/kg, whereas Direct Black 22, which does notuse benzidine, costs US$8.00–10.00/kg. The AhmedabadTextile Industry’s Research Association (ATIRA) estimated

that the cost of azo-free substitutes is 2.5 times that of azodyes. These changes were prohibitive for small- and medium-sized textile producers, which constituted 60% of the textileindustry in India. Hence, the use and manufacture of benzi-dine and benzidine-based dyes still continues in India andsome other countries like China, Korea, Taiwan and Argen-tina (Snyderwine et al. 2002). Several recent studies havedemonstrated water contamination resulting from continueddischarge of mutagenic textile and dye house effluents inthese countries (Carneiro et al. 2010).

Treatment methods for azo-dye-containing effluentsMany industries, such as dyestuff, textile, paper, plastic,

food, pharmaceuticals, and cosmetics, use dyes to colourtheir products. It has been estimated that the degree of fixa-tion of dyes to fabrics is never complete, resulting in dye-containing effluents. Approximately 2%–50% of dyes arelost in the effluent during dyeing process (McMullan et al.2001). These dyes are designed to resist fading by differentphysical, chemical, and biological agents and are thereforenot degraded by conventional treatment processes. These col-oured discharges are not only aesthetically unpleasing butalso pose ecological and public health risks. Different physi-cal, chemical, and biological techniques have been applied totreat these effluents.

Physical treatmentThe physical methods are often expensive, are greatly af-

fected by other wastewater constituents, and create seriousproblems related to the disposal of the concentrated sludge.It limits their use to small-scale in situ removal. Also, themain problem i.e., toxicity of dyes, remains largely unsolved.This section describes the advancements in different physicaltreatment methods to address these problems.

Coagulation–flocculationConventionally, coagulation, and flocculation using Fe, Al,

and Mg salts is used for the primary treatment of differentkinds of wastewater. It is a simple and economically feasibleprocess. However, it generates large amount of dye-contain-ing sludge that presents handling and disposal problems. Alot of work is currently going on to reduce these problems.Reuse of ferric chloride sludge has been demonstrated forthe removal of Acid Red 119, which may present an econom-ical coagulation–flocculation system (Sadri Moghaddam etal. 2010). Although synthetic polymeric flocculants are very

Fig. 3. Metabolic activation of aromatic amines.

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effective because of their tailorability, they can leave harmfulchemical residues. Hence, there is increasing interest in natu-ral polymers, such as chitosan, which are low cost, non-toxicand biodegradable. Several investigators have attemptedgrafting synthetic polymers onto the backbone of natural pol-ymers to obtain desired functional properties. Lignin-basecationic polyelectrolyte (Fang et al. 2010) and acrylamide-grafted Ipomoea seed gum (Sanghi et al. 2007) are some ofthe successfully used examples of such flocculants.

ElectrocoagulationIt involves application of electric field between metal elec-

trodes immersed in polluted water, which causes dissolutionof the metal plates. The metal ions, usually Fe or Al, formmetal hydroxides that adsorb and precipitate the suspendedparticles and dissolved contaminants. However, the techniquesuffers from several of the disadvantages of conventional co-agulation process, apart from the high cost of electricity. Theelectrode and energy consumptions during decolourization ofLevafix Orange dye were found to be 1.8 kg Al/kg dye and35 kWh/kg dye, respectively (Kobya et al. 2006). Also, Palá-cio et al. (2009) reported that electrocoagulation could not re-move the toxicity of a textile dye wastewater completely.Essadki et al. (2008) developed an external-loop air-lift reac-tor for electrocoagulation, which did not use mechanical agi-tation or air injection, but liquid recirculation was induced byH2 microbubbles generated by water electrolysis. It showedequivalent colour removal efficiency with lower energy andelectrode consumptions as compared to the conventionalelectrocoagulation cell. Eyvaz et al. (2009) found that alter-nating current was superior to direct current for electrocoagu-lation of reactive and disperse dyes.

AdsorptionAdsorption is one of the most popular methods for the re-

moval of pollutants from wastewater. It has been found to besuperior to other physical techniques in terms of initial cost,flexibility, simplicity of design, ease of operation, and insen-sitivity to toxic pollutants. However, adsorption process is in-fluenced by many physico-chemical factors, such as dye/sorbent interaction, sorbent surface area, particle size, tem-perature, pH, and contact time (Gupta and Suhas 2009).Amongst all the adsorbent materials tested, activated carbonis the most popular and effective, but it is very expensive.Activated carbon produced from waste materials, such as tirerubber (Mui et al. 2010) or bamboo (Ahmad and Hameed2010), have been found to be very effective in dye adsorp-tion. The use of agricultural wastes, natural materials, and bi-oadsorbents (living or dead biomass, especially fungi) hasalso attracted wide attention at the laboratory-scale only asthese adsorbents have lower surface area and require longercontact times. Natural materials like chitosan, fruit peels,wood chips, alginate, and microbial biomass have been usedsuccessfully in several studies (Gupta and Suhas 2009). In aninteresting study, Golder et al. (2006) demonstrated reusingof metals hydroxide sludge generated during electrocoagula-tion for the removal of Congo Red. Dye-sensitized solar cellsinvolve adsorption of dye molecules onto electrode surface,but the process requires a very long time. Seo et al. (2010)applied an electric field to ionize the dye molecules, whichresulted in much faster dye adsorption.

Ion exchangeThe ion exchange method uses synthetic or natural ion ex-

change resins for adsorption of dyes. Akceylan et al. (2009)developed a calix[4]arene-based polymer which could re-move azo dyes as well as aromatic amines in a wide pHrange. Modified natural materials, such as cationic-polymer/bentonite complex and organofunctionalized layered silicate(Royer et al. 2010), have also shown promising results. How-ever, this method is not widely used for the treatment of dye-containing effluents, mainly due to the opinion that ion ex-changers cannot accommodate a wide range of dyes. Anothermajor disadvantage is the cost involved.

IrradiationSufficient quantities of dissolved O2 are required for or-

ganic substances like dyes to be broken down effectively byradiation. The dissolved O2 is consumed very rapidly and aconstant supply is required, which increases the cost. Hosonoet al. (1993) used high energy electron beam for degradationof Acid Red 265 in a solution supersaturated with O2. Thismethod has now been modified by inclusion of catalysts,which greatly enhance the efficiency of process, as discussedin the following.

UltrasoundWhen aqueous solutions are exposed to ultrasound, transi-

ent cavitations are formed by compression and rarefaction ofthe bulk water. The collapse of cavities produces locally highpressure and temperature peaks, which can cleave water intohydroxyl radicals and hydrogen atoms. The combined actionof high temperature, pressure and radicals leads to sonolyticdegradation of various pollutants. Addition of catalysts canfurther increase the efficiency of the process. Eren and Ince(2010) compared sonolytic and sonocatalytic degradation oftwo azo dyes. High-frequency ultrasound was required forsignificant colour decay, but addition of CCl4, TiO2 or zero-valent Cu improved the performance of low-frequency ultra-sound above that of high-frequency ultrasound. The methodhas some disadvantages, such as the formation of toxic andcarcinogenic aromatics by pyrolysis of azo dyes. Also, theprocess requires high energy input.

Membrane filtrationUltrafiltration and nanofiltration membranes can be used to

clarify and concentrate dyes from the effluent in a continuousprocess. Several materials, such as nanofiltration polyamidecomposite membranes (Mo et al. 2008) and ceramic mem-branes developed from alumina and clay (Bhattacharya et al.2010), have been shown to give good colour removal, espe-cially when applied after the coagulation–flocculation step.However, the concentrated residue left after separation posesdisposal problems. Also, the membranes have a limited life-time before clogging or fouling occur, and the cost of peri-odic replacement makes the process economically unviable.Uzal et al. (2010) tested another membrane process, i.e., re-verse osmosis, for removal of indigo dyes and found that theproblems of low flux rate and fouling were reduced as com-pared to nanofiltration.

Chemical treatmentThe chemical techniques are often expensive and, although



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the dyes are removed, accumulation of concentrated sludgemay create a disposal problem. There is also a possibilitythat secondary pollution problem will arise because of exces-sive chemical use. High consumption of electrical energy andchemical reagents are common problems. Recently, advancedoxidation processes (AOPs), which are essentially photo-chemical or electrochemical methods involving generation ofvery powerful oxidizing agents such as hydroxyl radicals,have been applied with success for pollutant degradation.Although these methods are efficient, they are very costlyand commercially unattractive. Major chemical methods usedfor treatment of dye wastewater are as follows:

OzonationOzone is a very good oxidizing agent due to its high oxi-

dation potential (2.07) compared to chlorine (1.36), and H2O2(1.78). However, a disadvantage of ozone is its short half-life,typically being 20 min. The stability is also affected by thepresence of salts, pH, and temperature. Due to its short half-life, continuous ozonation is required, which increases thecost. To address this problem, Santana et al. (2009) generatedozone in a laboratory-made electrochemical reactor and usedit for degradation of Reactive Orange 122 in a bubble columnreactor. A study about supplementation of catalysts duringozonation showed that Mn and kaolin enhanced decolouriza-tion of Methylene Blue (Gao et al. 2009).

Sodium hypochloriteThis method attacks at the amino group of dyes, and ini-

tiates and accelerates azo bond cleavage. Chlorination of dyewastewater by in situ generation of active chlorine or by ad-dition of hypochlorite has been demonstrated by many inves-tigators (Oliveira et al. 2007). Li et al. (2009) showed thataddition of hypochlorite to potassium ferrate(VI) enhancedthe decolourization of azo dye Orange II above that achievedwith potassium permanganate or potassium ferrate(VI). Theuse of chlorine for dye removal, however, is becoming lessfrequent due to its negative effects upon release into water-ways, and the release of carcinogenic aromatic amines.

Redox-active metalsFenton reagent (H2O2–Fe(II)) is a suitable chemical means

of treating wastewaters that are resistant to biological treat-ment or are poisonous to live biomass. One major disadvant-age of this method is the excessive generation of sludge thatcreates a disposal problem. In a heterogeneous Fenton-typeprocess using Fe-exchanged zeolite, dyes could be degradedwithout releasing significant amounts of Fe ions in the bulkphase, and the process could be operated at mild pH (Aleksicet al. 2010). Zero-valent metals, especially Fe0, also providea very cheap alternative for degradation of azo dyes. The re-dox couple formed by Fe0 and dissolved Fe2+ can reduce notonly the azo bonds but also O2 to generate H2O2. The reac-tion then proceeds via Fenton mechanism (Chang et al.2009). Gomathi Devi et al. (2009) described optimization ofdye degradation using zero valent Fe and found that additionof oxidizing agents, such as H2O2 or ammonium persulphate,enhanced the efficiency of process.

Photochemical treatmentThis method uses UV light to activate chemicals such as

H2O2, resulting in the production of hydroxyl radicals that

degrade dye molecules to CO2 and H2O. UV radiation hasbeen shown to increase the decolourization and mineraliza-tion efficiency in both Fenton-type process (Aleksic et al.2010) and zero-valent metal oxidation (Gomathi Devi et al.2009) by several fold. Rodríguez Couto et al. (2002) showedthat ZnO immobilized in alginate beads catalyzed photode-gradation of organic dyes with different structures, revealingthe nonspecificity of the system. Addition of H2O2 was foundto increase the efficiency of TiO2-catalyzed photodegradationof azo dyes, and decolourization and degradation efficienciesup to 100% could be achieved (Soutsas et al. 2010). The dis-advantages of this method include potential formation of by-products, which may be more toxic and poor colour removalfor some dyes. However, with significant amount of researchwork going on in the area, these problems may soon besolved.

Electrochemical destructionElectrochemical destruction is a relatively new technique

with little or no consumption of chemicals and no sludgebuild up. However, some issues, like high cost of electricityand electrolytic apparatus and poor colour removal for somedyes, may be prohibitive. One electrochemical approach in-volves direct oxidation of pollutants after adsorption on theanode surface. In a comparison of different anodic materialsfor oxidation of Methyl Red, lead dioxide, and boron-dopeddiamond showed superior performance in terms of colour re-moval and polarization characteristics (Panizza and Cerisola2007). Another method is based on cathodic reduction of O2to H2O2, which can oxidize several azo dyes. Addition of Fecatalyst to the electrogeneration of H2O2 (electro-Fentontechnology) can improve the process performance by severalfold. Advantage of this modified Fenton method include con-tinuous supply of the reactant H2O2, continuous regenerationof Fe2+ at the cathode, and additional generation of hydroxylradicals by water oxidation at the anode apart from the regu-lar production from Fenton reaction. In a comparison of ano-dic oxidation, oxidation with electrogenerated H2O2 and theelectro-Fenton process, Wang et al. (2010) found that electro-Fenton reaction generated higher amount of hydroxyl radicalsand increased the subsequent biodegradability of Acid Red14. The efficiency of the process can be further improved byirradiation with UV light (photoelectro-Fenton process).Wang et al. (2008) showed that photoelectron-Fenton processexhibited much better mineralization of Acid Red 14 as com-pared to the electro-Fenton method.

Biological treatmentBiological treatment is often the most economical alterna-

tive when compared with other physical and chemical proc-esses. It has attracted wide interest because of its efficiency,versatility, lower construction, and operation costs, robustnessand eco-friendliness. Unlike physical and chemical methods,biological treatment mineralizes the pollutant, leading tocomplete detoxification, and avoiding the problems of sludgedisposal and secondary pollution. The most important prob-lem with bioremediation is the slowness of the process,which limits its application at field level. Most of the workin this area is focused on microorganisms, although othertechniques like phytoremediation have also been applied suc-cessfully. Davies et al. (2009) obtained about 68% removal of

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Acid Orange 7 by Phragmites australis, the most widelyused plant in constructed wetlands. They found that the dyecaused oxidative stress, resulting in the induction of ROS-scavenging enzymes in the plant. However, phytoremediationhas several disadvantages, like time and space requirement,and chances of groundwater contamination (Kagalkar et al.2009).

Decolourization by fungiBy far the most widely studied dye-decolourizing microor-

ganisms are the white-rot fungi, such as Phanerochaetechrysosporium, which are characterized by their ability to de-grade lignin. In addition to their natural substrate, white-rotfungi can mineralize a diverse range of persistent organicpollutants, such as azo dyes. Experiments using 14C-labeledazo dyes demonstrated that P. chrysosporium could mineral-ize azo dyes to 14CO2 (Paszczynski et al. 1992). This is be-cause of the relatively nonspecific nature of their lignolyticenzymes: lignin peroxidase (LiP), manganese peroxidase(MnP), and laccase. LiP catalyzes oxidation of non-phenolicaromatic compounds such as veratryl alcohol (VA), whileMnP oxidizes Mn2+ to Mn3+ which, in turn, is able to oxi-dize many phenolic compounds. Laccase can directly oxidizephenolic substrates by using O2 as the electron acceptor. Ver-satile peroxidases (VP) have been recently described as anew family of lignolytic peroxidases, which exhibit both LiPand MnP-like activity. These lignin metabolizing enzymescan mineralize azo dyes either directly or indirectly throughcertain redox mediators (Fig. 2). The detailed mechanismand catalytic cycles of these enzymes have been reviewedelsewhere (Gao et al. 2010). The action of these enzymes onazo dyes has been shown to catalyze oxidative cleavage ofazo bonds and aromatic ring opening in several studies (Svo-bodová et al. 2007). In a comparison of white-rot fungi forthe bioremediation of textile effluent, Bjerkandera adustawas found to show very high decolourization in solid sub-strate fermentation (Robinson and Nigam 2008). Enzymeproduction by fungi is highly affected by nutrient media. Tra-metes trogii grown in the presence of glutamic acid producedhigh laccase and MnP activities, resulting in fast decolouriza-tion of several azo dyes (Levin et al. 2010). Lu et al. (2010)studied suitability of P. chrysosporium bioreactors for dye de-colourization. They found that contamination with foreignfungi increased over time and negatively affected the growthand MnP activity, resulting in a decline in dye decolouriza-tion. Diversity of the foreign fungi was higher in sequentialreactor than in continuous reactor, suggesting that the latteris more suitable for dye decolourization. Application of fungiin wastewater treatment has been limited owing to contami-nation by bacteria and other microorganisms. Tang et al.(2011) used a lactic acid buffer solution to avoid this prob-lem and successfully decolourized several dyes with Schizo-phyllum sp. F17 under non-sterile conditions. Non-white-rotfungi such as Geotrichum candidum and yeasts like Pichiapastoris also possess peroxidases and laccases capable of de-colourizing dyes (Kim and Shoda 1999; Lu et al. 2009).Although fungi can decolourize dyes in liquid fermenta-

tion, enzyme production has been shown to be unreliable.This is mainly because of the unfamiliar environment ofliquid fermentation (Robinson et al. 2001). Utilization ofthese fungi in their natural environment requires solid sub-

strate fermentation, which is not practically feasible in waste-water treatment plants.

Aerobic bacterial decolourizationLike the white-rot fungi, actinomycetes, particularly Strep-

tomyces, can also produce laccases and peroxidases that candegrade lignin and xenobiotic compounds like azo dyes. Alaccase produced by Streptomyces cyaneus could decolourizeazo dyes by more than 90% in the presence of redox media-tor acetosyringone (Moya et al. 2010). Similarly, a DyP-typeperoxidase from the thermophilic actinomycete Thermobifidafusca was found not only to decolourize azo dyes but also todegrade phenolic and aromatic sulphide compounds (vanBloois et al. 2010). The finding that actinomycetes are capa-ble of aerobic decolourization and degradation of azo dyes issignificant given the recalcitrance of these compounds todegradation by other bacteria under such conditions. Apartfrom actinomycetes, some peroxidase-producing bacteriasuch as Acinetobacter calcoaceticus have also been shown todecolourize azo dyes (Ghodake et al. 2009). Similarly, thecyanobacterium Anabaena was found to produce a DyP-typeperoxidase capable of decolourizing both anthraquinone andazo dyes. The efficiency of decolourization increased in thepresence of redox mediators like syringaldehyde (Ogola etal. 2009).Some bacterial strains can aerobically decolourize the azo

dyes by reductive mechanisms. This requires aerobic azore-ductase enzymes that catalyze azo bond cleavage in the pres-ence of O2 (Fig. 2; Bafana et al. 2008). Such oxygen-insensitive enzymes have been isolated from several bacteria,such as, Bacillus, Enterococcus, Staphylococcus aureus, E.coli, Pseudomonas aeruginosa, Shigella flexneri, R. sphaer-oides, Xenophilus azovorans, and Pigmentiphaga kullae (Ba-fana and Chakrabarti 2008). Azoreductase activity has alsobeen characterized in eukaryotes such as yeasts, human, rat,and rabbit. Since azoreductases from various sources showsignificant sequence variation, they were hypothesized tohave evolved independently from each other. However, Ba-fana and Chakrabarti (2008) proposed horizontal transfer ofazoreductase genes among phylogenetically diverse organ-isms. Although azoreductases can reduce azo dyes both invivo and in vitro (Feng et al. 2010), it is widely believedthat azo dye reduction is a fortuitous reaction and azoreduc-tases evolved for some other in vivo functions. As a suppor-tive evidence, Liu et al. (2009) found that azoreductase in E.coli can act as a quinone reductase, providing resistance tothiol-specific stress caused by electrophilic quinones.Recombinant over-expression of azoreductases has been

used to enhance azo dye decolourization by several research-ers (Sandhya et al. 2008). Gopinath et al. (2009) followed adifferent approach for azoreductase over-expression. They ob-tained azoreductase over-expressing mutants of Bacillus byUV and ethidium bromide-induced random mutagenesis.However, azoreduction of dyes results in the production ofcarcinogenic aromatic amines and hence, azoreductases alonecannot be used for treatment of azo dyes. The isolation ofbacteria capable of using azo dyes as sole source of carbonand energy, resulting in their mineralization under aerobicconditions, has proven difficult. The first such report wasfrom Overney who isolated a Flavobacterium capable ofgrowing aerobically with 4,4-dicarboxyazobenzene. Later,



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Sphingomonas, Comamonas, Pseudomonas, Xanthomonas,and Alcaligenes were also found to degrade this compoundaerobically (Stolz 2001). Coughlin et al. (1999) reported theisolation of a Sphingomonas that was capable of aerobicallydegrading a suite of azo dyes, using them as sole source ofcarbon and nitrogen. The pathway of azo dye degradation fol-lowing azo bond cleavage has still not been determined,although a few degradation intermediates have been identi-fied. Bafana et al. (2009a, 2009b) identified 4-aminobiphenylas an intermediate during Direct Black 38 degradation byseveral microorganisms like Bacillus velezensis and Entero-coccus gallinarum.Since very few bacteria have been reported to aerobically

decolourize azo dyes, aerobic treatment proves to be ineffec-tive in most cases. Moreover, the substrate specificity ofaerobic azoreductases is fairly limited resulting in azo dyesoften passing through conventional activated sludge facilitieswith little or no reduction in colour (Hsueh et al. 2009).

Anaerobic bacterial decolourizationIn contrast to aerobic decolourization, a wide range of or-

ganisms, such as Bacteroides, Eubacterium, Clostridium,Proteus, Streptococcus, yeasts and even higher organisms,are able to reduce azo compounds anaerobically (Stolz2001). Photosynthetic bacteria have also been reported to de-colourize azo dyes under anaerobic conditions only. Liu et al.(2007) showed that R. sphaeroides and R. palustris were bet-ter decolourizers of sulphonated azo dyes, as compared to arecombinant E. coli strain over-expressing azoreductase,under anaerobic condition. Anaerobic dye decolourization oc-curs by nonspecific reductive cleavage of the azo linkage byreduced electron carriers. Under aerobic condition, O2 outcompetes the azo compounds for the reduced electron car-riers, resulting in poor decolourization. Cytoplasmic flavinreductases have been proposed to exhibit the azoreductase ac-tivity under anaerobic conditions by facilitating transfer ofelectrons to the azo dye via reduced flavins (Fig. 2; Stolz2001). However, such cytoplasmic enzymes cannot reducehighly polar sulphonated azo compounds because of the lowpermeability of the cell membrane (Wuhrmann et al. 1980).These dyes can be reduced by the addition of redox media-tors that can shuttle electrons between the cell and extracellu-lar azo dyes in a purely chemical reaction. Cervantes et al.(2010) showed that quinoid redox mediators, like 1,2-naph-thoquinone-4-sulfonate and anthraquinone-2,6-disulfonate,adsorbed on anion exchange resins greatly enhanced the re-ductive decolourization of azo dyes by an anaerobic granularsludge. Sphingomonas xenophaga was shown to synthesizeits own redox mediators during reduction of the sulphonatedazo dye amaranth (Keck et al. 2002). In a similar manner,certain anaerobic bacteria produce metabolic end productslike Fe2+ or H2S, which can reduce azo dyes in a purely re-dox reaction. Bioaugmentation of an anaerobic sludge withDesulfovibrio desulfuricans resulted in significant improve-ment in dye decolourization due to the production of H2S(Kim et al. 2007). In a different mechanism, certain bacteriacan utilize azo dyes as the terminal electron acceptor in therespiratory electron transport chain. Hong et al. (2007) usedseveral respiratory inhibitors to show that Shewanella decol-orationis cells can generate energy by the dissimilatory azor-eduction process. Anaerobic reduction of azo dyes has been

utilized in the construction of microbial fuel cells (MFC),where microbial oxidation of organic waste material at theanode is coupled to abiotic cathodic decolourization of azodyes. Ding et al. (2010) developed a photocatalytic MFC forimproved azo dye removal. Irradiation of rutile-coated cath-ode with visible light enhanced the cathodic electron transferto azo dyes, resulting in rapid azoreduction with concomitantelectricity production. However, the process resulted in therelease of carcinogenic amines. Li et al. (2010b) constructeda sequential anaerobic (anode)-aerobic (cathode) MFC toovercome this problem. Here, azo bond was cleaved biologi-cally in the anaerobic chamber and abiotically in the aerobicchamber, while the toxic aromatic amines were removed bio-logically in the aerobic chamber.With their nonspecific azoreductase activity, anaerobic or-

ganisms present a robust and versatile system for azo dye de-colourization. However, the hazardous aromatic aminesformed by reduction of azo dyes are generally recalcitrantunder anaerobic conditions (Pinheiro et al. 2004). A waste-water treatment process where anaerobic and aerobic condi-tions are combined is, therefore, proposed as the mostlogical option for complete removal of azo dyes. In the firstanaerobic stage, azo dyes are readily reduced to colourless ar-omatic amines, which are then metabolized relatively easilyunder aerobic conditions. Franciscon et al. (2009) describedbiodegradation of four different azo dyes in a sequential mi-croaerophilic–aerobic treatment by a facultative Klebsiella sp.Different bioreactor designs to obtain an effective continuousanaerobic-aerobic treatment of azo dyes have been reviewedby van der Zee and Villaverde (2005).

Enzymatic decolourizationAs dye decolourization and detoxification activities of var-

ious organisms are ultimately catalyzed by their enzymes,there has been much interest in the direct use of enzymes fortreatment of dye wastewaters. The potential dye decolouriz-ing enzymes mainly include various oxidoreductases such asazoreductases, peroxidases and laccases. Although azoreduc-tases from various sources have been shown to decolourizeazo dyes very efficiently, they generate carcinogenic aromaticamines and hence, are not used for treatment purpose (Sand-hya et al. 2008). Fungal laccases and peroxidases, on theother hand, have great potential in treating a wide spectrumof dyes. These enzymes convert a broad range of dyes intoless toxic insoluble compounds, which can be easily removedout of wastewater. In a comparative study, MnP from B.adusta was found to show better dye decolourization thanthe fungus itself (Mohorčič et al. 2006). Ghodake et al.(2009) showed that LiP activity could be stabilized by trypto-phan resulting in improved decolourization. Peroxidase actionrequires addition of large amount of H2O2 as cofactor, which,at times, inhibits the enzyme activity. In situ generation ofH2O2 at a slow rate by addition of glucose oxidase and glu-cose was found to support efficient dye degradation by LiP(Lan et al. 2006). Application of Trametes villosa laccase forazo dye decolourization produced large amount of polymer-ized products, which showed unacceptable colour levels, lim-iting the application of laccases as bioremediation agents(Zille et al. 2005). While using whole white-rot fungi, otherlignin degrading enzymes probably cooperate with laccaseand prevent the backward polymerization of reaction products

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(Svobodová et al. 2007). Biswas et al. (2007) proposed thatsuch polymerization products can be removed by coagula-tion–flocculation process, resulting in effective decolouriza-tion and detoxification.Several plant peroxidases, especially horseradish peroxi-

dase (HRP), have also been applied for dye decolourization.Citraconic anhydride-modified HRP was found to showgreater affinity and catalytic efficiency for dye decolouriza-tion than the native HRP (Liu et al. 2006). Kim et al. (2005)developed a process for electrochemical generation of H2O2,which was used as the cofactor during dye decolourization byHRP. The process, however, resulted in the formation of aro-matic amines. Use of immobilized enzymes and redox medi-ators can improve the efficiency of dye decolourization byincreasing the enzyme stability and the range of susceptibledyes. Myceliophthora thermophila laccase covalently immo-bilized on polymethacrylate-based polymer showed betterstability towards pH, temperature and storage time. Also, thedecolourization efficiency was improved in the presence ofredox mediator 1-hydroxybenzotriazole (Kunamneni et al.2008). A recombinant CotA-laccase from Bacillus subtiliswas found to decolourize a variety of structurally differentdyes in the absence of redox mediators. Oxidation of SudanOrange G with this enzyme resulted in the production ofoligomers along with significant decrease in the toxicity (Per-eira et al. 2009).Some issues that need to be addressed for successful appli-

cation of enzymatic decolourization approach are develop-ment of low-cost and high-yield sources of enzymes,efficiency of the enzymes under field conditions, character-ization of reaction products, and impact on any downstreamprocess or on the environment into which the treated wastesare released.

Biological detoxification of dyesAlthough there is a tremendous amount of work currently

ongoing in the field of dye decolourization, the main issue(i.e., detoxification of dyes) has been addressed by very fewstudies. The majority of such studies have used biologicalagents for dye decolourization and detoxification. White-rotfungi like P. chrysosporium (Choudhary et al. 2004), B.adusta and T. versicolor (Apohan and Yesilada 2005) havebeen shown to detoxify certain azo dyes. El-Rahim et al.(2008) demonstrated detoxification of Direct Violet by theascomycete Aspergillus niger through sensitive genotoxicityassays like micronucleus assay and RAPD–PCR fingerprint-ing pattern in male rats. Certain aerobic bacteria can miner-alize and detoxify the dyes in pure culture, although withlimited substrate specificity. Bacteria such as Pseudomonas(Ben Mansour et al. 2007) and Bacillus (Bafana et al. 2008)have been reported to detoxify dyes in pure cultures. Com-bined anaerobic–aerobic reactors, utilizing mixed cultures,have also been successful in detoxification of dyes in severalcases (Melgoza et al. 2004).A review of the literature reveals that very diverse proce-

dures and test organisms have been employed to assess toxic-ity during dye degradation studies. For example, toxicitytowards D. magna, cytotoxicity and inhibition of respirationin bacteria, and inhibition of bioluminescence (Microtox),methanogenesis (ATA) or plant seed germination have beenused as the test systems. While the above assays may provide

simple test systems, the nonuniformity in procedures usedmakes correlation or comparison between different studiesdifficult. This may be because of the absence of a specificlegislation stating the most appropriate tests to be applied indifferent situations and providing tools for unequivocal inter-pretation of data. In a study by Anastasi et al. (2010), differ-ent tests, and even several parameters within the same test,showed different results for the same textile wastewaterwhich was treated using B. adusta. Also, toxicity and muta-genicity are two different attributes. However, very few stud-ies have complemented the dye detoxification data withmutagenicity results. In two independent studies, Bafana etal. (2009a, 2009b) showed that toxicity and mutagenicity re-sults were different during the treatment of azo dyes by purebacterial cultures. Also, the toxicity and mutagenicity testsystems used for azo dyes lack a systematic dose-responsedata, and risk assessment data, which is needed for extrapola-tion of results to higher organisms, including humans. Hence,there is urgent need to develop or adopt a standard battery oftoxicity testing procedures to ascertain detoxification of dyes.

Combinatorial treatmentAs discussed previously in the text, none of the treatment

methods has sufficiently broad substrate range and robustnessto decolourize complex dye wastewaters that vary in compo-sition depending not only on the source but also on theschedule and requirements of a single source. A feasible sol-ution to this problem is the sequential application of a combi-nation of treatments. The treatments must be selectedcritically so that they complement each other in terms of sub-strate range and insensitivity towards other wastewater con-stituents. A variety of promising combinations have beeninvestigated at the laboratory level. Most of these involvephysico–chemical treatment methods, probably because ofthe sensitivity of biological methods towards the reagents re-quired during physico-chemical treatments, or because of alack of integration between the different disciplines. Coagula-tion–flocculation followed by separation of the resultingsludge is a widely used approach. Harrelkas et al. (2009)used coagulation–-flocculation using aluminium sulphate fol-lowed either by membrane processes like microfiltration orultrafiltration, or by adsorption on activated carbon. Thecombination of coagulation–flocculation followed by ultra-filtration was found to yield the best result with 74% colourremoval. Shkavro et al. (2010) effectively used a combinationof activated carbon adsorption and ultrafiltration, resulting insubstantially higher degree of dye removal, increase in theprocess capacity, and prolongation of the membrane life. Sev-eral combinatorial studies have focused on AOPs, such asFenton reaction, because of their relative nonspecificity to-wards the substrate. More than 95% colour removal wasachieved by complementing Fenton oxidation with sludge re-moval by lime coagulation (Kulik et al. 2007). Treatment ofthe azo dye Basic Red 46 by photoelectro-Fenton reactioncombined with photocatalysis using TiO2 nanoparticles re-sulted in 98.8% mineralization (Zarei et al. 2010). Electroca-talytic and photocatalytic methods have also attracted muchinterest. A two-step process involving electrocatalytic pre-ox-idation followed by photocatalytic oxidation was found to de-colourize high concentrations of Methyl Orange. A SnO2/TiO2–NTs/Ti electrode, simultaneously possessing the photo-



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catalytic oxidation properties of TiO2–NTs and the electroca-talytic oxidation abilities of Sb-doped SnO2, was used for thispurpose (Zhao et al. 2010). A combination of zero-valent Fe/activated carbon and microwave discharge electrodeless lamp/sodium hypochlorite was found to give much higher degrada-tion of Reactive Red 195 than both single steps. The firststep could break the azo bond, and then the second step de-graded the aromatic amine products effectively. Reversing theorder of treatments reduced the degradation efficiency (Fu etal. 2010). Although ultrasound alone is not very efficient atdye degradation, it has been shown to considerably enhancethe performance of other AOPs. Ultrasound-assisted electro-catalytic oxidation process was found to exhibit synergisticdecolourization of several azo dyes (Ai et al. 2010). Simi-larly, efficient and convenient degradation of Acid Red 97by a combination of ultrasound and Fenton reagent was re-ported by Li and Song (2010).Combinations of biological and physico–chemical treat-

ments, in any order, have been attempted by relatively fewerstudies. García-Montaño et al. (2008) compared several bio-logical and chemical coupled treatments and found that anae-robic biotreatment followed by ozonation yielded the bestresults. The combination treatment achieved 83% mineraliza-tion and produced harmless effluent. A treatment in reverseorder (i.e., ozonation and subsequent biological degradationwith a biofilm) was found to reduce the toxicity of RemazolBlack B, as demonstrated by D. magna assay (de Souza et al.2010). Similarly, application of a combination of oxidativeenzymatic treatment with laccase and ultrasound treatmentled to increased degradation of Acid Orange and Direct Bluedyes, as compared to individual treatments (Tauber et al.2008).

Industrial application of dye wastewater treatmenttechniquesSeveral innovative and nonconventional methods are being

applied towards dye decolourization at pilot or full scalestudies. Apart from efficiency, economy, and ease of opera-tion are also important prerequisites for these methods. Themajority of such applications are based on or involve biolog-ical techniques. Soares et al. (2006) applied a cocktail of lac-case and peroxidases for decolourization of real-worldwastewater from a textile dying and printing industry in Por-tugal, using a 1 m3 stirred-tank bioreactor. The efficiency ofdecolourization varied considerably with fluctuations in tem-perature and other conditions, but on average, decolourizationachieved was within the consent limits established by thelegislation. A combination of zero-valent Fe and biologicaltreatments was used at a treatment facility in China, receiving80% industrial (including dye manufacturing) and 20% mu-nicipal effluent. The facility had a treatment capacity of60 000 m3/day of wastewater. Integration of zero-valent stepin the treatment resulted in impressive improvement in COD,BOD (biological oxygen demand), nitrogen, and phosphorusremovals. The average colour removal was about 80% (Maand Zhang 2008). An integrated electron beam-biologicaltreatment was used to treat dye wastewater in a pilot plant(with a capacity of 1000 m3/day) in Korea. Pretreatmentwith a low dose (1 kGy) of electron beam resulted in partialdegradation of dyes to intermediates, which were more sus-ceptible to subsequent biodegradation (Han et al. 2005).

Tseng et al. (2001) developed a full-scale process using bio-logical activated carbon, which combined both physical ad-sorption and biological degradation, resulting in increase inthe retention time of pollutants with subsequent enhancementof the microbial biodegradation. The process complied withthe regulatory limits for removal of organics and colour,with a relatively lower operation cost. A pilot-scaleanaerobic-aerobic membrane bioreactor (with a capacity of10 m3/day) was found to show excellent removal of COD,BOD, and colour, and met with the reuse water standard(Xiang et al. 2003).Unfortunately, all of these studies have used general pa-

rameters like COD, BOD, and colour removal to determinethe treatment efficiency. However, without the toxicity andmutagenicity assay results, it is not possible to predict thesafety of treated effluent.

Future trends and needsGlobal dyestuff industry is currently facing major chal-

lenges, such as high competition, over-capacity, falling mar-gins, and increased environmental considerations. This hasresulted in a general unwillingness towards overhead expendi-tures including R&D and wastewater treatment. Hence, eco-nomical removal of colour and toxicity from effluentsremains an important problem. Dye removal is complicatedby the structural diversity of dyes that may be used in a singledyeing operation, and also by other wastewater constituentsthat may attenuate the treatment process. A conventional treat-ment plant, generally consisting of coagulation-flocculation,activated sludge process and chlorination, is clearly incapableof treating dye wastewaters. At the same time, limited avail-ability of water supplies is forcing the implementation ofwater saving and recycling, which tends to generate concen-trated waste streams. On the other hand, environmental con-cerns and relative recalcitrance of dyes demand effluents withincreased treatability, producing a very complex situation.With the realization that a single technique cannot give

universal solution, the recent trend in dye wastewater treat-ment is focused around integration of multiple techniques.Different combinations of AOPs and other methods are top-ping the lists of publications. Unfortunately, fewer studieshave targeted combinations of physico–chemical methods, es-pecially the AOPs, with biological treatment. As biologicaltreatment is a common component of wastewater plants andhence, is easily accessible, industries need not make addi-tional expenditure for its construction and maintenance.Also, it is desired to utilize the versatility, detoxification ca-pability and low-cost advantages of biological methods. Theefficiency of biodegradation can further be improved by mo-lecular tools such as recombinant DNA technology and bio-engineering approaches. AOPs, on other hand, are highlyefficient broad-specificity methods that can satisfactorilycomplement biological treatment. Hence, a combination ofbiological methods with AOPs can be an ideal solution.However, this will require consideration of some importantissues. Pretreatment with an AOP may involve addition of orgeneration of compounds/conditions that are inhibitory to mi-croorganisms. Conversely, it may turn out to be advantageousby converting azo dyes to less recalcitrant forms that can bedegraded more rapidly by microorganisms. Hence, the order,nature, complementarity and compatibility of the combined

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techniques are very important. As AOPs are still very costly,their development into a cost-effective technology will be theimmediate research target in the future. Adsorption on a suit-able support, such as activated carbon or natural adsorbents,may be included at the end of dye treatment processes as afail-safe mechanism. This will prevent the release of un-treated dyes or toxic degradation intermediates into the envi-ronment. Desorption of wastewater constituents from theadsorbent and treatment of the resulting concentrated eluatewill be another avenue for intensive research in the future.Broader validation and scale-up of these integrated technolo-gies in the future will most likely produce an efficient andeconomically viable process.Pathways and enzymes involved in microbial azo-dye deg-

radation and detoxification are still not extensively character-ized. This has negatively affected the attempts towardsprocess understanding and optimization. More mechanisticstudies need to be undertaken to address this question. Also,sensitive analytical methods need to be developed to eluci-date the structures of intermediates formed during dye degra-dation. This will not only increase the process understanding,but also help in testing the presence of toxic intermediates forregulatory purpose. The literature is saturated with reports re-garding new metabolite detection and reduction in toxicityduring dye degradation. Unfortunately, the procedures usedfor detection of new or residual metabolites, as well as toxic-ity testing are highly nonuniform and differ greatly in theirlimit and range of detection. This may be because of the ab-sence of a specific legislation stating the most appropriatetests to be applied in different situations. It makes the corre-lation or comparison among different studies very difficult.Hence, another future development may be in the form ofuniformity in the metabolite detection and toxicity testingprocedures to improve the reproducibility, comparability, andsensitivity of results.

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