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Genotoxic effects of kraft pulp mill effluents treated by biological aerobic systems/Efectos genotoxicos de efluentes provenientes de celulosa kraft tratados por sistemas biologicos aerobicos/Efeito genotoxico de efluentes a partir de celulose kraft tratados por sistemas biologicos aerobicos.


Kraft mills are responsible for massive discharges of highly polluted effluents containing high COD concentration, and also exert toxicity on aquatic organisms. This toxic effect is generally related to the presence of abietic acid and sterols. The present work focuses on the search of a possible correlation between the presence of these compounds and the toxic effect of both untreated and treated bleached kraft mill effluents (BKME). An activated sludge system and an aerated lagoon, fed with BKME, were operated at organic loading rates (OLR) of 0.20, 0.40 and 0.60g COD/L x day, and the genotoxicity of both untreated and treated BKME was evaluated using the Bacillus subtilis 'rec' assay. The results indicate that toxicity of BKME could not be explained by the presence of abietic acid and sterols. Moreover, only a partial removal of the chronic toxicity could be achieved by the biological system used.


Los molinos de papel kraft son responsables de descargas masivas de efluentes altamente contaminantes con una alta demanda quimica de oxigeno (DQO), los cuales tambien son toxicos para organismos acuaticos. Este efecto toxico se relaciona generalmente con la presencia de acido abietico y esteroles. El presente trabajo se enfoca en la busqueda de una posible correlacion entre la presencia de estos compuestos y el efecto toxico de efluentes blanqueados de molinos de papel kraft (EBMK), bien sea tratados o no. Un sistema de lodos activados y una laguna de aeracion alimentados con EBMK fueron operados a niveles de carga organica de 0,20; 0,40 y 0,60g DQO/L x dia, y la genotoxicidad de los EBMK tratados o no fue evaluada utilizando el ensayo de Bacillus subtilis "rec (+/-)'. Los resultados indican que la toxicidad de los efluentes no puede ser explicada por la presencia de acido abiorico y esteroles. Mas aun, solo se logro una remocion parcial de la toxicidad con los sistemas biologicos utilizados.


Os moihnos de papel kraft sao responsaveis de descargas massivas de efluentes altamente contaminantes com uma alta demanda quimica de oxigenio (DQO), os quais tambem sao toxicos para organismos aquaticos. Este efeito toxico se relaciona geralmente com a presenca de acido abietico e esterois. O presente trabalho esta focado na procura de uma possivel correlacao entre a presenca destes compostos e o efeito toxico de efluentes de celulose branqueada de moihnos de papel kraft (EBMK), sejam tratados ou nao. Um sistema de lamas ativadas e uma lagoa de aeracao alimentados com EBMK foram operados a niveis de carga organica de 0,20; 0,40 e 0,60g DQO/L.dia, e a genotoxicidade dos EBMK tratados ou nao foi avaliada utilizando o ensaio de Baeillus subtilis "rec (+/-)'. Os resultados indicam que a toxicidade dos efluentes nao pode ser explicada pela presenca de acido abiotico e esterois. Mais ainda, somente se conseguiu uma remocao parcial da toxicidade com os sistemas biologicos utilizados.

KEYWORDS / Activated Sludge / Aerated Lagoon / Bacillus subtilis / Genotoxicity / Kraft Pulp Mill Effluent /

Received: 10/12/2009. Modified: 04/19/2011. Accepted: 04/25/2011.


Pulp mill effluents are characterized by their high concentrations of biochemical oxygen demand (up to 13.3g [BOD.sub.5]L), chemical oxygen demand (up to 39.8g COD/L) and suspended solids (up to 6.1g SS/L) (Bajpai, 2000) and their genotoxic effect on aquatic organisms (Salem et al., 1995; Gravato and Santos, 2002; Maria et al., 2003; Fernandez et al., 2007). In order to avoid the environmental effects of this kind of effluents, biological aerobic technologies such as activated sludge systems (AS) or aerated lagoons (AL) are widely used (Thompson et al., 2001; Chamorro et al., 2009; Xavier et al., 2009). Removal efficiencies >80% and >40% for [BOD.sub.5] and total COD, respectively, were reported for both technologies (Xavier et al., 2009) but their capacity to reduce genotoxicity was scarcely studied (Houk, 1992; Kostamo and Kukkonen, 2003; Xavier et al., 2009).

Some authors attribute the genotoxic effects mainly to resin acids (abietic and dehydroabietic acid; Fernandez et al., 2007) and sterols (Lehtinen et al., 1999) contained in the kraft mill effluents. For this reason, recent work has focused on the fate of these compounds during biological treatment (Chamorro et al., 2010a, b). Belmonte et al. (2006) and Chamorro et al. (2009) observed that 98% of the resin acids and 96% of stigmasterol were removed, respectively, when the pulp mill effluent was treated in an aerated lagoon. Kostamo and Kukkonen (2003) also found removal efficiencies >97% for resin acids and sterols in an activated sludge system. These authors detected that resin acids were mostly degraded, while sterols were removed by both biodegradation (41-67%) and absorption to sludge (31-57%).

The objective of this work is to study the capacity of an activated sludge system and an aerated lagoon to reduce the genotoxicity of kraft mill effluents and relate it to the removal efficiency of resin acids and sterols.

Materials and Methods

Raw wastewater

The effluent was obtained from a modern kraft mill located in Southern Chile, which bleaches softwood pulp of Pinus radiata using an elemental chlorine-free sequence. The kraft mill effluent was collected after a primary treatment and stored in the dark at 4 [+ or -] [degrees]C (Table I). The raw wastewater was supplemented with [(N[H.sub.4]).sub.2]S[O.sub.4] and K[H.sub.2]P[O.sub.4] as nitrogen and phosphate sources ([BOD.sub.5]:N:P = 100:5:1) and pH was adjusted to 7.0 [+ or -] 0.1.

Experimental set-up and operational strategy

An activated sludge reactor and an aerobic lagoon with a useful volume of 0.9L and a settling zone of 0.45L were used. Both systems were operated at dissolved oxygen (DO) concentration >2mg [O.sub.2]/L, room temperature and without pH control. Each reactor was inoculated with biomass from an industrial aerated lagoon treating BKME (5g VSS/L).

The AS and AL reactors were operated during 175 days (Table II). During this period, the organic loading rate (OLR) was increased stepwise from 0.20 to 0.60g COD/L x day by decreasing the hydraulic retention time (HRT). Removal efficiencies for COD, [BOD.sub.5], color, total phenolic compounds and lignin derived were measured for the AS and AL systems during these three different phases.

Genotoxicity determination

Genotoxicity of [beta]-sitosterol (0-32mg x [1.sup.-1]), stigmasterol (0-32mg x [1.sup.-1]), abietic acid (0-25mg x [1.sup.-1]), effluent (0-0.5mg. x [1.sup.-1]) and treated effluent (0-0.5mg x [1.sup.-1]) was determined by using Bacillus subtilis PB 1791 (rec-) and Bacillus subtilis PB 1652 (rec+) (Mazza, 1982). To test the toxic effects, stock solutions of [beta]-sitosterol (Calbiocem, 95%), stigmasterol (Sigma, 95%) and resin acid (Sigma, 99%) were prepared, while samples of effluent and treated effluent (pH= 7.0) were previously filtrated through a 0.45 [micro]m membrane and sterilized by using a filter syringe (0.20 [micro]m). All 'rec' assays were done in tubes containing 2ml of soft agar maintained on a dry batch at 45[degrees]C. Each experiment was performed in duplicate. Each tube was supplemented with: i) a sample of the tested compound or treated effluent, and ii) 0.1ml of a [10.sup.4] CFU/ml dilution of an overnight culture nutrient broth (Difco). Then, each tube was mixed in a vortex and distributed onto an agar plate surface. Plates were incubated at 37[degrees]C during 24h. Plate efficiency (A) is provided by the survival ratio (N/[N.sub.0]) of Bacillus subtilis rec- and Bacillus subtilis rec+ according to

A = [N.sub.rec-]/[N.sub.0]/[N.sub.rec+]/[N.sub.0]

where [N.sub.0]: reference bacterial growth, Nrec+: rec+ bacterial growth within different effluent or influent doses, and [N.sub.rec]: rec- bacterial growth within different effluent or influent doses. When A<1.0, the tested compound yields genotoxicity to the cells.

Statistix for Windows 2.2 software was used to evaluate sample variance analysis (ANOVA- Bonferroni test).

Analytical methods

Chemical oxygen demand (COD) and biological oxygen demand ([BOD.sub.5]) were measured following APHA (1985). The total phenolic compound (UV phenol) concentration was measured by UV absorbance in a 1cm quartz cell at 215nm, pH 8.0 (0.2M K[H.sub.2]P[O.sub.4] buffer), and then transformed to concentration using a calibration curve with phenol as a standard solution. Spectrophotometric measurements of filtered samples were principally performed at wavelengths of 440 (color), 346 (lignosulfonic acids), 254 (aromatic compounds) and 280 (lignin derived compounds) in a 1x1cm quartz cell using a Genesys UVVIS spectrophotometer, and were determined according to the Chamorro et al. (2005) procedure. COD, [BOD.sub.5] color, total phenolic compounds and resin acid were measured after membrane (0.45 [micro]m) filtration.


Analyses of resin acid were performed by liquid chromatography using an HPLC system (Shimadzu model LC-10 ATVP, Kyoto, Japan) coupled to a mass spectrometry detector (DAD Shimadzu model SPDM 10 AVP). Liquid samples were extracted with dichloromethane using the procedure developed by Li et al. (1996). Extracts were evaporated to ~5ml using a rotary evaporator. Of the sample, 20[micro]l were injected in an RP18-Lichrospher-60 column (Darmstadt, Germany) thermostated at 20[degrees]C. The liquid phase was methanol:water (70:30, v/v) at a flow rate of 1ml x [min.sup.-1]. Calibration was performed according to Latorre et al. (2003). [beta]-sitosterol and stigmasterol were determined according to the analytical method described by Cook et al. (1997).



Removal of organic compounds

Figure 1 shows the average removal of COD, [BOD.sub.5], phenolic compounds ([UV.sub.215]) and color ([VIS.sub.440]) during the three successive operation phases. The activated sludge system achieved a COD removal efficiency of 63.3 [+ or -] 10.3% which was slightly higher than that obtained by the aerated lagoon (57.1 [+ or -] 7.1%). However, [BOD.sub.5] removal was similar in both reactors, with values up to 99.2 [+ or -] 0.2%. The fate of total phenolic compounds was very different in both systems. A low degradation was observed in the aerated lagoon while generation of these compounds was detected in the AS reactor. Color removal was higher in the activated sludge reactor but decreased when the OLR was increased to 0.6g COD/L x day.

Removal efficiencies of aromatic compounds ([UV.sub.254]) and lignin derivatives ([UV.sub.272] and [UV.sub.280]) were between 20-40% during whole operation period for both systems, AS being slightly more efficient than AL (Figure 2). A decrease of ligno-sulfonic acid ([VIS.sub.346]) removal efficiency was observed when the OLR was increased to 0.6g

COD/L x day. Both the activated sludge system and the aerated lagoon were able to totally remove abietic acid. However, removal of sterols only achieved an efficiency of ~100% in the AS reactor, the AL system reaching an efficiency of 40%.

Genotoxicity removal

Firstly, the genotoxic effects of different concentrations of [beta]-sitosterol, stigmasterol and abietic acid were , determined (Table III). Stigmasterol caused genotoxicity at the lower concentration assayed, while [beta]-sitosterol and abietic acid show a clear genotoxic effect at concentrations higher than 8 and 15mg x [1.sup.-1], respectively. Table IV shows the efficiency of plate values of the effluent and the treated effluent when the systems operated at OLRs of 0.2 and 0.6g COD/ L x day. Only the AS reactor was able to achieve a partial removal of genotoxicity (A values close to 1) when operated at 0.2g COD/L x day. At this OLR, the effluent of the aerated lagoon still presented citotoxic effects at all the doses tested but it was lower than that exerted by the BKME. Nevertheless, when an OLR of 0.6g COD/ L x day was applied to both systems, an increase of genotoxicity was observed during the aerobic treatment, this increase being higher for the aerated lagoon. This fact could be explained by the generation of intermediate products during biodegradation that may be more toxic than the compounds contained in the kraft mill effluents (Kostamo et al., 2004).


Both systems tested achieved COD and BOD5 removal efficiencies ~60 and 99%, respectively, which are similar to values reported for this kind of systems (Pokhrel and Viraraghavan, 2004) and for aerobic moving bed bioreactors (Villamar et al., 2009), although for this type of effluents removal of COD may be improved up to values higher than 90% by using SBR systems (Tsang et al., 2007). The performance of both systems was quite different with regards to the degradation of total phenolic compounds: while the aerated lagoon, in general, removed only slightly these compounds, the activated sludge system generated them. This tendency was also observed by Xavier et al. (2009). However, the fate of total phenolic compounds could be more affected by the operational conditions than by the technology applied (Belmonte et al., 2006, Villamar et al., 2009). Color in pulp and paper mills is largely due to lignin and lignin derivates. For this reason, the poor removal of color could relate to the resistance of these compounds to be biodegraded. In fact, similar profiles were observed for color and lignosulfonic acid ([VIS.sub.346]) (Figures 1d and 2d).

The high efficiencies of abietic acid removal obtained in this work agree with those found by other authors using either aerobic lagoons (Zender et al., 1994; Belmonte et al., 2006) or activated sludge reactors (Kostamo and Kukkonen, 2003). Sterols were completely removed when the effluent was treated in the activated sludge reactor, as was also found by Kostamo et al. (2004), but a removal of only 40% was achieved by the aerated lagoon. Fernandez et al. (2007) also found that both aerated lagoons and trickling filters showed a lower capacity than activated sludge systems to remove sterols.

In this work, an increase of the genotoxic effect was observed in the treated effluent. This was also found by Chamorro et al. (2009), who evaluated the acute toxicity, using Daphnia obtuse, of both raw and treated (with an aerated lagoon) kraft mill effluents. Similar results were also obtained by Pintar et al. (2004) when they treated this kind of wastewater by catalytic wet-air oxidation and found that the end product solutions were all more toxic to Daphnia magna than the starting effluents by factors ranging from 2 to 33, although the TOC removal efficiency achieved was ~95%.

This means that intermediate products even more toxic than the original compounds could be generated during aerobic biodegradation (Pintar et al., 2004). For example, resin acids are not mineralized by aerobic bacteria, but only transformed into forms like decarboxylated resin acid hydrocarbons, or oxygenated resin acids or retene (Zender et al., 1994). Similar results have been observed for sterols (Mattsson et al., 2001).

On the other hand, the genotoxic effects of the kraft mill effluent were higher than those obtained from assays with solutions containing similar concentrations of sterols and resin acid. Therefore, these genotoxic effects may not be directly associated to such compounds. In fact, the treated effluent contains lower concentrations of sterols and resin acid than the raw effluent but its toxicity is higher. This agrees with results obtained by Chamorro et al. (2009), who observed an increase of toxicity after the biological treatment, in spite of the fact that their system removed 96% of the inlet stigmasterol. Moreover, Chamorro et al. (2010b) showed that a biological system treating Pinus radiata kraft mill effluent was able to remove 80-83% of estrogenic activity at HRTs of 1 and 2 days.

The use of either activated sludge system and aerated lagoon appear not to be efficient systems to remove chronic toxicity. Therefore, the use of hybrid systems (Kennedy et al., 2000) or a post-treatment of the kraft mill effluent, such as ozonation (Yeber et al., 1999) or activated carbon (Reyes et al., 2009), is recommended.


The activated sludge system and aerated lagoon was able to remove COD and [BOD.sub.5] around 60% and 99%, respectively. Only the activated sludge reactor was able to achieve a partial removal of genotoxicity which was operated at 0.2g COD/L x day. The results indicate that toxicity of BKME could not be explained by the presence of abietic acid and sterols.


This work was supported by FONDECYT grant 1070509. Jose L. Campos thanks Direccion de Investigacion (UDEC) of the Universidad de Concepcion, Chile, for supporting his stay at the Environmental Science Center EULA-Chile.


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Claudia R. Xavier. Doctor in Environmental Science, Universidad de Concepcion (UDEC), Chile. Professor, Universidade Tecnologica Federal do Parama, Brazil.

Elizabeth Onate. M.Sc. Student in Chemical Engineering, UDEC, Chile.

Maria A. Mondaca. Doctor in Biological Sciences, UC, Chile. Professor, UDEC, Chicle

Jose L. Campos. Doctor in Chemical Science, Universidad de Santiago de Compostela (USC), Spain. Professor, USC, Spain.

Gladys Vidal. Doctor in Chemical Science, USC, Spain. Professor, UDEC, Chile. Address: Environmental Science Center, EULA-Chile, UDEC, Chile. P.O. Box 160-C. Concepcion, Chile. e-mail: glvidal


Parameter                                               Value

pH                                                3.4 [+ or -] 0.2
COD (mg x [l.sup.-1])                           881.5 [+ or -] 24.3
BODS (mg x [l.sup.-1])                          300.5 [+ or -] 9.5
Total phenolic compounds                        271.9 [+ or -] 14.2
  ([UV.sub.215]) (mg x [l.sup.-1])
Color ([VIS.sub.440]) (1 x 1cm)                  0.41 [+ or -] 0.01
Aromatic compounds ([UV.sub.254]) (1 x 1cm)      6.69 [+ or -] 0.07
Lignin derived ([UV.sub.272]) (1 x 1cm)          5.90 [+ or -] 0.08
Lignin derived ([UV.sub.280]) (1 x 1cm)          5.37 [+ or -] 0.06
Lignosulphonic acid ([VIS.sub.346]) (1 x 1cm)    1.73 [+ or -] 0.04
Resin acid (abietic acid) (mg x [l.sup.-1])      1.45 [+ or -] 0.93
[beta]-sitosterol (mg x [l.sup.-1])              0.33 [+ or -] 0.03
Stigmasterol (mg x [l.sup.-1])                   0.07 [+ or -] 0.01



Phase     Operation         OLR         HRT
         time (days)   (g COD/L-day)   (days)

I           0-87           0.20         4.4
II         88-108          0.40         2.2
III       109-175          0.60         1.1



(mg [l.sup.-1])         [beta]-
                       sitosterol         Estigmasterol

       0           1.00 [+ or -] 0.00   1.00 [+ or -] 0.00
       1           1.10 [+ or -] 0.02   0.54 [+ or -] 0.10
       2           1.17 [+ or -] 0.58   0.67 [+ or -] 0.10
       4           1.28 [+ or -] 1.06   0.72 [+ or -] 0.03
       5                  - *                   -
       8           0.93 [+ or -] 1.03   0.68 [+ or -] 0.05
       15                  -                    -
       16          0.81 [+ or -] 0.17   0.80 [+ or -] 0.28
       25                  -                    -
       32          0.44 [+ or -] 0.96   0.72 [+ or -] 0.07

(mg [l.sup.-1])       Abietic acid

       0           1.00 [+ or -] 0.00
       1           1.12 [+ or -] 0.15
       2                   -
       4                   -
       5                   -
       8                   -
       15          0.95 [+ or -] 0.26
       16                  -
       25          0.80 [+ or -] 0.09
       32                  -

* Genotoxicity was not determined at this concentration.



                 Efficiency of plate (A) value
(g COD/   Dose        Kraft mill
L-day)    (ml)         effluent             AS effluent

  0.2     0.1    1.017 [+ or -] 0.052   0.971 [+ or -] 0.156
          0.3    0.828 [+ or -] 0.017   0.925 [+ or -] 0.166
          0.5    0.792 [+ or -] 0.132   1.188 [+ or -] 0.029

  0.6     0.1    1.017 [+ or -] 0.052   0.731 [+ or -] 0.020
          0.3    0.828 [+ or -] 0.017   0.880 [+ or -] 0.085
          0.5    0.792 [+ or -] 0.132   0.692 [+ or -] 0.144

                 Efficiency of plate
  OLR                 (A) value
(g COD/   Dose
L-day)    (ml)       AL effluent

  0.2     0.1    0.887 [+ or -] 0.290
          0.3    0.881 [+ or -] 0.092
          0.5    0.893 [+ or -] 0.100

  0.6     0.1    0.561 [+ or -] 0.116
          0.3    0.639 [+ or -] 0.136
          0.5    0.740 [+ or -] 0.196
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Author:Xavier, Claudia R.; Onate, Elizabeth; Mondaca, Maria A.; Campos, Jose L.; Vidal, Gladys
Date:Jun 1, 2011
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