Waste Management 38 (2015) 312320

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Waste Management
journal homepage: www.elsevier.com/locate/wasman

Sewage sludge composting in a two-stage system: Carbon and nitrogen

transformations and potential ecological risk assessment
Dorota Kulikowska , Zygmunt M. Gusiatin
University of Warmia and Mazury in Olsztyn, Department of Environmental Biotechnology, Soneczna St. 45G, 10-709 Olsztyn, Poland

a r t i c l e

i n f o

Article history:
Received 22 September 2014
Accepted 16 December 2014
Available online 17 January 2015
Keywords:
Sewage sludge composting
Two-stage system
Aeration rate
Organics removal kinetics
Er, MF, IR indices

a b s t r a c t
The study examined how aeration rate (AR) in bioreactor (1.0 and 0.5 l/min kg dm) at low C/N ratio
(ca. 1516) affected kinetics of organic matter (OM) removal, i.e. rate constant of OM removal (k) and
maximum degradation of OM (A) and nitrogen evolution during sewage sludge composting. Moreover,
potential ecological risk (Er) based on metal (Cd, Cr, Cu, Hg, Ni, Pb, Zn) content was evaluated. The process
involved a two-stage system (bioreactor and windrow). In the bioreactor, at higher AR, k and A equaled
0.34 d1 and 101.9 g/kg dm, respectively; at lower AR k was 0.38 d1, however A 1.4-fold lower. Interestingly, in the windrow, k was much higher (0.086 d1) for the biomass subjected to a lower AR, compared
to 0.026 d1 at higher AR. Moreover, although at lower AR, k in the windrow was 4.4-fold lower than in
the bioreactor, A was 1.15-fold higher. Total N content in mature compost was on the level 23.5122.35 g/
kg dm and metal concentration showed low ecological risk (Er < 16).
2014 Elsevier Ltd. All rights reserved.

1. Introduction
An important strategy for recycling organic waste, e.g. sewage
sludge, is their use in agriculture as fertilizer or to reclaim soil.
However, before organic wastes are applied to the soil, they must
be subjected to appropriate treatments. One of these is composting. The main purposes of this process are to: (i) reduce mass
and volume of the sewage sludge, (ii) destroy pathogens and weed
seeds present in the substrate, (iii) reduce and or even eliminate
inorganic and organic pollutants, and (iv) obtain mature and stabilized organic material (Senesi et al., 2007). The process also provides nutrient conservation and carbon recycling. An overview of
compost qualities is presented in ECN (European Compost
Network, 2010, 2011).
The use of compost in eld applications is mainly limited by its
total heavy metal (HM) content and by these metals bioavailability
or mobility. It is known, that the mobility of HMs, their bioavailability and related eco-toxicity to plants depend strongly on their
specic chemical fractions or ways of binding rather than total
metal concentration (Fuentes et al., 2006; Gupta and Sinha,
2007). Therefore, it is important to analyze not only total HMs content but also estimate the metal distribution and ecological risk of
Abbreviations: Er, potential ecological risk factor; MF, mobility factor; IR, reduced
partition index.
Corresponding author. Tel.: +48 89 5234145; fax: +48 89 5234131.
E-mail address: dorotak@uwm.edu.pl (D. Kulikowska).
http://dx.doi.org/10.1016/j.wasman.2014.12.019
0956-053X/ 2014 Elsevier Ltd. All rights reserved.

heavy metals in sewage sludge composts (Gusiatin and

Kulikowska, 2014).
Composting proceeds in two phases, mineralization and humication. In the rst step degradation of readily biodegradable compounds occurs, and the process range and rate depends on the type
of composted waste and the operational conditions. For effective
composting, adequate parameters such as temperature, moisture
and C/N ratio should be controlled. Moreover, for effective mineralization of organics oxygen must be also delivered.
Oxygen can be supplied to the composting biomass by forced or
passive aeration. It is important to remember that composting proceeds under moist conditions, and that oxygen diffuses much more
slowly through water than through air. This means that regardless
of the aeration method, the amount of the air that is being supplied
does not necessarily reect the amount of oxygen that is actually
reaching the microorganisms. Therefore, even though that theoretically oxidation of 1 g of organic matter needs 1.5 g of oxygen, in
practice, more air is required to evaporate excess water, remove
gases and prevent overheating. According to Rynk (1992), the
amount of air needed to remove water is 6 times higher than that
needed to maintain the activity of the microorganisms; the amount
needed to remove excess heat is 16 times higher.
So far, the most commonly used aeration systems are turned
windrow and forced aeration. The effects of both aeration strategies on organics removal efciency and compost quality have been
reviewed, and it has been proved that both systems are effective in

D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

composting of organic waste (Brewer and Sullivan, 2003). Different

aeration systems mainly affected the temperature prole, organics
removal efciency and composting duration needed to obtain
mature compost. So far, these kinds of research were performed
for many types of waste, e.g. pig litter with sawdust (Tiquia and
Tam, 1998), sheep manure with straw (Solano et al., 2001), vinasse
waste with cotton waste (Diaz et al., 2002), and olive oil husks
(Baeta-Hall et al., 2005). It is worth emphasizing that due to different type of composted waste, the optimal amount of air required
was different. Because aeration rate obviously inuences composting process efciency, air amount is one of the most important
parameters to be optimized. Although the composting processes
may be conducted in windrows or bioreactors, most studies have
focused on composting in windrows supplied with oxygen by
mechanical turning or forced aeration. Despite the benets of composting in bioreactors, only a limited number of investigations
have dealt with composting using this technology (Yamada and
Kawase, 2006). In contrast, there is no information available on
process efciency during composting in a two-stage system consisting of an aerated bioreactor and a periodically turned windrow.
Specically, there is a lack of knowledge about the kinetic parameters of organic matter degradation in each step of composting,
although the prediction of aeration requirements is necessary for
a better design of composting plants. It is especially important
for composting of sewage sludge characterizing by low C/N ratio.
Although it is common that sewage sludge is mixed with lignocellulosic materials, composting is often conducted below optimal C/
N. When the C/N ratio is low, nitrogen may be lost from the system
as ammonia. As conservation of nitrogen in the composted biomass
is one of the objectives of composting, it is also important to check
how aeration intensities inuence nitrogen dynamics at low C/N
ratio. The impact of technological parameters of composting,
including aeration intensity, on nitrogen dynamics has been studied a little and for other waste than sewage sludge, i.e. dairy manure (Li et al., 2008), legume trimmings residues (Bueno et al., 2008;
Cabeza et al., 2013) and household waste, separated pig solids,
food waste, pig slaughterhouse sludge and green algae (de
Guardia et al., 2010).
Therefore, the primary objective of this study was to determine
how aeration rate affects the efciency and kinetics of organic matter removal during sewage sludge composting in a two-stage system and at low C/N ratio. In addition, nitrogen losses and
environmental risk for composts based on total metal contents
and their toxicity (as potential ecological risk factor, Er) and metal
distribution (as mobility factor, MF and reduced partition index, IR)
have been evaluated.

2. Materials and methods

2.1. Feeding materials and composting process design
Excess sewage sludge was collected from a municipal wastewater treatment plant (WWTP) working as SBR system. The WWTP
was designed for an average daily ow rate of wastewater on the
level 4200 m3/d and works with a mechanical-biological system.
The WWTP was operated with the following technological parameters: MLSS 5140 (412 mg/l; MLVSS 3870 240 mg/l; DO during
aeration phase of 34 mg/l; DO during anoxic phase about
0.5 mg/l, and a SRT of 22 3 d.
Because of high moisture (88% after dewatering on lter press
with polyelectrolyte) and low C/N ratio (6.4), the sludge was mixed
with other materials (wood chips, grass, rape straw). In the feedstock the proportions of individual components was as follows:
sewage sludge 60% (w/w), wood chips 20% (w/w), grass 15% (w/w),

313

rape straw 2% (w/w) and inoculant (mature compost from the

previous series) 3% (w/w). The total mass of composted feedstock
was ca. 500 kg.
Two series, differed in aeration rates (AR, dened as amount of
air (in liters) delivered to bioreactor per minute and per kilogram
of dry mass of the feedstock) in bioreactor, were performed. In
series 1, AR was 1.0 l/min kg dm; and in series 2, 0.5 l/min kg dm.
These values were selected on the basis of previous research of
the author (11.5 l/min kg dm; Kulikowska and Klimiuk, 2011)
and other works, in which authors suggested lower aeration rates
(Li et al., 2008; Guo et al., 2012).
The feedstock characteristics in both series are shown in
Table 1.
The composting process was conducted in a two-stage system:
the rst stage was an aerated bioreactor (1 m3; air was introduced
with ventilator); and the second, a periodically (weekly) turned
windrow. The bioreactor was equipped with an aerated system
that enabled regulation of air supply quantity. Air was pumping
from the ventilator to the aeration box, constituting the platform
oor of the bioreactor. More details about the bioreactor were presented in paper of Kulikowska and Klimiuk (2011).
Composting system was placed at technological laboratory; the
ambient temperature was on the level of 202 C. The composting
process lasted 180 days: 10 days in the bioreactor 170 days in the
windrow.
2.2. Analytical methods
Samples of composted materials were collected in accordance
with the Polish standard (PN-Z-15011-1:1998). Primary samples
(3 samples, 1.5 kg each, taken from the top to the bottom of the
bioreactor/windrow) were thoroughly mixed to obtain average
sample. In order to reduce volume of the average sample, it was
piled up in the shape of a pyramid with a square base. Then, the
sample was divided with diagonals into 4 parts. Two opposite parts
were discarded and the remaining two opposite were mixed. The
samples were dried at 105 C and grinded to a diameter of
0.5 mm using a Retsch SM 100 mill.
Composted materials were sampled at the following intervals:
0, 1, 2, 4, 6, 8 and 10 day during composting in bioreactor and at
0, 3, 10, 13, 24, 36, 46, 62, 81, 103, 125, 149 and 170 day of composting in windrow.
Total organic matter (OM, dened as content of organic matter
in whole dry mass of the feedstock/compost) was determined by
ignition of the samples at 550 C (PN-Z-15011-3:2001), total N by
the Kjeldahl method (PN-Z-15011-3:2001) and total organic carbon (TOC) using Shimadzu Liquid TOCVCSN analyzer. In water
extracts from composts, the ammonium nitrogen (PN-C-0457615:1975), nitrite nitrogen (PN-C-04576-06:1973) and nitrate nitrogen (PN-C-04576-08:1982) were determined.
To determine total metal (Cd, Cu, Cr, Hg, Ni, Pb, Zn) concentration in the feedstock and composts, the samples dried previously at
105 C were digested in a microwave oven (MARSXpress, CEM,
USA) using a HCl:HNO3 mixture at a 3:1 ratio (v/v) and 2 ml of
30% H2O2 at one-stage microwave program (T = 170 C,
P = 900 W, t = 30 min.). After cooling, the extracts were ltrated
through Whatman 42 lter papers and analyzed by atomic absorption spectrometer (Varian AA280FS, Australia). For preparation of
calibration curves, stock standard solutions of a given metal were
purchased from SigmaAldrich Co. (Poland).
In the feedstock and mature composts, selected metals (Cu, Cr,
Ni, Pb, Zn) were fractionated into four chemical fractions:
exchangeable and acid soluble (F1), reducible (F2), oxidizable
(F3) and residual (F4) using a modied BCR sequential extraction
procedure (Pueyo et al., 2008).

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D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

Table 1
Feedstock characteristic in series 1 and 2 (variation coefcient expressed as percentage in brackets).
Series no.

pH

Moisture (%)

Organic matter OM (g/kg dm)

TOC (g/kg dm)

N (g/kg dm)

OM/N

C/N

1
2

7.36 (0.4)
7.45 (0.4)

69.5 (0.3)
68.2 (0.6)

684.1 (2.0)
623.1 (2.0)

345.3 (0.7)
349.2 (0.8)

22.8 (1.0)
21.9 (2.0)

30.0
28.5

15.1
15.9

2.3. Mathematical formulae

Er T ir 

Loss of organic matter (OM) during composting (OM removal

efciency) was calculated according to the equation given by
Paredes et al. (2000):

Ci
C in

The kinetics of OM degradation was calculated with the rstorder kinetic equation:

where:
F1, F2, F3, F4 exchangeable and acid soluble (F1), reducible
(F2), oxidizable (F3), residual (F4) metal fractions based on the
BCR sequential extraction procedure.
i the index number of the extraction step, progressing from 1
(for the weakest) to the strongest extractant (in the BCR procedure, k = 4).
Fi the percentage of a particular metal present in fraction i.
Tri toxic-response factor for a given metal (Zn = 1; Cr = 2; Cu,
Ni and Pb = 5; Cd = 30, Hg = 40) (Hakanson, 1980).
Ci total metal concentration in compost.
Cin a reference value for the metal referring to threshold limits
in compost according to Polish legislative.

OMloss A  ekt

3. Results and discussion

EOM;loss 100  100

X 1 100  X 2 
X 2 100  X 1 

where:
EOM,loss OM removal efciency (%).
X1 ash concentration in the feedstock (%).
X2 ash concentration during composting (%).

where:
A the maximum degradation of OM in the composted material
(g/kg dm).
k the rate constant of degradation of OM in the composted
material (d1).
t composting time (d).
Both parameters, i.e. A and k were calculated using STATISTICA 9.0
(StatSoft, Inc.).
Loss of N during composting was calculated according to the
equation given by Cayuela et al. (2006):


Nloss 100  100 

X 1  N2
X 2  N1


3

where:
Nloss N loss (%).
X1 initial ash concentration (%).
X2 nal ash concentration (%).
N1 initial total N concentration (%).
N2 nal total N concentration (%).
Although total metal concentrations may indicate the overall
level of metals in compost, it is generally recognized that the specic chemical forms of a metal determine its mobility, bioavailability and related eco-toxicity to plants. To describe the composts
ecological quality, calculation methods can be adopted, the same
as for soils and sediments contaminated with heavy metals. The
most important parameters to consider are mobility factor (MF),
the reduced partition index (IR), and the potential ecological risk
factor (Er). These parameters are described with the following
equations:

MF

IR

F1
 100%
F1 F2 F3 F4

k
X
2
2
i F i =k
i1

3.1. Organic matter removal and temperature evolution

Many biodegradable wastes can be composted alone if they
have the proper physical and chemical properties. However, it is
more commonly done with other materials (additives) playing a
role as amendments and bulking agents. In the case of sewage
sludge, owing to its low porosity, high moisture and low C/N ratio,
it is necessary to add other waste, which provide structure and
porosity (bulking agents) and improve moisture and C/N ratio
(amendments). This is important because the latter two parameters, apart from oxygen, are the most important factors for efcient
composting process.
It is known that moisture content for composting must be a
compromise between achieving adequate water content for microorganisms to move and transport nutrients, and adequate oxygen
ow to maintain aerobic conditions. The moisture content for composting is generally recommended to be between 40% and 60%. The
second factor, which has the largest effect on the composting process, is the C/N ratio as carbon and nitrogen are the main nutrients.
If these nutrients are present at the proper ratio, the other nutrients also tend to be present in acceptable amounts. An initial C/N
ratio of 2030/1 is recommended for rapid composting.
Mixing of sewage sludge with materials of lower moisture and
lower N reduced the moisture content and increased the C/N ratio
in the feedstock. However, despite mixing of sewage sludge with
additives, both moisture and C/N ratio differed from the values
considered as optimal for composting. It is commonly practiced
that for waste with high moisture and a low C/N ratio, like sewage
sludge, the composting process is conducted at higher moisture
content and a lower C/N content than those considered as optimal.
This results in reduction of the amount of amendments normally
used as co-composting materials. Although optimal conditions
may work more efciently, they require large amounts of additives
(such as wood chips, straw or grass), which in turn reduces the
quantity of sewage sludge and inuences economy of composting
process.
It should be noticed that despite identical proportions of components, organic matter content in the feedstock differed and
equaled 684.1 g/kg dm and 623.1 g/kg dm (Table 1). This resulted

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D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

mainly from the changeable organic matter concentrations in the

sewage sludge used in the individual series.
In the present study, a rapid increase of temperature was
observed in both series (Fig. 1). This means that easily biodegradable organic compounds were intensively decomposed. This process is accompanied by the generation of large amounts of heat
and is typical for the initial phase of composting.
By measuring the temperature in the composting material
(Fig. 1a and b), it was shown that in series 1, the temperature
exceeded 45 C after 1 day of composting, while in series 2, it
reached 56 C already within 12 h of the process. Therefore, it
can be concluded that the very rapid increase of temperature and
the resulting lack of a mesophilic phase in the second case was
the result of the low aeration rate.
The temperature proles also show that in series 1, the temperature did not exceed 69 C. In series 2, the composting material
was overheated, sustaining temperatures of 7879 C for 3 consecutive days. The large rise in temperature in series 2 may be connected with the fact that the amount of air needed to remove
excess heat is much higher than that needed to maintain the activity of the microorganisms (Rynk, 1992). However, according to de
Guardia et al. (2012) too low aeration rates limited O2 supply and
thus, the biodegradation rate, while led to heat accumulation. This
may have occurred in our study, as OM removal rate (r) in bioreactor in series 2 was 28.44 g/d kg dm and was lower than in series 1
(34.64 g/d kg dm) (see: Kinetics of organics removal).
de Guardia et al. (2012) showed also that evaporation and surface convection were the highest contributors to heat losses,
whereas conduction and sensible convection were the lowest.
Moreover, heat losses by evaporation increased with increase of
the aeration rate. Similarly, Ahn et al. (2007) proved that the
amount of evaporated water from the high-ow reactor was 37
60% more than from the low-ow reactor (this led to decrease of
moisture content from 62% in the feedstock to 4147% after
12 days). However, in our study decrease in moisture content
was not observed.
During composting in windrows, in series 2, the temperature
increased again, prolonging the thermophilic phase for another
28 days. Therefore, in this experiment, the thermophilic phase
was 1.8-fold longer than in series 1 (16 days).
Therefore, the present study shows that the intensity of aeration affects both the length of the thermophilic phase and the maximum temperature. Although the relationship between the
aeration strategy/aeration rate and the temperature prole during
composting of different waste has been the subject of numerous
studies, the results are not conclusive. Gao et al. (2010a) during
composting of chicken manure with sawdust in an aerated bioreactor, have shown that an increase in aeration rate from 18 l/h kg OM
to 30 l/h kg OM had only a small effect on the length of the thermophilic phase and the maximum temperature of the process. These

(a) bioreactor

were 65 C and 9 days (18 l/h kg OM) and 68 C and 8 days (30 l/
h kg OM), respectively. A further increase in aeration rate to 42 l/
h kg OM caused cooling; the maximum temperature did not
exceed 60 C and the duration of thermophilic phase was only
5 days, at which temperatures exceeded 55 C only for 2 days. On
the contrary, research by de Guardia et al. (2008) has shown that
the maximum temperature during composting rises with increases
in aeration rate. At aeration rate of 1.69 l/h kg dm, the maximum
temperature did not exceed 50 C. At 3.2 l/h kg dm it increased to
62 C, while in range of 8.4816.63 l/h kg dm, it exceeded 67 C.
These discrepancies may be because of two factors: (i) in both
cases tested range of aeration rate was different, (ii) optimal aeration rate depended on the type of composted waste. Aeration at
lower or higher intensity than that considered optimal, may result
in overheating or excessive cooling. This means that the optimum
amount of introduced air for composting a particular kind of waste
should be determined experimentally. However, other authors
have proven that temperature proles depend not only on aeration
rate but also on type of bulking agents and ratio between waste
and bulking agents as they both may increase the amount of biodegradable organics in the feedstock and C/N ratio. Gao et al. (2010b)
analyzed temperature proles during composting chicken manure
with sawdust at proportions of 16.3:1, 6.9:1 and 3.4:1, yielding initial C/N ratios of 12, 18 and 28, respectively. The thermophilic
phase of composting mixture with initial C/N ratio of 12 and 18
was shorter than composting mixture with initial C/N ratio of 28.
This was attributed to insufcient of carbon source of the low C/N.
The main requirement for the use of compost in agriculture is
its sanitary safety, which means that there must be no pathogenic
bacteria of the genus Salmonella, live eggs of parasites (Ascaris sp.,
Trichuris sp., Toxocara sp.) or weed seeds. As the temperature
required to destroy the pathogens is at least 55 C, and weed seeds
should be above 60 C, in most cases the temperature during the
thermophilic phase of composting makes the feedstock completely
hygienic (Haug, 1993). However, it is known that not only height of
temperature but also duration of high temperature is important.
For example, according to guidelines contained in ECN (European
Compost Network, 2011) for stabilization and pathogen/weed seed
inactivation purposes, proposed time-temperature proles are:
65 C or more for at least 5 days, 60 C or more for at least 7 days
and 55 C or more for at least 14 days. In the present study, during
the thermophilic phase, the temperature was higher than 65 C for
several subsequent days, which was sufcient to destroy the
pathogens and weed seeds in the compost. However, it is worth
emphasizing that before composting in the present study, the
dewatered sewage sludge already contained no bacteria of Salmonella spp. or eggs of parasites of Ascaris sp., Trichuris sp., Toxocara
sp. Similarly, Jasiewicz et al. (2007) noted that in sewage sludge
from wastewater treatment plant in Olecko Salmonella bacillus or
_
parasite eggs were not found. However, when Bozek
and Kapec

(b) windrow
90

temperature [oC]

temperature [oC]

90
70
50
30
10

70
50
30
10

composting duration [d]

series 1

series 2

10

20

40

60

80

100

120

140

composting duration [d]

series 1

series 2

Fig. 1. Temperature proles during sewage sludge composting. (a) Bioreactor, and (b) windrow.

160

180

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D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

(a) bioreactor

(b) windrow
OM removal efficiency [%]

shown). Because HS and HA content is one of the parameters of

compost quality, it should be emphasizing that higher aeration
intensity in bioreactor increases HS and HA concentration in the
nal product. It is connected with the fact that aeration intensity
in the bioreactor inuenced the temperature in the composting
biomass, which in turn affected the formation of HS, especially HA.
The kinetic parameters of OM degradation was calculated from
Eq. (2). Fitting of kinetic equations to mineralization curves
enables to calculate the fraction of potentially mineralizable organics in composted material and its mineralization rate. In the present study, during 10 d of composting in the bioreactor, at an
aeration rates of 1 l/min kg dm and 0.5 l/min kg dm, maximum
degradation of OM (A) were 101.87 g/kg dm and 74.84 g/kg dm
(Fig. 3a, Table 2), respectively. As the amount of air needed to
remove excess heat from the composted mass is about 16-fold
higher than that required for maintaining the activity of microorganisms (Rynk, 1992), the lower degradation of OM at lower aeration rate was probably because of the temperature prole during
composting; overheating at this aeration rate may have had a disadvantageous effect on the activity of microorganisms. This is more
likely that during composting there was no excessive drying and
moisture content in both series remained on the similar level
(6062%).
In the windrow in series 1, the maximum degradation of OM (A)
was 65.88 g/kg dm, about 1.5 times less than in the bioreactor.
However, in series 2 it was 85.34 g/kg dm (about 1.1 times more
than in the bioreactor) (Fig. 3b). In the windrow, in series 2, the
higher A could have been related to the higher temperatures and
the prolonged thermophilic phase, which was almost twice as long
as in the windrow in series 1.
The rate constants for organics degradation (k) in the bioreactor
were 0.34 d1 and 0.38 d1 at 1 l/min kg dm and 0.5 l/min kg dm,
respectively (Table 2). However, considerable differences in the
maximum degradation of OM between series (A, described earlier)
(Table 2) caused the rate of OM degradation (r) at aeration rate 1 l/
min kg dm to be higher (34.64 g/d kg dm) than at aeration rate of
0.5 l/min kg dm (28.44 g/d kg dm). During composting in the windrow, both k and r were an order of magnitude lower than in the bioreactor. In the windrow, after lower intensity of aeration, the rate
constant k and the rate of degradation of organic matter r were,
however, both much higher (Table 2). This means that at lower aeration rate, removal of organic matter also occurred in the windrow.
Although data concerning organic matter removal during composting of different waste have been the subject of numerous studies, investigations on process kinetics are rare. However, these data
are extremely important for process design, especially when estimating retention time of feedstock in a bioreactor. The small
amount of data available in the literature concerns composting of
agro-industrial waste.

OM removal efficiency [%]

(2008) examined 110 samples of sewage sludge, Salmonella were

isolated from 9 samples (8.2%), and the eggs of helminthes from
31 samples (28.1%). In that study, the eggs of Ascaris spp. were
detected in 24 samples of sewage sludge (21.8%), followed by
Trichuris spp. eggs in 11 samples (10.0%), and Toxocara spp. eggs
in 6 samples (5.4%).
Loss of OM was calculated from Eq. (1). In the literature concerning the mineralization of sludge under aerobic conditions, this
equation is often known as the Rawn and Bant module and is identical to the fermentation module. In the present study, EOM,loss values obtained in series 1 and 2 are presented in Fig. 2. From these
data it can be concluded that in the bioreactor, the larger process
efciency was observed at series 1; in the windrow higher EOM,loss
was noticed in series 2. However, the overall efciency of OM
removal (as sum of EOM,loss in the 1st and 2nd stage of composting)
was similar (ca. 5859%) in both series. Moreover, it is worth noticing that in both series, the nal process efciency was much higher
in comparison with other authors who composted anaerobically
digested sewage sludge (Hernandez et al., 2006; Ponsa et al.,
2009). However, some authors indicate high efciency of OM
removal during composting other kind of waste. According to
Kulcu and Yaldiz (2004), OM removal during composting of garden
waste ranged between 42% and 58%, whereas for goat manure and
wheat straw it was higher than 72% (Kulcu and Yaldiz, 2007). Similarly, high values of OM removal during composting different mixtures or organic waste rich in N with industrial waste were
obtained by Paredes et al. (2000).
In this study, higher mineralization at higher AR in bioreactor
(series 1) might be connected with higher efciency of ber
removal. Although a key parameter for degradation of bers is
achieving the thermophilic conditions, it must be emphasized that
too high a temperature can be a limiting factor of process efciency. At high temperature, actinomycetes dominate which are
specically active in decomposition of hemicellulose. When the
temperature decreases below 60 C, thermophilic bacteria and
fungi utilize cellulose. Fungi are mainly involved in lignin degradation, for which optimum temperature is below 60 C. At low aeration rate, high temperature of the process (7879 C) could cause a
decrease of enzyme activity responsible for ber degradation that
resulted in lower process efciency in the bioreactor. It is more
likely, as it is known that the products of ber degradation are precursors to the formation of humic substances. So, lower EOM,loss in
the 2nd stage in series 1 can follow from the fact that during compost maturation in windrow, beside mineralization of organic matter, an intensive humication also occurred. In series 1, there was
higher content of humic substances (HS) and humic acids (HA) in
the nal product: 186.4 mgC/g OM and 113.4 mgC/g OM, respectively. For comparison, in series 2 these concentrations were lower,
148.8 mgC/g OM and 84.5 mg C/g OM, respectively (data not

60
50
40
30
20
10
0
0

composting duration [d]

series 1

series 2

10

60
50
40
30
20
10
0
0

20

40

60

80

100

120

140

160

composting duration [d]

series 1

series 2

Fig. 2. Organic matter removal efciency (OM loss) during sewage sludge composting. (a) Bioreactor, and (b) windrow.

180

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D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

(b) windrow

700

700

650

650

OM [g/kg dm]

OM [g/kg dm]

(a) bioreactor

600
550
500
450

600
550
500
450
400

400
0

10

20

composting duration [d]

series 1 (exp. data)
1. order kinetic

40

60

80

100

120

140

160

180

composting duration [d]

series 1 (exp. data)
1. order kinetic

series 2 (exp. data)

series 2 (exp. data)

Fig. 3. Kinetic of organic matter removal during sewage sludge composting. (a) Bioreactor, and (b) windrow.

Table 2
Kinetics of organic matter removal.
Series no.

1
2

Aeration rate in bioreactor (l/min kg dm)

1.0
0.5

1 aerated bioreactor

2 windrow

k (d1)

A (g/kg dm)

r (g/d kg dm)

k (d1)

A (g/kg dm)

r (g/d kg dm)

0.34
0.38

101.87
74.84

34.64
28.44

0.026
0.086

65.88
85.34

1.71
7.34

r OM removal rate (in the case of rst-order kinetic equation r = kA).

Garca-Gmez et al. (2003), during composting of the solid fraction of olive mill wastewater with olive leaves, found the rate constant k to range from 0.01 to 0.011 d1. Similarly, low values of k
0.02030.0594 d1 and 0.00830.0226 d1 were obtained by
Paredes et al. (2001), Alburquerque et al. (2009), respectively.
The former composting concerned olive mill wastewater mixed
with solid organic waste and a latter wet solid lignocellulosic
material called alperujo. The rate constants obtained by the
authors of those studies were one and even two orders of magnitude lower than those in the present study of mineralization in
the bioreactor. The higher values of k in the present study may
result from differences in composting materials and composting
technology (a two-stage system or windrows). Additionally, the
high value of k would affect the type of composted sludge (excess
sludge without stabilization) with high concentration of organic
matter (74%).
3.2. Nitrogen evolution
In the present study, a considerable amount of nitrogen was lost
at the beginning of the composting process in both series. During
composting in the bioreactor, nitrogen content decreased from
24.8 to 18.52 g/kg dm in series 1, and from 23.4 to 21.3 g/kg dm
in series 2 (Fig. 4a). The same trend was observed in case of organic
nitrogen (Fig. 4b). Simultaneously, the concentration of ammonia
nitrogen increased from 2100 mg/kg dm to 5554 mg/kg dm (series
1) and from 2126 mg/kg dm to 3972 mg/kg dm (series 2) during
the rst few days of the process (Fig. 4c); this was connected with
organic matter degradation and ammonication.
Loss of N during composting was calculated according to the Eq.
(3). In the rst stage for both series, there were considerable losses
of organic N (Fig. 5). N loss was higher (over 40%) in series 1; this
loss occurred mainly during the rst 10 days of composting. The
loss was lower in series 2 (less than 32%); at this series the concentration of volatile fatty acids (VFAs) was higher, nearly 14,000 mg/l
(data not shown). The high concentration of VFAs meant that in
this experiment the pH was below 7.9, which could limit ammonia
stripping.
Total nitrogen contents started to increase after 14 d of composting in series 1 and after 24 d in series 2. It was due to the

net loss of dry mass in terms of carbon dioxide and water loss by
evaporation caused by heat evolved during oxidization of organic
matter (Huang et al., 2004, after Kalamdhad and Kazmi, 2009).
No differences in total nitrogen concentrations were observed
between series after about 40th day of composting (Fig. 4b) and
the nal total nitrogen contents were 23.51 g/kg dm and 22.35 g/
kg dm in series 1 and 2, respectively. It means that in both series
N concentration in mature compost met Polish requirements on
N in fertilizers (OMARD, 2008).
Cayuela et al. (2006) examined the effect of aeration strategy
(forced aeration or turned windrow) on composting of olive mill
waste mixed with sheep litter and grape stalks. Nitrogen loss
was higher (about 45%) when the windrow was turned. In the
windrow with forced aeration, nitrogen loss did not exceed 10%.
Because of the pH in both windrows was similar (increasing from
pH 7 to pH 9 during the process), the larger loss of nitrogen in
the turned windrow may be associated with its higher temperature
and longer thermophilic phase.
In mature compost, nitrate was the predominate form of inorganic nitrogen (Fig. 4d). Additionally, irrespective of aeration rate
in the bioreactor, ammonia nitrogen concentration did not exceed
100 mg NNH4 /kg dm (Fig. 4c) and the NNH4 =NNO3 ratios were 0.09
(series 1) and 0.07 (series 2). According to the literature, ammonia
concentration should be below 400 mg NNH4 /kg dm in mature compost (Zucconi and de Bertoldi, 1987), and the NNH4 =NNO3 ratio below
1 (Jouraiphy et al., 2005 after Garcia et al., 1992). In the present
study, these requirements were met at both aeration rates.
At lower aeration intensities and for a different waste (manure
with sawdust), Gao et al. (2010a), reported that the ammonia concentration could become too high. In their study, aeration rates of
0.5 l/min kg OM and 0.7 l/min kg OM gave acceptable ammonia
nitrogen concentrations of 256 mg NNH4 /kg and 386 mg NNH4 /kg,
respectively. However, at a rate of 0.3 l/min kg OM, ammonia
concentration was 586 mg NNH4 /kg.
3.3. Heavy metal concentration and potential ecological risk
Beside sanitary quality, compost used in agriculture should
meet ecological standards, i.e. have low metal concentration.
According to Hsu and Lo (2001), concentration of metals in

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D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

30

(a)

25

Norg. [g/kg dm]

Ntot. [g/kg dm]

30

20
15
10
5

(b)

25
20
15
10
5
0

0
0

20

40

60

80

100

120

140

160

180

20

series 1

series 2
2000

(c)

5000

60

80

100

series 1

N-NO3 [mg/kg dm]

N-NH4 [mg/kg dm]

6000

40

120

140

160

180

composting duration [d]

composting duration [d]

4000
3000
2000
1000
0

series 2

(d)

1500
1000
500
0

20

40

60

80

100

120

140

160

180

composting duration [d]

series 1

20

40

60

80

100

120

140

160

180

composting duration [d]

series 2

series 1

series 2

Fig. 4. Nitrogen evolution during sewage sludge composting. (a) Total nitrogen, (b) organic nitrogen, (c) ammonia nitrogen, and (d) nitrate nitrogen.

60

N loss [%]

50
40
30
20
10
0
0

20

40

60

80

100

120

140

160

180

composting duration [d]

series 1

series 2

Fig. 5. Nitrogen loss during sewage sludge composting.

compost depends on the type of substrate and the composting

technology. In a present study, the main source of heavy metals
in the composting materials was sewage sludge. Concentrations
of heavy metals in other composted materials were considerably
lower (Table 3).
In order to regulate the use of potentially contaminated composts, many countries have established specic guidelines for use
of composts on agricultural lands. However, these standards vary
considerably and they only specify the maximum allowable total
metal concentrations. In Poland, the maximum levels of heavy
metals in organic and organo-mineral fertilizers and organic and
organo-mineral plant conditioners were given in the Ordinaces of
the Ministry of Agriculture and Rural Development (OMARD,
2004, 2008) on the implementation of certain provisions of the
Act on fertilizers and fertilization (Table 3). In the present study,
total heavy metal concentrations in mature composts did not
exceed the permissible values (Table 3), which means that the
heavy metal content meets the requirements for organic
amendments.

As it is known that the nal metal contents in compost are

mainly governed by their concentrations in the composted materials (feedstock composition), the impact of aeration rate on their
concentration is rather limited. However, heavy metal concentration in the nal compost is one of the factors determining the possibility of their use as organic amendments. Therefore, evaluation
of their concentration is mandatory.
When composting process nished, the total metal concentrations in nal product increased. During composting, metal concentration can increase or decrease and such uctuations are a typical
phenomenon. In the present study, one of the main factors responsible for increase in metal concentration may be mass losses during
decomposition of organic matter. This is in accordance with the
results reported by Ingelmo et al. (2012).
In the feedstock in both series, among all metals Zn characterized with the highest mobility (MF = 43.3% in series 1 and
MF = 39.8% in series 2) (Fig. 6a and b). This means that for that
metal the content of exchangeable and acid soluble fraction in relation to total metal concentration was the highest. However, the
composting led to decrease of Zn mobility below 30% as a result
of its transformation into more stable fractions. Mobility of Cu
did not exceed 13%, whereas for Ni, Pb and Cr it was below 1.5%.
The results indicate that in both series most metals occurred in
more stable chemical forms. These values corresponded well with
the values of reduced partition index (IR), reecting on Cu, Ni, Pb
and Cr stability in mature composts (0.65 < IR > 0.89) (Fig. 6c and
d). According to Han et al. (2003), the IR close to 0 means very
mobile metals, whereas close to 1 very stable metal. Due to very
low total concentration of Cd and Hg in compost their mobility (as
MF) and stability (as IR), based on sequential extraction, were
impossible to be estimated. Fractionation of metal occurring at
low concentrations may cause high relative errors (Tokalioglu
et al., 2003).
The potential ecological risk of composts produced at different
aeration regimes was evaluated using the scale proposed for the
Er factor: <40 (low risk), 4080 (moderate risk), 80160 (considerable risk), 160320 (high risk), >320 (very high risk) (Zhu et al.,
2012). This factor does not include metal fractionation, but their
total concentration and toxicity. Among analyzed metals, the

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D. Kulikowska, Z.M. Gusiatin / Waste Management 38 (2015) 312320

Table 3
Heavy metals concentrations in materials used for composting, mature compost and compost standards (values are means standard deviation, n = 3).
Sample

Total concentrations (mg/kg dm)

Sewage sludge
Wood chips
Grass
Rape straw
Series 1
Series 2
OMARD (2004, 2008)*
EU range**
*
**

Cd

Cr

Cu

Ni

Pb

Zn

Hg

0.92 (0.09)
0.0
0.0
0.0
1.35 (0.4)
1.21 (0.2)
5
0.710

47.9 (3.2)
11 (1.1)
7.8 (0.9)
6.1 (0.8)
53.4 (2.8)
55.2 (3.6)
100
70200

79.9 (4.1)
24.7 (1.3)
18.2 (2.6)
20.9 (1.7)
83.6 (5.2)
78.3 (4.7)
400
70600

29.4 (3.3)
10.2 (0.9)
12.9 (1.5)
24.5 (3.1)
41.9 (3.9)
46.8 (4.1)
60
20200

18.9 (2.1)
0.0
0.0
0.0
25.4 (2.5)
23.5 (1.8)
140
701000

425.0 (11.3)
104.8 (7.2)
54.2 (6.1)
29.8 (3.5)
370 (10.2)
349 (11.6)
1500
2104000

0.022 (0.008)
0.0
0.0
0.0
0.036 (0.01)
0.029 (0.009)
2
0.710

Polish standards.
European standards after Brinton (2000).

50

(a)

1d

50

180 d

30
20
10

20

Cu

Zn

Ni

Pb

Cr

(c)

1d

Cu
180 d

1.0
0.8

0.6

0.6

Zn

Ni

Pb

Cr
1d

(d)

180 d

IR

IR

0.8

0.4

0.4

0.2

0.2

0.0

0.0

Cu
20

Zn

Ni

Pb

Cr

(e)

1d

Cu
20

180d

16

16

12

12

Er

Er

30

10

1.0

180 d

40

M F (%)

M F (%)

40

1d

(b)

Zn

Ni

Pb

(f)

Cr

1d

180d

0
Cu

Zn

Ni

Pb

Cd

Cr

Hg

Sum

Cu

Zn

Ni

Pb

CdCr

Hg

Sum

Fig. 6. Changes of metal mobility (MF), reduced partition index (IR), potential ecological risk factor (Er) during composting. (a, c, e) Series 1, and (b, d, f) series 2.

highest value of the Er was for Cd, despite its low total concentration. Due to Cd toxicity it has one of the highest toxic response
factor (TCd
r = 30). During composting, there was a slight increase of
Er values for most metals due to increase of their total metal concentration in mature compost. Nevertheless, total Er for all analyzed
metals in mature composts was 15.6 (series 1) and 14.9 (series 2)
(Fig. 6e and f). These values indicate that metals in both composts
showed low ecological risk and can be used as soil amendment.

to 74.84 g/kg dm at 0.5 l/min kg dm. However, in the windrow, for

the biomass subjected earlier to lower AR, OM loss was higher than
in the bioreactor (85.34 g/kg dm). It means that in this case,
intense OM decomposition also occurred in the windrow. Irrespective of considerable losses of organic N, total N content in mature
compost was 23.5122.35 g/kg dm. Low heavy metals concentrations (Cd, Cr, Cu, Hg, Ni, Pb, Zn), low value of potential ecological
risk factor (Er < 16) and suitable sanitary quality indicate that compost can be used as a soil amendment.

4. Conclusions
Acknowledgement
With the same feedstock composition, higher organic matter
(OM) losses in the aerated bioreactor (101.87 g/kg dm) were
obtained at a higher aeration rate (AR) (1.0 l/min kg dm), compared

The study was supported by a Grant from the National Science

Centre in Poland, Project No N523 4550 36.

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