Science of the Total Environment 686 (2019) 681–708

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

Review

Biological wastewater treatment (anaerobic-aerobic) technologies for

safe discharge of treated slaughterhouse and meat
processing wastewater
Asad Aziz a, Farrukh Basheer b,⁎, Ashish Sengar c, Irfanullah b, Saif Ullah Khan b, Izharul Haq Farooqi b
a
Department of Civil and Environmental Engineering, University of Auckland, New Zealand
b
Department of Civil Engineering, Zakir Husain College of Engineering and Technology, Aligarh Muslim University, Aligarh 202002, India
c
Department of Civil Engineering, Indian Institute of Technology, New Delhi 110016, India

H I G H L I G H T S G R A P H I C A L A B S T R A C T

• SWW is rich in proteins, fats, lipids, fi-

bres, and carbohydrates.
• Anaerobic treatment can be used for
production of biogas, and removal of or-
ganics.
• Intermittent sequencing batch reactor is
ideal for slaughterhouse waste treat-
ment.
• Aerobic granulation technology can be
used to remove N and P in SBRs.
• Sequential anaerobic-aerobic treatment
can produce biogas and remove C, N
and P.

a r t i c l e i n f o a b s t r a c t

Article history: Slaughterhouse industry generates considerable amount of wastewater rich in proteins, lipids, fibres, and carbo-
Received 16 March 2019 hydrates. Numerous technologies such as electrocoagulation, membrane separation, advanced oxidation,
Received in revised form 18 May 2019 physico-chemical processes, and biological treatment have been implemented for reducing the concentrations
Accepted 20 May 2019
of these compounds. Nevertheless, this review aims to provide extensive information solely on the biological
Available online 23 May 2019
treatment (anaerobic and aerobic) of slaughterhouse wastewater. The advantages of anaerobic treatment are ex-
Editor: Huu Hao Ngo cellent organic matter removal, less sludge production, low energy requirement, execution of higher loading
rates, and considerable production of biogas. Aerobic treatment on the other hand is a less sensitive process, pos-
sess lower start-up period, and efficient nutrient removal process. Numerous case studies are described to

Abbreviations: ABR, anaerobic baffled reactor; ACR, anaerobic contact reactor; AF, anaerobic filter; AFFR, anaerobic fixed film reactor; AFP, aerated facultative pond; AOB, ammonia
oxidizing bacteria; APEDA, Agricultural and Processed Food Products Export Development Authority; ASP, activated sludge process; BOD, biochemical oxygen demand; COD, chemical
oxygen demand; CPCB, central pollution control board; CWs, constructed wetlands; DAF, dissolved air flotation; DO, dissolved oxygen; EU, European Union; HRT, hydraulic retention
time; ISBR, intermittent sequencing batch reactor; LCFAs, long chain fatty acids; MBR, membrane bioreactor; MBBR, moving bed biofilm reactor; MLSS, mixed liquor suspended solids;
MLVSS, mixed liquid volatile suspended solids; N&P, nitrogen and Phosphorous; NOB, nitrite oxidizing bacteria; O&G, Oil and Grease; OLR, organic loading rate; ORP, oxidation reduction
potential; RBC, rotating biological contactor; SBOD, soluble biochemical oxygen demand; SBR, sequencing batch reactor; SCOD, soluble chemical oxygen demand; SND, simultaneous ni-
trification and denitrification; SOUR, specific oxygen uptake rate; SRT, sludge retention time; SVI, sludge volume index; SWW, slaughterhouse wastewater; TA, total alkalinity; TCOD, total
chemical oxygen demand; TDS, total dissolved solids; TF, trickling filter; TKN, total kjeldahl nitrogen; TN, total nitrogen; TOC, total organic carbon; TP, total phosphorous; TS, total solids;
TSS, total suspended solids; UASB, upflow anaerobic sludge blanket; US EPA, United states environmental protection agency; UV/H2O2, ultraviolet light and hydrogen peroxide; VFAs, vol-
atile fatty acids; VOCs, volatile organic compounds; VS, volatile solids; VSS, volatile suspended solids.
⁎ Corresponding author.
E-mail addresses: aazi762@aucklanduni.ac.nz (A. Aziz), farrukhbasheer.cv@amu.ac.in (F. Basheer).

https://doi.org/10.1016/j.scitotenv.2019.05.295
0048-9697/© 2019 Elsevier B.V. All rights reserved.
682 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708

Keywords:
Slaughterhouse wastewater
Anaerobic/Aerobic treatment
Biogas
Intermittent sequencing batch reactor
bestow maximum understanding of the wastewater characteristics, kind of treatment employed, and complica-
tions involved in managing and treating of slaughterhouse effluent. Additionally, role of microbial community in-
volved in the treatment of slaughterhouse waste is also discussed. Sequential anaerobic and aerobic reactors are
also reviewed in order to present their advantages over single bioreactors. Intermittent sequencing batch reactor
is a promising technology than other high rate digesters in the removal of carbon, nitrogen, and phosphorous.
© 2019 Elsevier B.V. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 682
2. Current meat production and export in the entire globe . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 682
3. Slaughterhouse wastewater characteristics and discharge guidelines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 683
4. Anaerobic digestion and treatment technology for slaughterhouse wastewater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 684
4.1. Anaerobic ponds . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 684
4.2. Anaerobic contact reactor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 685
4.3. Anaerobic filter/Anaerobic fixed film reactor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 686
4.4. Upflow anaerobic sludge blanket reactor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 686
4.5. Anaerobic SBR . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 687
5. Aerobic treatment for slaughterhouse wastewater . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 690
5.1. Aerobic ponds/Lagoons . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 691
5.2. Constructed wetlands . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 691
5.3. Trickling filters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692
5.4. Activated sludge process . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 692
5.5. Rotating biological contactor. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 694
5.6. Moving bed biofilm reactor (MBBR) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695
5.7. Intermittent sequencing batch reactor . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 695
6. Sequential anaerobic and aerobic treatment for slaughterhouse wastewater. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697
7. Microbial community responsible for slaughterhouse waste treatment . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 697
8. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 703
Acknowledgement . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 703
References. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 703

1. Introduction
Over the last few decades of increased population and industrializa-
tion have resulted in declined water quality. Effluent wastewater com-
ing from slaughterhouses, food processing units, dairy, brewery,
tannery, and pharmaceutical industries are rich in impurities, and can
cause detrimental effects on both human beings and aquatic flora and
fauna. Particularly the slaughterhouse industry has elevated amount of
organic matter, suspended solids, oil and grease, and nutrients
(Bustillo-Lecompte and Mehrvar, 2015; Mittal, 2006). Moreover, con-
siderable amount of wastewater is generated from slaughterhouses as
a result of slaughtering, meat processing, and cleaning of equipment's.
Hence, proper mitigation is required before its final disposal. Discharge
in sewers, land application, physico-chemical processes, and biological
treatment are the current treatment techniques. Land application and
discharge in sewers are not recommended because of their nuisance
odour, contamination to aquatic water bodies, and possible emanation
of harmful gases (Avery et al., 2005; Mittal, 2006). Additionally, chemi-
cal treatment is not a feasible option as the addition of chemicals in-
creases the cost of treatment, and also the difficulty in disposing of
chemical sludge makes that process uneconomical and unfavourable.
On the other hand, biological treatment (anaerobic and aerobic pro-
cesses) provides substantial amount of advantages over other treatment
systems (discharge in sewers, land application, electrocoagulation,
membrane separation, advanced oxidation, and physico-chemical pro-
cesses) (Oğuz and Oğuz, 1993; De Villiers and Pretorius, 2001; Masse
and Massé, 2005; Del Nery et al., 2007). The advantages of using anaer-
obic treatment are excellent organic matter removal, less production of
sludge, low energy requirement, execution of higher loading rates, less
nutrients requirement, and considerable production of renewable en-
ergy in the form of methane. However, the anaerobic process possesses
some limitation as well. Longer start up period, higher temperature sen-
sitivity, inability to remove nutrients, and low to moderate effluent
quality are the chief drawbacks (Chan et al., 2009). Therefore, to tackle
this quandary, both anaerobic and aerobic processes must be employed
for the removal of nutrients and organic matter (Del Pozo and Diez,
2005; Bustillo-Lecompte and Mehrvar, 2017a). Moreover, by installing
a post aerobic unit can viably reduce the concentration of perilous pol-
lutants. In addition to that, biogas generated in anaerobic processes
can be used by the industry in numerous purposes like heating, cooking,
and for generating electricity (Coimbra-Araújo et al., 2014; Martins das
Neves et al., 2009). All in all, biological processes must be executed as a
principal secondary treatment unit in any slaughterhouse or meat pro-
cessing industry.
Hence, the objective of this article is to provide extensive knowledge
on biological treatment by imparting information on different anaerobic
and aerobic technologies employed over a period of almost three de-
cades in the management of slaughterhouse and meat processing
wastewater. Global meat production, slaughterhouse wastewater char-
acteristics, and international discharge regulations have also been
reviewed. Furthermore, each treatment technique whether anaerobic
or aerobic is presented in such a way that provides excellent under-
standing of each treatment process, design, functioning, and its profi-
ciency in eliminating the perilous contaminants. Additionally, the role
of microbial community involved in the degradation of slaughterhouse
waste is comprehensively discussed.
2. Current meat production and export in the entire globe
The global meat production in 2017 reached to almost
330 million tonnes in case of bovine, poultry, pig, and ovine. The leading
meat producing countries in 2017 were United States, Brazil,
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708 683

Table 1
World's meat production and export in 2017.

World China EU United States Brazil Russia India Mexico Argentina

Meat production 330.38 85.81 47.88 45.84 27.07 9.81 7.34 6.80 5.58
Meat export 32.71 0.59 4.98 7.71 7.02 – 1.73 – 0.55

All values in million tonnes.

Russia, Argentina, Mexico, and India. Poultry meat production
(120.5 million tonnes) was greatest when compared with other meat
productions in that particular year (Food and Agriculture Organization
of the United Nations, 2018). Table 1 gives world's meat production
and export in the year 2017.
In India, meat production has considerably increased over the last
few decades. In 2010, India was approximately exporting about
1.45 million tonnes of meat worldwide, and thus was generating
about 1500 million US$ as revenue (Central Pollution Control Board of
India, 2017). In the present scenario, India's meat production has soared
to around 1.73 million tonnes (Food and Agriculture Organization of the
United Nations, 2018). According to Agricultural and Processed Food
Products Export Development Authority (APEDA), there are almost
1176 slaughterhouses and 75 modern abattoirs in India. Major meat
producing states are Andhra Pradesh, Uttar Pradesh, Tamil Nadu, and
Maharashtra (Central Pollution Control Board of India, 2017; Rao et al.,
2010).
3. Slaughterhouse wastewater characteristics and discharge
guidelines
Slaughterhouse wastewater (SWW) characteristics generally de-
pend upon various factors such as size of slaughtering facility, kind of
animals slaughtered, type of slaughtering involved, quantity of water
consumed per animal, and washing of slaughtering equipment's. Ac-
cording to World Bank Group (2007), around 1.62–9 m3 of water is
consumed per tonne of cattle carcass, and 1.6–8.3 m3 per tonne of
pig carcass. Additionally, water consumption and wastewater com-
position largely depend upon the type of animal slaughtered. Beef
or cattle carcass requires much more water than pig or poultry car-
cass (Gerbens-Leenes and Mekonnen, 2013). Apart from that,
Mekonnen and Hoekstra (2012) illustrated that the type of food
manufactured greatly increases the water requirement. For example,
animal products such as beef and chicken have comparatively
greater water requirement than crop products like cereals and
pulses. Furthermore, size and type of plant (slaughtering or render-
ing or meat processing) will also contribute to the amount and inten-
sity of wastewater generated (Massé and Masse, 2000a). All in all,
wastewater generated as a result of slaughtering and processing
units have elevated amount of organic matter, nutrients, pathogens,
detergents, and sometimes antibiotics and heavy metals as well
(Torkian et al., 2003b; Sirianuntapiboon and Yommee, 2006; Cao
and Mehrvar, 2011; Bazrafshan et al., 2012; Carvalho et al., 2013).
The aquatic environment can be enormously damaged as a result of
discharge of this kind of wastewater. There are several cases of
deaths throughout the world due to the presence of excessive
amount of pollutants particularly pathogens (Cai and Zhang, 2013;
Toze, 1999). Eutrophication is also a cause of concern observed due
to the presence of ample amount of nutrients (Sengar et al.,
2018a). Slaughterhouse wastewater along with different industrial
wastewaters are presented to highlight better understanding of its
characteristics (Table 2) (Bustillo-Lecompte and Mehrvar, 2015;
Caixeta et al., 2002; Choi et al., 2002; Del Nery et al., 2007, 2016;
Del Pozo and Diez, 2005; Demirel et al., 2005; Filali-Meknassi et al.,
2005a; Fongsatitkul et al., 2004; He et al., 2005; Johns, 1995;
Lemaire et al., 2008a; Manjunath et al., 2000; Martínez et al.,
1995a; Nandy and Kaul, 2001; Rajakumar and Meenambal, 2008;
Schneider et al., 2011).
World leading organisations such as United States Environmental
Protection Agency (US EPA), European Union (EU), Central Pollution
Control Board (CPCB) of India, People's Republic of China Ministry of
Environmental Protection, Environment Canada, and Australia and
New Zealand Environment and conservation council have given
their effluent discharge standards for SWW (Bustillo-Lecompte and
Mehrvar, 2017a; Central Pollution Control Board of India, 2016).
Table 3 shows the effluent discharge limits for pH, chemical oxygen
demand (COD), biochemical oxygen demand (BOD), nitrogen and
phosphorous (N&P), oil and grease (O&G), and total suspended
solids (TSS) by these governing bodies.
The wastewater discharged after proper treatment must comply
with these standards in order to safely dispose the effluent. The type
of treatment usually depends upon the wastewater characteristics,
availability of treatment facility, and effluent discharge standards of
that particular country. However, in case of organic rich wastewaters es-
pecially slaughterhouse effluent, biological treatment is usually
employed over other treatment options such as electrocoagulation,
membrane separation, and advanced oxidation (Demirel et al., 2005;
Chan et al., 2009).

Table 2
Characteristics of different industrial wastewater.

Parameter SWWa DWWb ORWWc TWWd PWWe LWWf

pH 5–7.8 6–11 6.9–10 7–7.2 4.2–4.5 –

COD (mg/l) 1100–15,000 1150–9200 125–1095 773–1290 5000–80,000 6190–78,600
BOD (mg/l) 600–3900 – – 400–490 – 3940–34,600
TN (mg/l) 50–840 – – – 135–1250 1530–6500
TKN (mg/l) 40–700 14–272 – 42.7–161 – –
NH4-N (mg/l) 20–300 – 5–51 – 40–320 –
TP (mg/l) 15–200 8–68 – 9.4–27.9 30–120 116–1770
PO−3
4 (mg/l) 8–120 – – – – –
TSS (mg/l) 220–6400 340–1730 9–93 – 900–18,800 1850–29,000
O&G (mg/l) 40–1385 – – – – –
VFA (mg/l) 175–797 – – – – –
Alkalinity (mg/l) 350–1340 320–970 – – – –

SWWa - Slaughterhouse wastewater; DWWb - Dairy wastewater; ORWWc - Oil refinery wastewater; TWWd - Textile wastewater; PWWe - Pharmaceutical wastewater; LWWf - Livestock
wastewater.
684 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708

Table 3 this step (2−3 h). In anaerobic digestion VFAs production and accumu-
International Effluent discharge standards for SWW. lation can cause drop in pH, and ultimately can effect methane produc-
Parameter US EPA EU CPCB China Canada Australia tion (Kuglarz et al., 2011). Nevertheless, amino acid degradation to
pH 6–9 – 6.5–8.5 6–9 6–9 5–9
ammonia will provide adequate alkalinity for the reactor's stability
COD (mg/l) – 125 250 100–300 – 40 (Del Nery et al., 2007). VFA/alkalinity ratio is an important factor in de-
BOD (mg/l) 16–26 25 30 20–100 5–30 5–20 termining reactor's performance, and in no case it should be N0.3
TN (mg/l) 4–8 10–15 – 15–20 1.25 10–20 (Francioso et al., 2010; Li et al., 2014).
TP (mg/l) – 1–2 – 0.1–1 1.0 2
Thereafter in the acetogenesis step the VFAs produced are degraded
O&G (mg/l) – – 10 – – –
TSS (mg/l) 20–30 35–60 50 20–30 5–30 5–20 to mainly acetate and hydrogen. The only requisite condition is low hy-
drogen partial pressure (H2 b 10−4 atm) (Salminen and Rintala, 2002).
Butyrate

CH3 CH2 CH2 COO− þ 2H2 O→2CH3 COO− þ Hþ

4. Anaerobic digestion and treatment technology for slaughterhouse
wastewater
Anaerobic digestion of organic waste, sludge, and high strength in-
dustrial wastewater is a widespread technique in biological treatment.
Complex organic compounds are degraded with the help of diverse
group of microorganisms (bacteria and archaea) in the absence of oxy-
gen. The degradation rate depends mainly upon different bacteria activ-
ity rates (Kondusamy and Kalamdhad, 2014). The end product of one
species may be the desired substrate for the other, and hence appropri-
ate conditions must be prevailed inside anaerobic digester to obtain
final end product in the form of methane (CH4), carbon dioxide (CO2),
ammonium (NH4), water (H2O), and hydrogen sulphide (H2S)
(Husain, 1998; Yadvika et al., 2004). The degradation process consists
of following four basic consecutive steps, viz. hydrolysis, acidogenesis,
acetogenesis, and methanogenesis (Fig. 1) (Demirel and Scherer,
2008; Mao et al., 2015).
The first step involved in the degradation of complex compounds is
hydrolysis. Here the hydrolytic bacteria excrete the co-enzymes in order
to provide the soluble products for other microbial species, and hence
the soluble monomer can be easily passed through the acidogenic bac-
terial cell walls (Appels et al., 2008; Amani et al., 2010). The rate of hy-
drolysis depends upon factors such as temperature, substrate size,
porosity, and their biodegradability, and due to that hydrolysis is con-
sidered to be rate limiting step in the entire degradation process
(Palatsi et al., 2011). The end products obtained are amino acids, long
chain fatty acids (LCFAs), monosaccharide's, alcohols, purines and py-
rimidines (El-Mashad et al., 2004).
The second step involved after hydrolysis is the acidogenesis step,
which involves further degradation of soluble compounds like LCFAs, al-
cohols, amino acids, and monosaccharide's. Acidogenic bacteria finally
degrade them to higher (butyrate, propionate) and smaller organic
compounds (acetate), which are known as volatile fatty acids (VFAs)
(Li et al., 2019). Additionally, H2, CO2, ammonia, methanol, lactate, eth-
anol, formate, isovaleric acid, caproic acid, and valeric acid are also pro-
duced, and the bacterial growth and conversion rates are maximum for
þ 2H2 ðΔG◦ ¼ 48:1 kJ=molÞ ð1Þ
Propionate
CH3 CH2 COO– þ 3H2 O→CH3 COO– þ HCO−3 þ Hþ þ 3H2 ðΔG◦ ¼ 76:1 kJ=molÞ
ð2Þ
Palmitate
CH3 ðCH2 Þ14 COO− þ 14H2 O→8CH3 COO− þ 7Hþ þ 14H2 ðΔG◦ ¼ 345:6 kJ=molÞ
ð3Þ
From Eqs. (1), (2), and (3) it can be seen that the value of free energy
change (ΔGO) for butyrate, propionate, and LCFAs palmitate reactions
are 48.1 kJ/mol, 76.1 kJ/mol, and 345.6 kJ/mol respectively (Wang
et al., 1999). It indicates that a negative free energy change is required
for hydrogen producing acetogenic bacteria (HPAB) to proceed in the
forward direction, and this can be done by maintaining low hydrogen
partial pressure within the digester. The partial pressure can be reduced
considerably with the help of methanogenic and sulphate reducing bac-
teria (Appels et al., 2008). Methanogenic species utilize the hydrogen
produced by HPAB so promptly that it reduces the partial pressure of
hydrogen (H2 b 10−4 atm), and thereby increasing the activity of
HPAB. The combined production and uptake of hydrogen by two differ-
ent bacterial consortiums is known as interspecies hydrogen transfer
(Morita et al., 2011).
The last step involved in the anaerobic digestion process is
methanogenesis. The optimum pH required in this phase is 6.8–7.2
(Mun, 2012). The acetate and hydrogen produced in acetogenesis
phase gets converted into methane by two classes of methanogens
namely acetate utilizing bacteria (AUB) and hydrogen utilizing bacteria
(HUB). AUB are mainly responsible for maximum methane production
(72%) (Tchobanoglous et al., 2003). However they usually have lower
growth rate as compared to HUB. Thus, it is recommended to provide
higher sludge concentrations with longer retention time in anaerobic
digesters. Apart from that, higher growth rate of HUB results in provid-
ing sufficient hydrogen partial pressure for acetogenic bacteria, and
thereby the performance of the reactor can be successively maintained.
AUB can be further classified into methanosarcina and methanosaeta.
Methanosaeta consumes only acetate for its conversion to CH4, while
methanosarcina beside acetate can also utilize H2, CO, CO2, methyl-
amines and methanol as substrates (Mun, 2012).

4.1. Anaerobic ponds

Anaerobic ponds (covered) have been successfully implemented in

Fig. 1. Steps involved in anaerobic digestion process.
the waste management of slaughterhouse effluent. They have been ef-
fectively used for trapping biogas and removing the nuisance odour
from the wastewater (Fig. 2(a)) (Massé and Masse, 2000a). The two
main factors that allow the usage of anaerobic pond for high strength
wastewater are the availability of land and appropriate weather
(Mittal, 2006; Massé and Masse, 2000a). Hence, large anaerobic ponds
were constructed exclusively in Australia and United States in the late
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
(a). Schematic diagram of anaerobic pond
(c). Schematic diagram of upflow anaerobic sludge blanket
Fig. 2. Schematic diagram representing: (a). Anaerobic pond. (b). Anaerobic filter. (c). Upflow anaerobic sludge blanket. (d). Anaerobic sequencing batch reactor.
1980's. The hydraulic retention time (HRT) of a typical anaerobic pond
is primarily between 3 and 5 d with a maximum depth of 5 m. According
to Dague et al. (1990), covered anaerobic pond was established and op-
erated for a meat processing industry of United States. The pond
achieved 90% removal of organic matter, with a concurrent production
of 0.51 m3 CH4/kg-organic matter. However, the production of biogas
is largely dependent upon organic matter loading. Lower BOD loading
results in deprived biogas production and vice versa (Safley and
Westerman, 1988).
Peña et al. (2000) compared the feasibility of using anaerobic pond
over high rate upflow anaerobic sludge blanket (UASB) reactor. The re-
sult showed that there was no significant difference between the two
anaerobic processes. The COD removal efficiencies were 68% and 66%
for anaerobic pond and UASB reactor respectively. However, anaerobic
pond is considered to be better than other high rate digesters because
it required lesser maintenance and operation cost, lower initial invest-
ment, and cheap availability of land (Yacob et al., 2006).
Also, the production of biogas largely depends upon temperature
(Safley and Westerman, 1992). Hammer and Jacobsen (1970) have de-
clared that the efficacy of anaerobic pond can be greatly affected with
the decrease in temperature (b21 °C), and it would be very hard for
685
(b). Schematic diagram of anaerobic filter
(d). Schematic diagram of anaerobic sequencing batch reactor
an anaerobic pond to revive its efficiency if it collapses in winter
(Johns, 1995). A study of moderate temperature (18.2–24.9 °C) in
Brazil was conducted by Del Nery et al. (2013) for determining the
pond's effectiveness. HRT was varied from 2.2 to 3.8 d, and the organic
loading rates were increased from 0.26 to 1.05 kg BOD/m3-d in the en-
tire study. The removal efficiencies obtained were 62%, 42%, and 38% for
O&G, COD, and BOD respectively.
McCabe et al. (2014) have asserted that the anaerobic pond was ca-
pable enough in degrading organic matter and potentially viable in gen-
erating 328 m3/d of biogas as well. The only shortcoming associated
with that pond was the problematic measurement of the exact amount
of biogas generated due to the accumulation of fats/crusts on the surface
of the ponds.
4.2. Anaerobic contact reactor
Anaerobic contact reactor (ACR) is another type of anaerobic di-
gester which has been used productively in the treatment of slaughter-
house waste. The vital characteristic of the ACR is its exceptional ability
to retain anaerobic sludge with the help of recycling and sludge separa-
tion techniques. Apart from that, considerable reduction in reactor's
686 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
volume can be achieved by separating the system's HRT and sludge re-
tention time (SRT) (Tchobanoglous et al., 2003).
At full scale, Black et al. (1974) exhibited excellent removal in or-
ganic matter (90%) and volatile solids (40–70%) when operated at or-
ganic loading rates (OLRs) of 0.12–0.28 kg/m3-d. Numerous studies
have been performed to check the reactors stability. In one such study,
Bohm (1986) has examined the performance of 3 m3 of ACR, and con-
firmed that the reactor was effectively installed and operated at OLR
of 5 kg/−m3-d while treating slaughterhouse wastewater. Kostyshyn
et al. (1988) employed an ACR at mesophilic temperature for treating
the wastewater coming from United States (US) meat packaging plant.
The OLRs (2–3 kg/m3-d) and HRT (1.7–2.5 d) proved to be sufficient
enough in removing 75% TSS and 85% COD from the wastewater. An-
other study in US on the efficiency of ACR was evaluated by Stebor
et al. (1990). The reactor exhibited admirable removal in TSS (75%),
BOD5 (93%), and COD (84%) from meat processing wastewater. Addi-
tionally, biogas was also generated having a methane content of
68–98%. However, due to deprive settling of sludge in ACR, made their
usage reluctant in the field of anaerobic digestion.
4.3. Anaerobic filter/Anaerobic fixed film reactor
Anaerobic filter (AF) or anaerobic fixed film reactor (AFFR) have
been implemented largely in the treatment of high strength wastewater
especially in slaughterhouse effluent. They usually achieve higher ab-
straction efficiency with lower effluent suspended solid concentrations.
The wastewater flows either downwards or upwards depending upon
the reactor's configuration. The pollutant that is organic in nature gets
trapped on the surface of the filter media (stone/plastic media), and is
then removed by microorganism attached to that filter (Fig. 2(b))
(Young and Mccarty, 1969). The reactor is mainly suited for the treat-
ment of soluble wastewater, and its performance can be largely
inhibited due to clogging of filter media (Bustillo-Lecompte and
Mehrvar, 2015; Massé and Masse, 2000b; Mittal, 2006). Moreover, pa-
rameters like filter media depth, shape and size, temperature, and HRT
are crucial in the design of an AF.
Viraraghavan and Varadarajan (1996) reported that HRT and tem-
perature plays a vital role in the treatment of organic compounds.
Harrison et al. (1991) exhibited that maximum COD removal of 77%
was achieved at 26.7 °C by increasing the HRT to 3.9 d. Another study
on the performance of AF treating slaughterhouse wastewater was con-
ducted by Campos et al. (1986) over a period of six years, the reactor
achieved 85% COD and 88% suspended solids removal efficiency at
OLR of 1.4 kg/m3-d.
Apart from that, Andersen and Schmid (1985) and Festino and
Aubart (1986) have declared that around 70–85% of organic matter
was successfully converted to methane at 2–3 kg/m3-d OLRs. However,
higher COD loadings resulted in deprived performance of AF (Tritt,
1992; Johns, 1995). Also, the performance of AF can be further dimin-
ished due to the presence of suspended solids and oil and grease. In a
case study by Andersen and Schmid (1985), lower performance of
pilot scale AF was examined as a result of evaluated concentrations of
oil and grease. Therefore, removal of oil and grease is an essential pre-
requisite in AF. Metzner and Temper (1990) achieved 90% COD reduc-
tion as a result of combined primary (drum screen, mud trap and a
grease separator) and secondary treatment (AF) in case of German
meat processing plant. In order to observe the effect of organic loading
rate on the performance of AF, Ruiz et al. (1997) conducted a research
in Spain. The loading rates were gradually increased from 0.5 to
6 kg/m3-d over a period of about 90 d. The organic matter removal effi-
ciency was mainly between 60 and 90% at 37 °C in that particular period.
However, further increasing the loading rate resulted in declined re-
moval efficiency, but the performance of the reactor was stable up to
OLR of 11 kg/m3-d.
Higher organic loading rates were also applied by Del Pozo et al.
(2000) for evaluating the performance of down flow and up flow
anaerobic fixed film reactors by using PVC corrugated pipes of 70 cm.
Both the reactors exhibited 85–95% organic matter removal efficiency
at a loading rate of 8 kg/m3-d when operated at 35 °C. Nevertheless, in-
creasing the loading rate to 35 kg/m3-d resulted in decline in removal
efficiencies (55%–75%), but the reactors demonstrated a well stabilized
behaviour after further increase in OLR (50 kg/m3-d).
In India, a study was conducted by Rajakumar and Meenambal
(2008) for evaluating the desired HRT and required start up time for
an AF treating poultry slaughterhouse wastewater. The HRT was de-
creased gradually from 36 h to 8 h throughout the research period.
That decrease in HRT resulted in increased organic loading rates. At an
HRT of 12 h, the reactor successfully removed 79% soluble COD
(SCOD) and 70% total COD (TCOD). Nevertheless, the reactor showed
lower efficiency of 66% when the HRT was further decreased.
Gannoun et al. (2009) treated SWW anaerobically in an AF at 37 °C
(mesophilic) and 55 °C (thermophilic). The COD loading rates were in-
creased from 0.9 to 9 kg/m3-d and 0.9 to 6 kg/m3-d for thermophilic and
mesophilic respectively. For mesophilic period the maximum organic
matter removal efficiency was around 92% at a loading rate of
2.8 kg/m3-d, but further increase in loading rate resulted in decline in
removal efficiency (80%). However, the biogas production enhanced
considerably by increasing the loading rate to 4.5 kg COD/m3-d. On
the other hand, the thermophilic period exhibited 93% COD removal
up to 3.6 kg/m3-d of OLR, and b1.4 l/d of biogas was produced at that
particular time period. However, on increasing the loading rate to
4.5 kg/m3-d resulted in decreased biogas production and organic matter
removal efficiency.
A research on the applicability of AF in case of high strength waste-
water (cold meat industry) was conducted by León-Becerril et al.
(2016). The start-up period was reduced to just 15 d as a result of utiliz-
ing the already acclimatized sludge. The AF reactor exhibited excellent
removal efficiency in case organic matter with TCOD and BOD removal
efficiency of 84% and 88% respectively. The average methane yield of
422 ml CH4/g-COD was obtained when the reactor operated stably
(OLR of 1.17–3.5 kg/m3-d) at a temperature of 37 °C.
4.4. Upflow anaerobic sludge blanket reactor
In late 1970's, UASB technology was developed by Lettinga and his
co-workers in Netherlands as a modification of high rate anaerobic di-
gesters (Tchobanoglous et al., 2003). Over the last three decades,
UASB technology has been proven to be proficient enough in the treat-
ment of slaughterhouse wastewater. The wastewater enters from bot-
tom most part of the reactor, and travels within a blanket of sludge in
an upward continuous manner. The treated effluent can be acquired
from the top most portion of the digester (Fig. 2(c)). Solid (sludge), liq-
uid (wastewater), and gases (CH4 & CO2) are the three main component
of upflow anaerobic sludge blanket reactor. Mixing of the sludge is usu-
ally carried out by the upflow velocity and biogas. Nevertheless, the size
of the sludge particle (flocculent/granular) is also a vital parameter in
the performance and operation of an UASB. The particles must also re-
tain back to the bottom of the reactor in order to avoid their escape.
Therefore, upflow liquid velocity is a crucial component in the design
of an UASB, and it should be increased accordingly with the perfor-
mance of the reactor (Manjunath et al., 2000; Del Nery et al., 2007,
2008) Several full scale UASB reactors had been successfully established
in New Zealand and Belgian in the late 1980s (Steiner, 1987). The func-
tioning of UASB reactors largely depends upon the concentration of the
influent organic matter, and the main drawback of treating slaughter-
house wastewater in an UASB reactor is its inability to operate at higher
loading rates as a result of presence of suspended and colloidal (cellu-
lose, protein, and fats) impurities.
Sayed (1987) were able to provide maximum organic loading rate of
11 kg/m3-d to any UASB reactor (granular sludge) treating slaughter-
house wastewater. Sludge washout is a very common issue especially
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
at high loading rates, which generally results in decline in bacterial
activity.
Ruiz et al. (1997) evaluated the performance of UASB reactor by in-
creasing the organic loading rates from 1 to 6.5 kg COD/m3-d at a con-
stant temperature of 37 °C. The slaughterhouse wastewater was
having the following characteristics: COD = 8000 mg/l, TSS =
1200 mg/l, PO−3 4 = 20 mg/l, NH4 = 44 mg/l and pH = 7.2. Maximum
COD removal (90%) was observed at 5 kg COD/m3-d. However, further
increase in the loading rate resulted in declined removal efficiency
(59%). Nevertheless, SCOD and methane generation (60%) were inde-
pendent from increased loading rates, and were fairly constant through-
out the research period. Martínez et al. (1995b) examined the
performance of anaerobic reactor receiving high concentrations of fats
and suspended solids from an effluent treatment plant (slaughter-
house) of Uruguay. The wastewater was rich in suspended solids, or-
ganic and inorganic contents. The primary treatment was ineffective
in case of slaughtering (blood) wastewater, but showed positive result
in case of tripe processing and pen cleaning wastewater (60% particu-
late COD removal). The secondary treatment (UASB) removed about
70% particulate COD and 60% fats, but on the other hand was unable
to remove SCOD. Considerable removal of fats and solids were achieved
by employing a pressurized air in the flotation tank.
In Columbia, Hansen and West (1992) conducted a research by tak-
ing three different wastewater streams of a slaughterhouse. The three
streams were cooker condensate wastewater, raw blood, and wash-up
water. In the first phase 98% condensate water and 2% raw blood were
used in the anaerobic digester (UASB), while in the second phase 44%
condensate water and 56% of wash-up waster were used. The maximum
TCOD removal efficiency was 72% and 87% for phase I and II respectively.
However, accumulations of volatile fatty acids (VFAs) were observed
with increased loading rates, and thus the HRT was increased again to
avoid their accumulation.
According to Callaghan et al. (2002) and Kuglarz et al. (2011), VFA/
total alkalinity (TA) is an important indicator of the system's perfor-
mance and stability. The anaerobic digestion can be inhibited largely if
that ratio exceeds 0.3 (Hamawand et al., 2015; Kuglarz et al., 2011).
VFAs (acetate, propionate, and butyrate) are produced as intermediate
products in the process of anaerobic digestion. Their presence in exces-
sive amount can inhibit the process, and can ultimately affect the me-
thanogenic activity of the sludge (Chen et al., 2008). Wong et al.
(2007) have conducted two experiments in evaluating the consequence
of increasing VFAs and loading rates. In the first experiment mixed VFAs
(acetate/butyrate/propionate) having a COD of 20 g/l was used as sub-
strate. The increased loading rates (0.82–10.4 kg COD/m3-d) resulted
in increased biogas production (58–82% CH4) with simultaneous re-
moval of COD (83–99%). Thereafter, the mixed VFAs feed was changed
to single feed of acetate, propionate, and butyrate each with 20 g COD/
l as substrate. Acetate feed reactor showed some inhibitory effect of
pure acetate on biogas production but subsequently recovered after a
period of 200 h. The methane produced (90%) from acetate feed was
10% higher than mixed VFAs feed. However, 15% reduction (75%) in
COD was observed as a result of change in the feed. In case of butyrate
feed reactor around 72–80% of methane was produced as a result of
two step degradation of butyrate. Complete inhibition was observed
when propionate feed was used as a sole substrate for feeding. More-
over, it has been reported that the inhibition caused by acetate and bu-
tyrate are less significant than the inhibition caused by only propionate
feed (Callaghan et al., 2002; Rajagopal et al., 2013). Del Nery et al.
(2001) have also studied the performance of the VFAs by increasing
the upflow velocity and organic loading rates in case of 2 full scale
UASB reactors (each 450 m3) treating slaughterhouse wastewater. The
reactors received about 2695 mg/l of influent COD at an initial OLR of
0.51 kg COD/m3-d. However, the organic loading rate was increased
gradually to 2.11 kg COD/m3-d in a period of 144 d. The result showed
that both the reactors were capable enough in removing SCOD from
the system with the removal efficiency of 84–94% (R1) and 81–93%
687
(R2), and the process was not inhibited at increased VFAs
concentrations.
Additionally, the performance of anaerobic reactors can be greatly
influenced with the conversion of proteins to unionized ammonia and
degradation of lipids to long chain fatty acids (LCFAs). Both the factors
can affect the reactor's performance, and can ultimately inhibit the bio-
gas production (methane) (Salminen et al., 2001). In order to assess the
effect of long chain fatty acids on the performance of UASB reactor
(6.67 l) a research was conducted by Hwu et al. (1998) at 35 °C. LCFAs
mixtures of stearic acid (15%), palmitic acid (35%), and oleic acid
(50%) were used as sorbates (COD), and sludge granules as sorbents
from Taipei slaughterhouse, Taiwan. The performance of the digester
was evaluated by increasing the concentrations of LCFAs from 0.086 to
0.250 g/g VSS-d, and simultaneously observing the floatation of sludge
from the sludge bed in a specific time interval. The reason for collapsing
of an UASB reactor was found mainly because of the floatation of the an-
aerobic sludge, rather than due to the inhibition of methanogenic con-
sortium. Similar results of sludge washout, process inhibition, and
flotation of biomass were also observed (Hwu et al., 1998; Rinzema
et al., 1993; Silva et al., 2014; Sousa et al., 2009).
In another study by Rodríguez-Méndez et al. (2017), inhibitory ef-
fects of LCFA's were analysed. The result revealed that hydrolysis step
was not affected as a result of LCFAs inhibition as compared to later deg-
radation steps (acetogenesis and methanogenesis). Additionally,
palmitic acid concentrations and LCFA/volatile solid (VS) ratios can be
used as inhibitory indicators. Complete inhibition was observed as a re-
sult of increased palmitic concentrations (N40%) and LCFA/VS ratio
(N1.7). Hence, both factors can be used in controlling and preventing
LCFAs inhibition in case of anaerobic digester. Several other lab and
pilot scale studies using UASB reactors are shown in Table 4.
A full scale research on the slaughterhouse wastewater was evalu-
ated in Brazil by Miranda et al. (2005). The entire research was con-
ducted by installing two large scales UASB reactors each having a
capacity of 1600 m3 and 800 m3. The first UASB reactor (1600 m3) col-
lapsed after 6 months of operation. Accumulation of O&G on the surface
of biomass resulted in declined performance. Hence, another anaerobic
digester (800 m3) was established for the treatment of meat processing
and slaughterhouse wastewater. However, a pre-treatment (physico-
chemical) unit was installed before the second digester. The removal ef-
ficiencies for both the reactors are shown in Table 5. Though the re-
moval efficiency of the second digester (800 m3) was comparatively
lower than the first (1600 m3), but the influent value of COD and O&G
were significantly decreased after the installation of a pre-treatment
unit.
Del Nery et al. (2008) examined a study on the formation of granules
in case of poultry slaughterhouse wastewater. Granules formed were di-
verse in size ranging from 0.1 to 3.5 mm. Moreover, 0.6–1.5 mm size
granules were dominant in the anaerobic digester. The entire research
was conducted at a full-scale slaughterhouse located in Sorocaba, state
of Sao Paulo, Brazil. The wastewater was fed to the anaerobic digester
(UASB) of 450 m3 capacity after the preliminary treatment. Three verti-
cal ports were selected from bottom most part of the reactor for sludge
analysis. The results obtained were satisfactory for TCOD (65%) and
SCOD (85%) removal at an OLR of 1.64 ± 0.37 kg COD/m3-d.
Del Nery et al. (2016) on the other hand have asserted that 2.2 kg
COD/m3-d OLR resulted in 35% O&G, 71% BOD, and 69% COD removal
from a UASB (1260 m3) reactor in case of full-scale plant of Pereiras,
Sao Paulo State, Brazil. The main units involved in that plant were dis-
solved air flotation (DAF), UASB, aerated facultative pond (AFP), and
chemical DAF.
4.5. Anaerobic SBR
In case of slaughterhouse wastewater sequencing batch reactor is
considered to be the best available technology (Mace and Mata-
Alvarez, 2002; Pal et al., 2016). Anaerobic sequencing batch reactor
688 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708

Table 4
Numerous lab and pilot scale applications of UASB reactors treating slaughterhouse waste.

Temperature Reactor Reactor OLR HRT CODI CODR BODI BODR TSSR CH4 Biogas References
(°C) configuration volume (mg/l) (%) (mg/l) (%) (%) (%) (l/d)
(l)

35 UASBa 6.2 1.27–17 kg 4–0.3 d 5100 64–99 3100 – – 57.5–72 0.68–3.99 Borja et al., 1994
COD/m3-d
a
30 UASB 11.4 3.5 kg COD/m3-d 10 h 1100–7250 70 600–3900 – – – – Manjunath et al., 2000
30 DAF UASBb 11.4 4 kg COD/m3-d 10 h 1100–7250 90 600–3900 – – – – Manjunath et al., 2000
35 UASBa 7.2 2.7–10.8 kg 22–14 h 2000–6000 80–85 1300–2300 95 81–86 – 10.1–12.6 Caixeta et al., 2002
COD/m3-d
33 UASBa 1000 13–39 kg 7–2 h 3143–4288 68–85 914–1917 – – – – Torkian et al., 2003b
SCOD/m3-d
25–39 UASBa 3 31 kg BOD/m3-d 4.5–3.5 h 7333 – 5500 95 – – – Chávez et al., 2005
29–35 HUASBc 5.4 1.15–3.43 kg 24–8 h 3000–4800 80 750–1890 – 60–84 75 3.3 Rajakumar and
COD/m3-d Meenambal, 2008
19.7–27.31 UASBa 15 4–15 kg 0.88–0.3 3534–4994 76–90 2646 – 41–55 62–64 20–95 Nacheva et al., 2011
COD/m3-d d
29–35 HUASBc 5.4 9.27 kg 10 h 3000–4800 86 750–1890 – 93 72 5.8 Rajakumar et al., 2012
COD/m3-d
30 UASBa 33.9 6–36 h 2550–5350 36–84 – – 43–65 – – Saghir and Hajjar, 2018

CODI - Influent COD; CODR - COD removal; BODI - Influent BOD; BODR - BOD removal; TSSR - TSS removal; UASBa - Upflow anaerobic sludge blanket; DAF UASBb - Dissolved air flotation
upflow anaerobic sludge blanket; HUASBc - Hybrid upflow anaerobic sludge blanket.

(ASBR) was invented by Richard R. Dague and his associates at Iowa
State University (USA) in 1993 as a modification of anaerobic contact
and anaerobic activated sludge processes (Dague, 1993; Sung and
Dague, 1995). Feed, react, settle, and decant all takes place sequentially
a single batch reactor (Fig. 2(d)). As a result of that, post clarifier re-
quirement is eliminated. ASBR is simple in process and it requires less
operating and maintenance cost as compared to other anaerobic di-
gesters (Massé and Masse, 2000b). Moreover, biomass retention is a
key phenomenon in ASBR. During feeding, the wastewater enters into
a batch reactor having a fixed volume. Thereafter, in the react phase,
the biomass and the organic matter gets mixed either continuously or
intermittently with the help of mixer for a fixed interval of time. In
that phase, organic matter gets converted into biogas (CH4 and CO2)
(Steele and Hamilton, 2010). The rate of biogas production depends
upon the Food/Mass (F/M) ratio. During starting of the react phase,
high F/M ratio is observed with considerable generation of biogas
(Ndegwa et al., 2008). However, the rate of biogas production got de-
creased with time and so does the F/M ratio. Thereafter, in the third
(settling) phase, due to lower F/M ratio, supernatant (treated water)
gets separated from the biomass. Lower F/M ratio results in enhanced
settling of the biomass (Ndegwa et al., 2008). Subsequently to that
comes the decanting phase, which results in withdrawn of the treated
water from the reactor, and thus the completion of the cycle as well.
The next cycle continues in the same manner, and the number of cycles
depends upon the system's HRT (Dague, 1993; Wirtz and Dague, 1996).
The generation of biogas depends largely upon the rate of mixing in
the react phase. Therefore, a study was conducted by Sung and Dague
(1995) to evaluate the effect of mixing (continuous or intermittent) in
ASBRs. The researchers took 4 different ASBR (A, B, C, and D) which
were having different depth to diameter ratios (5.6, 1.83, 0.93, and
0.61). The OLR for reactors A and B were 2, 4, 6, and 8 kg/m3-d at each
HRT (48, 24, and 12 h), while for reactors C and D, the loading rates
were 2, 4, 6, 8 kg/m3-d at 48 and 24 h, and2, 4, 6, 8, 10, 12 kg/m3-d at
12 h. From that study, it can be concluded that methane production
rate (l/h) varied significantly in a course of 6 h with a peak production
of 3.5 l/h in case of continuous mixing, whereas for intermittent mixing
(5 min/h) the methane peak production was well below 3 l/h. However,
the rate of production of methane over a period of 6 h in case of inter-
mittent mixing was higher as compared to the continuous mixing. For
COD removal, both type of mixing proved to be efficient and there
was no substantial variation.
Formation of granules by artificial means was assessed by Wirtz and
Dague (1996) by using three different enhancement techniques. Granu-
lar activated carbon (GAC), powdered activated carbon (PAC), and cat-
ionic polymer were used in three different ASBRs at 35 °C. The fourth
reactor was used as a control unit with no chemical addition. The HRT
was maintained at 24 h, but the OLRs were increased from 3 to
12 kg/m3-d by increasing the synthetic sucrose concentrations. The cat-
ionic polymer enhancement took minimum of 108 d to reach the max-
imum loading rate of 12 kg/m3-d as compared to other three reactors.
Moreover, considerable granulation was observed by using cationic
polymer only within a period of 30 d, and after 60 d of stable operation,
around 95% removal in COD was observed at an OLR of 6 kg/m3-d.
In early 2000, extensive research was conducted by Daniel I Masse
and Lucie Masse in case of slaughterhouse effluent. In one such research,
Massé et al. (1999) collected the wastewater sample from six different
Canadian slaughterhouses. They collected two different types of anaer-
obic sludge (granular and flocculant) that can be used in 4 anaerobic se-
quencing batch reactors, each having a volume of 42 l. Reactor 1st and
2nd were fed with the granular sludge, while reactor 3rd and 4th with
flocculant one. The ASBRs were operated at 30 °C for varying OLRs
(1.1–11.5 kg COD/m3-d), and the results are shown in Table 6. Excellent
removal in COD, protein, and TSS were observed at all three loading
rates. Apart from that, no accumulation of VFAs were observed, which
resulted in considerable production of methane (74%) having a meth-
ane yield of 0.54–0.67 l/g VS in the entire research period.

Table 5
Removal efficiencies for two large scales UASB reactor.

Reactor OLR CODI CODE Removal O&GI O&GE Removal

(kg COD/m3-d) (mg/l) (mg/l) (%) (mg/l) (mg/l) (%)

UASB (1600 m3) 0.88–1.64 2030–3350 440–646 78–80 413–645 130–193 68–70
UASB (800 m3) 0.86–2.43 988–2774 104–400 70–92 140–460 27–134 27–58

CODI - Influent COD; CODE - Effluent COD; O&GI - Influent O&G; O&GE - Effluent O&G.
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
Table 6
ASBR's performance with varying COD, protein, and TS concentrations for both granular and flocculant sludge samples.
Run Sludge type CODI CODE Removal
(%)
1 Granular 6908 1511 78
Flocculant 1450 79
2 Granular 9665 1842 81
Flocculant 880 91
3 Granular 11,530 601 95
Flocculant 365 97
CODI - Influent COD; CODE - Effluent COD; ProteinI - Influent Protein; ProteinE - Effluent Protein; TSI - Influent TS; TSE - Effluent TS.
Another research of Massé et al. (2001), focussing on slaughterhouse
wastewater was conducted to evaluate the start-up performance at am-
bient temperatures (20 °C and 25 °C). The study confirmed that 136 and
168 d were ample enough for starting the ASBR at 20 °C and 25 °C re-
spectively. The OLR was increased swiftly from 0.46 to 2.34 kg/m3-d
just within a period of 20 d. As a result of that, decrease in methane pro-
duction was observed. Therefore, the loading rates were lowered to 1.12
and 1.57 kg/m3-d for 20 °C and 25 °C respectively. Thereafter, the load-
ing rates were increased gradually in order to allow complete degrada-
tion of the organic content. Methane production was almost 0.3 l/g-COD
at 2.6 kg/m3-d (20 °C) and 3 kg/m3-d (25 °C) respectively. Moreover,
above 90% of SCOD and 77% average SS removal were achieved at
both the temperatures. The limiting factors observed were the particu-
late matter hydrolysis at 25 °C and reduction of VFAs and soluble com-
pounds at 20 °C.
Massé and Masse (2001) examined the influence of temperature
and loading rates by installing 4 ASBRs in case of slaughterhouse waste-
water. Each reactor was operated at 30 °C, 25 °C, and 20 °C for 80 d,
137 d and 469 d respectively. At all the operating temperatures and
maximum OLRs (4.93, 2.94, 2.75 kg TCOD/m3-d), the TCOD and SCOD
removal efficiencies were exceptional (N90%). However, suspended
solids concentrations can cause turbulence, and may hinder the settling
process as a result of its slow degradation. Nevertheless, around 91%,
80%, and 86% SS were removed at operating temperatures of 30 °C, 25
°C, and 20 °C respectively. Maximum percentage of methane (78%)
was observed at 20 °C as compared to 25 °C (76%) and 30 °C (74%).
The reason for that behaviour was the increased solubility of H2 and
CO2 at lower temperatures. Hence, increase in concentration of methane
was observed as a result of their ultimate conversion to methane by hy-
drogen utilizing bacteria. Similar results of increased methane concen-
trations were observed by Massé and Croteau (1999) treating swine
manure. In order to evaluate the effect of shock load on the performance
of ASBRs treating slaughterhouse wastewater, Masse and Massé (2005)
applied soluble shock loads at 20 °C. The experiments were conducted
in four 42 l ASBRs. Two reactors were operated under varying shock
loads, while the other two received normal loading rates (2.60 ±
0.36 kg/m3-d). In soluble shock load, two experiments S1 and S2 were
conducted. In S1, two separate shock loads on day 8 (4.22 kg/m3-d)
and day 12 (7.93 kg/m3-d) were applied, while in S2, three successive
shock loads on day 33 (8.95 kg/m3-d), day 35 (7.55 kg/m3-d), and 37
(9.32 kg/m3-d) were applied to the reactors. In both the experiment in-
creased soluble loading rates resulted in increased effluent SCOD, SS,
VFAs (acetic acid, propionic acid, and isovaleric acid), NH4, alkalinity,
and pH. On the other hand, a decrease in methane yield was observed
with increased loading rates. However, under normal operating condi-
tions (OLR-2.60 ± 0.36 kg/m3-d), all the effluent parameters of shock
load reactors were similar to those of control reactors expect for meth-
ane yield which was higher in case of shock load reactors.
Masse et al. (2001) also evaluated the degradation of fat particles by
using NaOH and three different lipases of animal, plant, and bacterial or-
igin by conducting the experiments in 1 l beakers. Slaughterhouse
wastewater and distilled water (fats fragments) were mixed in a ratio
of 50:50, and were used as a substrate source. The results showed that
689
ProteinI ProteinE Removal TSI TSE Removal
(%) (%)
288 66 77 4892 2959 40
78 73 2091 57
530 95 82 6098 3381 45
73 86 1742 71
514 33 94 7121 1630 77
16 97 1457 80
animal lipase was very effective in removing fat particle (60%) than
any other lipases and NaOH.
Temperature plays a crucial role in anaerobic digestion process.
Higher temperature results in increased bacterial activity and substrate
removal (Dague et al., 1998). Rate of biochemical reaction gets doubled
for every 10 °C rise in temperature, but over a constrained temperature
range (Barber and Stuckey, 1999; Sawyer et al., 2003). At mesophilic
temperature (35 °C), Ruiz et al. (2001) carried out a study on a waste-
water coming from a slaughterhouse located in Narbonne (France).
The influent wastewater going to ASBR (3.5 l) was of following charac-
teristics: TCOD - 3.5-4.5 g/l, SCOD – 1.5-3 g/l, SS – 0.5-3.5 g/l. The OLR
applied after the feeding of the sludge was 0.6 kg COD/m3-d at an HRT
of 3.5–4.5 d. The loading rates were applied gradually, and the maxi-
mum loading rate (6.1 kg COD/m3-d) was applied at an HRT of 15 h
only after the passage of around 90 d. The result showed that the reactor
was efficient up to loading rate of 4.5 kg COD/m3-d with the removal ef-
ficiency of 86% and 91% for TCOD and SCOD respectively.
Bouallagui et al. (2009) studied the effect of mesophilic and thermo-
philic temperatures on performance of ASBRs treating SWW and fruit
and vegetable waste (F&VW). The research was conducted in 6 labora-
tory scale ASBRs each having an effective volume of 2 l. Three reactors
RI, RII, RIII were operated at mesophilic temperature (35 °C), while
RIV, RV, and RVI were operated at thermophilic temperature (55 °C).
Reactors RI and RIV were fed with SWW, RII and RV with F&VW, and
RIII and RVI with SWW F&VW. The reason for co digesting SWW and
F&VW was to increase Carbon/Nitrogen ratio (22.5). The results ob-
tained confirmed that the production of biogas was dependent upon
system's temperature and HRT. Biogas production at thermophilic tem-
perature (HRT-20 d) was much better than mesophilic temperature at
the same HRT.
In addition to that, temperature can also incite increased ammonia
concentration in anaerobic processes. According to Gallert and Winter
(1997), excessive NH3 concentrations can greatly hindered methane
production. At elevated temperatures (N50 °C), the production of meth-
ane can be inhibited by 50% as a result of ammonia inhibition. On the
other hand, with the decrease in temperature increased production in
alkalinity was observed as a result of degradation of protein to ammo-
nia, which shortly combines with carbonic acid to form ammonium bi-
carbonate (Cuetos et al., 2008). All in all, HRT and temperature plays a
crucial role in anaerobic digestion processes, and in order to protect
the system from overloading and failure the HRT should be changed ac-
cording to the temperature or vice versa.
Effect of varying HRT (16, 12, and 8 h) on the performance of ASBR
was also examined by Myra et al. (2015). The experiment was
conducted at laboratory scale in an effective volume of 10 l ASBR at
27–32 °C. Maximum COD removal was observed at 16 h HRT (97%) hav-
ing an average effluent value 83 mg/l. This value was in compliance with
the effluent discharge standard of Philippines (100 mg/l), while the con-
centrations obtained at other HRTs (12 and 8 h) failed to compliance
with the standard value. At 16 h HRT, biogas production was 2.7 l/d hav-
ing a methane content of 61%. TSS removal was not affected by the
change in HRT and the effluent value was well below 70 mg/l of pre-
scribed standard.
690 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708

Handous et al. (2017) recently carried a research for improving the
biogas generation in ASBR by co-digesting the effluent wastewater
(WW) and solid waste (SW) of a Tunisian slaughterhouse. Five ASBRs
(R1, R2, R3, R4, and R5) with 1 l capacity were selected for the experi-
mental work. Production of biogas (l/day) at all the loading rates for
R1, R2, R3, R4, and R5 were 0.43–1.76, 0.38–1.61, 0.4–1.21, 0.51–1.74,
and 0.35–0.73 respectively. The result confirmed that the production
of biogas was improved in R4 which was pre-treated with bacterial
flora, even though the mixture used in R4 was same as that of R3. Fur-
thermore, around 125,500€/year of net profit can be obtained by pre-
treating the waste before an anaerobic process.
Numerous other high rate digesters such as anaerobic fluidised bed
reactor, anaerobic baffled reactor, anaerobic membrane bioreactor, ex-
panded granular sludge bed reactor, continuously stirred tank reactor,
and static granular bed reactors have been implemented in the treat-
ment of slaughterhouse waste. Table 7 shows the case studies of such
reactors that have been used mainly in the treatment of slaughterhouse
effluent over the past few decades.
5. Aerobic treatment for slaughterhouse wastewater
Aerobic digestion takes place in the presence of oxygen with the
help of mixed culture of heterotrophic and autotrophic microorganisms.
Heterotrophic microbes utilize organic compounds as their carbon
source, while autotrophic microbes consume inorganic carbon such as
CO2. The mixed aerobic consortium degrades the organic matter and
ammonia into less harmful compounds like CO2, H2O, nitrite (NO−2),
and nitrate (NO−3), and with considerable production of new cells. Gen-
erally, oxidation with synthesis and endogenous respiration are the two
main steps in aerobic degradation.
Due to increased oxygen demand and treatment time require-
ment, aerobic processes are mainly installed after anaerobic pro-
cesses (Al-Mutairi, 2009; Bustillo-Lecompte and Mehrvar, 2017a).
The process is feasible to be applied to low strength wastewater
(COD b1000 mg/l) (Chan et al., 2009). The system is very efficient
in eliminating pathogens and awful odours from the wastewater as
well. (Arvanitoyannis and Ladas, 2008; Skjelhaugen and Donantoni,
1998). Excess biomass production, daily maintenance, and increased
oxygen demand are the main drawbacks. Additionally, biological
sludge must be treated before its final disposal. Nevertheless, excel-
lent organic matter and nutrients (N&P) removal can be achieved by
this method (Bustillo-Lecompte and Mehrvar, 2015; Chernicharo,
2006). Conventional biological nitrogen removal is achieved by nitri-
fication and denitrification, while phosphorous removal is accom-
plished by enhanced biological phosphorous removal (EBPR) in
anaerobic and aerobic cycles (Zeng et al., 2004).

Table 7
Implementation of high rate anaerobic digester's in slaughterhouse industry.

Temperature Waste Reactor Volume Loading rates HRT Influent COD TCOD SCOD VS CH4 References
(°C) (l) (mg/l) (%) (%) (%) (%)

35 SMWWa Fluidised bed reactor 2 1.8–9.5 kg – 2500–5000 71–76 – – 55–78 Stephenson and
COD/m3-d Lester, 1986
35 SWWb Fluidised bed reactor 0.5 0–12 kg 8h 340–680 – 75 – – Toldrá et al., 1987
SCOD/m3-d
– SWWb Fixed bed reactor 4.58 2–18.5 kg 5–0.5 d 7500–30,000 30–85 – – 70 Tritt, 1992
COD/m3-d
b
25–35 SWW Baffled reactor 5.16 0.67–4.73 kg 26–2.5 h 490–730 71–90 80–94 – 69–73 Polprasert et al.,
COD/m3-d 1992
35 SWWb Down flow fixed bed reactor 1 2.5–25 kg – 4700–28,700 – 98–50 – 58 Borja et al., 1995a
COD/m3-d
35 SWWb Fluidised bed reactor 1 2.9–54 kg 8–0.5 h 250–4500 75–99 – – 59–78 Borja et al., 1995b
COD/m3-d
a
15–35 SMWW Baffled reactor 10 – 20 h 4000 – 83–97 – 67–70 Nachaiyasit and
Stuckey, 1997
c
35 SFW Continuously stirred tank reactor 3 1–4.6 kg 45–18 d – – – 68% – Salminen and
VS/m3-d Rintala, 1999
35 SWWb Expanded granular sludge bed 2.7 2.1–15.8 kg 19–5.2 h 1440–4200 47–91 – – – Núñez and
reactor COD/m3-d Martínez, 1999
30 SWWb Membrane bioreactor 7 6–8 kg 1.2 d 5800–20,150 97 – – – Fuchs et al., 2003
COD/m3-d
d
33–39 FWW Membrane bioreactor 400 2–4.5 kg 16–100 h 2000–15,000 81–94 – – – He et al., 2005
COD/m3-d
37 SWWb Membrane bioreactor 50 4.37–13.27 kg 3.33–1.25 5440–15,500 – 62–97 – – Saddoud and Sayadi,
COD/m3-d d 2007
34 SSWe Completely mixed stirred digester 3 0.9–1.7 kg 50–25 d – – – 77–79 64–66 Cuetos et al., 2008
VS/m3-d
f
34 SMW Completely mixed stirred digester 3 1.85–3.7 kg 50–25 d – – – 81–83 59–65 Cuetos et al., 2008
VS/m3-d
b
22 SWW Static granular bed reactor – 0.64–4.97 kg 60–36 h 4200–9100 85–98 – – – Debik and Coskun,
COD/m3-d 2009
30–35 SWWb Anaerobic hybrid reactor 1.77 0.76–20.24 kg 24–4 h 760–4200 64–95 – – – Farooqi et al., 2009
COD/m3-d
36 PLg Continuously stirred tank reactor 17 – 30 d – – – – 31–67 Fantozzi and Buratti,
2009
b
38 SWW Anaerobic digester 2 0.5–4.5 g COD – 8450–41,900 18–57 – – – Marcos et al., 2010
37 SWh Continuously stirred tank reactor 6.2 – 31–10 d 40,500 57–77 – – 74 Marcos et al., 2012
37 SWWb Membrane bioreactor 200 3–3.5 kg 2d 5919–10,604 95 – – 70 Jensen et al., 2015
COD/m3-d
26 SWWb Acidogenic reactor (AR) AR = 0.4–0.7 kg – 13,500 32–69 – – – Wang et al., 2018
methanogenic reactor (MR) 40 COD/m3-d
MR =
87

SMWWa - Synthetic meat wastewater; SWWb - Slaughterhouse wastewater; SFWc - Slaughterhouse food waste; FWWd - Food factory wastewater; SSWe - Slaughterhouse solid waste;
SMWf - Slaughterhouse municipal waste; PLg - Poultry litter; SWh - Slaughterhouse waste.
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
Nitrification is the oxidation of inorganic nitrogen (NH3/NH4) to ni-
trite (NO−2) and then to nitrate (NO−3) by autotrophic microorganisms
(ammonia oxidizing and nitrite oxidizing bacteria) under aerobic condi-
tions. Thereafter, NO−3 under anoxic conditions get transformed into ni-
trogen gas (N2) with intermediate compounds as NO−2, N2O, and NO by
heterotrophic microorganisms (denitrifying bacteria) (Pan et al., 2013).
Nitrification requires oxygen demand, while denitrification sometimes
necessitate additional carbon source. Thus, recent studies have con-
ducted to make the process more economical and feasible. Novel pro-
cesses such as nitritation-denitrification, nitritation-denitritation,
nitritation-anammox have been performed recently (Winkler and
Straka, 2019). Each process has its own limitations and advantages. In
nitritation and denitrification process, partial nitirifation of NH3 to
NO−2 is carried out under limited oxygen supply. The process can reduce
the aeration cost by 25% as compared to conventional nitrification (Peng
and Zhu, 2006). Moreover, the technique can be further enhanced by di-
rectly converting the NO−2 into N2 gas by denitrifying polyphosphate ac-
cumulating organisms (DPAOs). The process can save additional carbon
source as DPAOs can denitrify in the absence of additional carbon. The
so-called process is known as nitritation-denitritation. The most recent
technique for nitrogen removal is Nitrititation-anammox process. Here
ammonia oxidizing bacteria converts half of ammonia into nitrite, and
then anammox uses that nitrite as an electron acceptor for converting
rest of ammonia into nitrogen gas. It possesses advantages such as com-
plete ammonia removal, less oxygen demand (60%), no carbon source
requirement, and less sludge production (75%) (Winkler and Straka,
2019).
Biological phosphorous removal is also dependent upon cyclic an-
aerobic and aerobic conditions. Polyphosphate accumulating microor-
ganisms (PAOs) utilize organic matter like VFAs and store them as
poly-hydroxyalkalanoate (PHA)/poly-hydroxybutyrate (PHB) in anaer-
obic conditions. The energy required for metabolizing comes from
breaking their polyphosphate bonds, and thus they release excessive or-
thophosphate. In limited organic carbon PAOs compete with
denitrifying microorganisms. Subsequently in aerobic conditions PAOs
utilizes stored PHA/PHB for growth and synthesis resulting in ortho-
phosphate uptake. Orthophosphate uptake is greater than its release,
and thus they are removed from the system by withdrawing certain
amount of sludge (Pan et al., 2013; Tanwar et al., 2007). Phosphate up-
take is also possible by DPAOs under anoxic condition in the presence of
NO−3/NO−2 (Monclús et al., 2010; Sengar et al., 2018a). Additional to that
aerobic granulation is also a latest technique for simultaneous removal
of nutrients. Hence, employing biological treatment with varying anoxic
and aerobic cycles can further reduce organic matter and nutrients con-
centrations. The aerobic case studies are thus reviewed to better present
their feasibility in the removal of organic and inorganic content from
slaughterhouse wastewater.
5.1. Aerobic ponds/Lagoons
The most common aerobic treatment process used in the treatment
of SWW is aerobic ponds/lagoons. The sole difference between ponds
and lagoons is the type of aeration provided. Artificial aeration is pro-
vided in lagoons, while photosynthesis process provides considerable
amount of oxygen in aerobic ponds. Maximum organic matter removal
(90–95%) can be observed from aerobic ponds/lagoons. However, due
to improper settling elevated concentrations of suspended solids can
be observed from these systems. Additionally, treatment time and oxy-
gen requirement largely depends upon influent wastewater character-
istics (Mittal, 2006).
In treating slaughterhouse wastewater, ponds and lagoons have
been usually employed after suitable anaerobic treatment. Hence,
limited studies are available in treating raw slaughterhouse waste-
water by these processes. A 1000 m3 aerobic lagoon was monitored
by Belanger et al. (1986) in the treatment of slaughterhouse waste-
water. Influent BOD concentrations varied between 1500 and
691
3000 mg/l. Oxygen was transmitted by 24 submerged emitters at a
rate of 850 l of O2/min. The lagoon effectively removed the organic
content at an average HRT of 11 d, and the effluent concentrations
of BOD were mostly below 50 mg/l. Apart from that, sludge genera-
tion was observed to be a prominent issue, and thus trained techni-
cians were employed for that.
Apart from that, Evans et al. (2005) evaluated the performance of
pilot scale high rate algal ponds on varying nitrogen loading rates. The
results showed that deeper ponds were much better in removing am-
monia as compared to shallow ponds. Moreover, excellent denitrifica-
tion efficiency (95%) was also observed when the slaughterhouse
wastewater was passed through a series of 3 ponds. Intermediate
pond acted as anaerobic/anoxic unit.
Evaporative ponds have also been used in treating slaughterhouse
waste like hide curing wastewaters. Evaporite salts are formed in such
ponds, and in few instances, increased concentrations of hazardous
metals were also observed (Tanji et al., 1992). Overall, aerobic ponds
are best suited as a post treatment unit where land availability and en-
vironmental conditions are appropriate.
5.2. Constructed wetlands
Constructed wetlands (CWs) are those systems that involve the use
of soil, wetland vegetation, microbial groups and all other natural pro-
cesses to treat domestic and industrial wastewaters. Constructed wet-
lands are specifically implemented to treat wastewaters after primary
and secondary treatment units (Vymazal, 2014). They are compara-
tively economical than other treatment options because of their simpler
design, lower operation and maintaining cost, and their harmless effects
on the environment (Chan et al., 2009; Oller et al., 2011). Constructed
wetlands are divided into subsurface flow and surface flow wetlands.
Moreover, depending upon the direction of flow they are further classi-
fied as vertical and horizontal flow wetlands. Subsurface wetlands due
to the presence of gravel, sand, and stones achieve higher pollutant re-
moval efficiencies as compared to surface flow wetlands (Odong et al.,
2015). Apart from that, their bottom stratum and slid slopes are covered
with a help of polyethylene plastic cover, which prevents the wastewa-
ter to get percolated into lower water table. First full scale application of
wetland was done in late 1960's (Vymazal, 2014). Application of wet-
land system started with municipal wastewater, but now wetlands are
used to treat industrial, agricultural and leachate waste water as well
(Vymazal, 2011).
Russell et al. (1994) evaluated the feasibility of surface flow wet-
lands for the removal of nitrogenous compounds especially nitrate.
The denitrifying activity was prevailed inside the surface of decaying
plant material. The result showed that proper contact between decaying
material and wastewater can further enhance the denitrification rate.
Van Oostrom (1995) also examined the feasibility of constructed wet-
land in treating nitrified slaughterhouse wastewater. Denitrification
accounted for 87% nitrogen removal, while remaining 13% through
plants and sediments assimilation.
Performance of full scale wetland system for treating slaughterhouse
wastewater was evaluated in Mexico (Gutiérrez-Sarabia et al., 2004).
Sedimentation tank, anaerobic lagoon and constructed wetland were
placed in series in the treatment unit. Overall removal efficiencies
achieved were 91% (BOD5), 89% (COD) and 85% (TSS). However, only
30% organic matter reduction was achieved in wetland system, which
was having 12 mm gravel size. On the other hand, certain pathogens
were also removed by the presence of Phragmites australis and Typha
latifolia plants.
Excellent pollutant removal efficiency was achieved by
Struseviciene and Strusevicius (2006) in two stage horizontal con-
structed wetlands while treating wastewater from a slaughterhouse in-
dustry. Primary treatment removed considerable amount of impurities
from the wastewater, while secondary biological treatment (con-
structed wetlands) provided the effluent that can be easily discharged.
692 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
To evaluate the performance of vertical flow constructed wetlands
and membrane bioreactor (MBR) a study was conducted by Scholz
(2006). Animal rendering wastewater was effectively treated in both
the cases after a pre-treatment (DAF). Wetlands proved to be as effec-
tive as membrane bioreactors, and the effluent COD and ammonia ob-
tained in case wetland were 167 mg/l and 63 mg/l respectively.
Soroko (2007) conducted two experiments to evaluate the removal ef-
ficiencies of wetlands while treating slaughterhouse wastewater. In the
first experiment, combination of two vertical flows and one horizontal
flow constructed wetlands were used, while in second experiment sin-
gle vertical flow and horizontal flow wetlands were employed. Nitrogen
removal efficiency obtained were 78% and 97% from first and second ex-
periment respectively. Additionally, it was reported in a study by
Gasiunas et al. (2005), that efficiency of organic pollutant and nutrient
removal depends on loading rates. Furthermore, physical and chemical
characteristics of the sand medium influence the phosphorus removal.
Average efficiency of total nitrogen removal obtained from that study
was between 37 and 44%.
To study the effect of temperature on wetlands a study was con-
ducted by Carreau et al. (2012) in Canada. The surface flow wetlands
were planted with Typha latifolia plants to treat the slaughterhouse ef-
fluent. Active volume taken was 89% with hydraulic retention time of
111 d. The results acquired from the system encouraged the implemen-
tation of wetlands in colder climates as well. The removal efficiencies re-
ported were quite high for both organic and inorganic contents. About
95% BOD, 72% TSS, 88% total phosphorous (TP), and 87% total kjeldahl
nitrogen (TKN) removal was achieved from constructed wetlands in a
span of two years. Two consecutive oxidation ponds were used to
treat high strength hog slaughterhouse wastewater (Poommai et al.,
2015). Ponds were found insufficient to meet the desired effluent stan-
dards. Vertical flow constructed wetland was used in addition and the
effluent quality was found to be little improved. However, the overall
treatment scheme was insufficient to meet the standards due to high
strength of wastewater comprising of grease, hairs, solids, and blood.
Odong et al. (2015) have used a horizontal subsurface flow con-
structed system to treat the wastewater by planting each Cyperus papy-
rus plant in 1m2 area. The horizontal wetland was fed with
slaughterhouse wastewater after pre-treating it with anaerobic and aer-
obic sequencing batch reactors (SBRs). At an HRT of 1.16 d, the COD,
total nitrogen (TN), TP, and turbidity removal efficiency obtained were
60%, 46%, 63%, 76% respectively. Apart from that, 100% faecal coliform
removal was observed from horizontal subsurface wetland system as
well. The authors strongly emphasized the implementation of con-
structed wetlands as a tertiary treatment unit in case of slaughterhouse
effluent.
5.3. Trickling filters
Trickling filter (TF) is one of the fixed bed reactors in which different
media of high permeability is used for microorganism's growth. Media
can be a rock or plastic of varying surface area. Generally, to achieve
higher loading rates and to prevent blockage, a media with high surface
area is employed. A slim layer comprising of microorganisms is then de-
veloped on that surface media. Distribution system is used to allow
wastewater to enter into bioreactor, where the wastewater is then
trickled over the media surface (Daigger and Boltz, 2011). Bacterial bio-
mass present on the media degrades the organic content in the presence
of oxygen. However, due to increased thickness of slim layer results in
insufficient oxygen transfer, and thus sloughing of bacterial biomass
can then be observed from media surface. Advantages of trickling filter
are low operational cost, minimal space and power requirement, and
near to ground cost requirement (Johns, 1995). In spite of numerous ad-
vantages its application as a secondary treatment unit in the treatment
of slaughterhouse effluent is limited, especially in countries like US and
Australia.
Phillips (1975) reported the implementation of one high rate trick-
ling filter followed by two sequential biofilters. Moreover, primary
treatment (flocculation and sedimentation) was also provided to reduce
the loading rate on trickling filters. The results showed that under con-
trolled conditions around 95% BOD removal can be achieved. Clogging of
filter media occurs due to high concentration of proteinaceous com-
pounds, which results in declined reactor's performance (Azad, 1976).
However, with suitable pre-treatment and plastic media usage, consid-
erable reduction in organic matter can be observed. According to
Moodie and Greenfield (1978), about 50% suspended COD discharged
from Brisbane slaughterhouse facility was treated by employing a pre-
liminary treatment.
A pilot plant comprised of primary (DAF) and secondary treatment
unit (two stage trickling filters) was set up by Li et al. (1984). Each trick-
ling filter was 2.4 m high and consisted of media (surface area-
98 m2/m3). Around 40–50% oil and grease removal were achieved
from DAF system. In case of trickling filters organic matter removal effi-
ciencies were 70–85%. Apart from that, nitrification also resulted, but
the process was entirely dependent upon loading rates.
Intensive studies by Banks and Wang (2004) have shown that load-
ing rates plays a vital role in biological treatment. Intensive studies con-
ducted by them have shown that the organic matter removal
efficiencies were 60–85% when operated at OLRs of 1.2–8.1 kg BOD/
m3-d for nine trickling filters.
5.4. Activated sludge process
In early 1900s, activated sludge process (ASP) was developed by
Ardern and Lockett, and up till now it is one of the most common waste-
water treatment technologies due to its simplicity and low cost treat-
ment techniques (Zhao et al., 2018). Treatment of wastewater takes
place inside a bioreactor (aeration tank), in which oxygen is provided
for degrading the organic content with the help of aerobic microorgan-
isms (Fig. 3(a)). Contaminants are adsorbed on the surface of biomass,
and thus get oxidized in the presence of oxygen. This process of adsorp-
tion is an integral step in the biodegradation process of organic content
(Seyhi et al., 2011). Thereafter, the treated effluent along with sludge
(activated sludge solids) enters into clarifier for its further separation.
A certain amount of mixed liquor suspended solids (MLSS) is required
inside bioreactor for maintaining a desirable F/M ratio. Hence, the set-
tled sludge in the clarifier is recycled back to the aeration tank for main-
taining the required ratio and MLSS concentrations. And finally, the
treated water can be collected from clarifier's effluent.
In early 1980s, implementation of ASP in the treatment of slaughter-
house waste was soared tremendously, and numerous ASP plants were
installed worldwide in order to remove both organic and inorganic con-
tent. However, in some cases due to the presence of fats in slaughter-
house effluent poor settling of the activated sludge have been
reported widely (Hopwood, 1977). Additionally, dissolved oxygen
(DO) is another factor that plays a crucial role in degrading fat content.
90% removal in fat content was observed when DO was increased up to
4 mg/l, whereas about 60% removal was obtained when the value of DO
was reduced to b0.5 mg/l (Travers and Lovett, 1984). Nevertheless,
under similar DO (lower) concentration but with lower fat content no
such issue of sludge bulking was perceived (Johns, 1995). Apart from
that, attached growth systems are more vulnerable to fat content than
suspended growth systems (Heddle, 1979).
Heddle (1979) conducted a study to evaluate the performance of
ASP by varying F/M ratios. It was done to observe the COD, nitrogen,
phosphorus, oil and grease, and suspended solids removal efficiencies.
Moreover, production of biomass and consumption of oxygen were
the foremost objectives of that research. Lower F/M (0.2–0.4) proved
beneficial as compared to higher F/M ratios (1.8–2.0) in removing
COD (96%), TSS (95%), TKN (96%), phosphorus (47%), and O&G (94%).
Additionally, much less oxygen was utilized with concurrent production
of biomass, which was rich in protein (55%). Gariépy et al. (1989) on the
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708 693

(a). Schematic diagram of activated sludge process

(b). Schematic diagram of rotating biological contactor

(c). Schematic diagram of moving bed biofilm reactor

(d). Schematic diagram of intermittent sequencing batch reactor

Fig. 3. Schematic diagram representing: (a). Activated sludge process. (b). Rotating biological contactor. (c). Moving bed biofilm reactor. (d). Intermittent sequencing batch reactor.
694 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
other hand, obtained maximum protein content (78%) while treating
slaughterhouse waste.
Continuous and intermittent feeding strategy was examined by
Lovett et al. (1984) in 4 laboratory scale reactors. An aeration tank of
9 l and settling tank of 1 l was separated by an adjustable baffle. Three
reactors were operated continuously with slaughterhouse wastewater,
while the single reactor was fed intermittently with wastewater (8 h)
and tap water (16 h). The SRT was fixed to 5, 10, and 20 d for the
three reactors and 10 d for the last intermittent reactor by maintaining
mixed liquor volatile suspended solids (MLVSS) concentrations. The in-
termittent ASP was comparatively better in removing the impurities
from the wastewater. The COD, TKN, and phosphorous removal efficien-
cies were 98%, 96%, and 96% respectively for intermittent ASP, and 94%,
95%, and 60% respectively for continuous ASP at 10 d SRT.
ASP's have also been installed in the treatment of waste generated
from pig slurries. In Italy a pilot plant study was conducted by Bortone
and Piccinini (1991) for the treatment of waste generated from pig
farms. A post aerobic ASP was employed after an anaerobic baffled reac-
tor (ABR) for the desired treatment. The COD and TKN removal efficien-
cies were 82% and 92% respectively. Additionally, another research on
the treatment of pig slurry but at full scale was carried by Bicudo and
Svoboda (1995) in Portugal in mid-1990s. Four different aeration strat-
egies (19.5 h, 16.5 h, 14.5 h, and 12 h) were adopted in a modified acti-
vated sludge process i.e., extended aeration system. 12 h intermittent
aeration showed enhanced SCOD and soluble BOD(SBOD) removal effi-
ciencies of 85% and 98% respectively.
As slaughterhouse waste contains high fraction ammonia due to the
degradation of proteinaceous compounds, it must be treated before its
discharge. Campos et al. (1999) gradually increased the ammonia load-
ing rates from 0.5 to 7.7 kg NH4/m3-d at lab scale in order to observe ASP
performance. The findings confirmed the implementation of ASP in re-
moving nitrogenous compounds from the wastewater at large scale,
and about 97–99% of ammonia was effectively transformed to nitrate
by using a conventional ASP. O'Flynn (1999) too observed the removal
efficiencies of organic matter and inorganic impurities by installing a
pilot plant and comparing the results with a mathematical model. The
maximum COD, ammonia, and phosphorous removal efficiencies were
98%, 99%, and 65% respectively.
Using a chemical treatment with biological treatment (activated
sludge) has enhanced the level of treatment for abattoir wastewater
as reported in a study by Bohdziewicz et al. (2002). Aeration period of
10.5 h resulted in optimum treatment, giving COD removal efficiency
of 91.5% and nitrogen removal by 59%. Efficiencies were reported to be
dropped using aeration period less than or N10.5 h. Coagulant was
added simultaneously to achieve phosphorus precipitation.
In order to eradicate the issue of sludge bulking an improvement in
the existing ASP was done by incorporating different arrangements in
step feeding, tapered aeration, increased volume of aeration tank, and
especially by employing an aerobic selector. As a result of that, substan-
tial increase in settling was observed, which enhanced the effluent qual-
ity (Al-Mutairi, 2009).
Removal of certain drugs such as enrofloxacin and tetracycline from
slaughterhouse wastewater by using activated sludge was evaluated by
Table 8
Performance of ASP over the last two decades for slaughterhouse effluent.
Year Scale TCOD removal BOD removal
(%) (%)
2003 Full 96 97
2004 Lab 98 99.6
2006 Lab 92 – 92.5
2008 Full – 99
2009 Full 89 90
2011 Lab 97.6 – –
2012 Lab 97 – –
2015 Full 99 99
Carvalho et al. (2013). These pharmaceuticals were significantly re-
moved through sorption to sludge and to organic content of wastewater
in batch reactors. Study showed 68% removal of enrofloxacin and 72% of
tetracycline from the wastewater.
Slaughterhouse wastewater was also treated by using different se-
quential setup consisting of ABR, ASP system and UV/H2O2 photo reac-
tor at lab scale by (Bustillo-Lecompte et al., 2014). The results
illustrated that ABR ASP UV/H2O2 combination provided excellent
total organic carbon (TOC) removal (92.5%) at reasonable cost. Table 8
illustrates the implementation of ASP's in the last two decades.
5.5. Rotating biological contactor
Rotating biological contactor (RBC) is also another type of fixed film
biological reactor in which series of circular plastic discs or plates are
supported on a common horizontal shaft (Fig. 3(b)). This horizontal
shaft rotates the partially submerged disc (40%) in a tank or contactor
with the help of a power driven mechanism (motor) (Bull et al., 1982;
Oğuz and Oğuz, 1993). Discs in RBC are usually 2–4 m in diameter,
and generally made up by corrugated plastic material having sufficient
surface area for the growth of microorganisms (Najafpour et al.,
2005). Plates are sufficiently spaced up to 30–40 mm for suitable con-
tact reaction between substrate, oxygen, and microorganism. Bacterial
consortium grows rapidly on the surface of plates, and barely within a
period of one week, about 1–4 mm thick biofilm can be observed on
the plate surface. However, the thickness of the biofilm depends upon
the rotational speed of the plates and wastewater strength. Microorgan-
ism degrades the organic content present in the wastewater by consum-
ing oxygen from the atmosphere. Excessive growth of biomass is
inhibited due to the shearing effect of wastewater on the media surface,
and this result in sloughing of the biofilm. Low energy and maintenance
cost, minimal requirement of skilled workers, capable of handling vary-
ing organic loads, and simplicity in construction are the chief advan-
tages of RBC (Torkian et al., 2003a; Sirianuntapiboon, 2006).
Additionally, RBC consumes less energy than ASP system and also it
saves cost on capital investment due to no usage of pumps and recycling
systems (Bull et al., 1982). Nevertheless, in spite of numerous advan-
tages their execution in the treatment of slaughterhouse wastewater
is very limited (Bull et al., 1982; Bustillo-Lecompte and Mehrvar,
2015; Johns, 1995).
In early 1970s, a pilot scale study employing RBC as a post treatment
unit after an anaerobic lagoon was done by (Chittenden and Wells Jr.,
1971). Three stage configurations having 50 plates in each stage were
used in RBC. Furthermore, three tests were conducted by varying the
discharge and rotational speed of the shaft. The first test was conducted
for a discharge of 38 m3/d, and at a rotational speed of 3 rpm in all three
stages. The influent average BOD of 250 mg/l was reduced to 50% in the
first test. While in the second test the removal efficiency was increased
to 64.5% by solely increasing the shaft speed to 6 rpm (first stage only).
And in the third test by keeping the rotational speed constant the dis-
charge was reduced to 19 m3/d. The BOD removal efficiency as a result
of that soared up to 83%.
O&G removal TSS removal References
(%) (%)
88 93 Chen and Lo, 2003
– – Sroka et al., 2004
– Rosa et al., 2006
95 92 Al-Mutairi et al., 2008
– 94 Pabón and Suárez Gélvez, 2009
– Fongsatitkul et al., 2011
– Hsiao et al., 2012
– 94% Amanatidou et al., 2016
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
Johnson and Krill (1976) also evaluated the performance of RBC in
meat processing and slaughterhouse effluent. The wastewater was pre-
liminary treated in DAF system before its final secondary treatment. At
different hydraulic loading rates (0.112, 0.53, and 1.06 l/d-m2) the aver-
age BOD of 650 mg/l was effectively reduced to 95%, 83%, and 64%. Effect
of hydraulic loading rates on RBC was also evaluated by Oğuz and Oğuz
(1993) while treating meat packaging plant wastewater. A total of six
experimental runs were performed by varying the hydraulic loading
rates. The results confirmed that on increasing the loading rates from
38 to 76 l/d-m2 resulted in declined removal efficiency for both BOD
(80–56%) and TS (61–40%).
In order to assess the feasibility of RBC after an UASB reactor a re-
search was carried out by Torkian et al. (2003a). The study was per-
formed in 280 l pilot scale RBC (6 stage) at various rotational shaft
speeds and OLRs. The OLRs were varied from 5 to 18 g SBOD/m2-d in a
span of six experimental tests conducted. Here also similar results of de-
creased BOD removal efficiencies were observed with increased loading
rates. However, at 5.3 g SBOD/m2-d about 85% SBOD removal efficiency
was attained. And thus, the wastewater can be suitably discharged for
agricultural purposes at that particular loading rate.
Thus, it can be inferred that RBC performance largely depends upon
the influent wastewater concentration, organic and hydraulic loading
rates, shaft rotational speed, and number of stages or units installed in
RBC. Increased loading rates and wastewater strength can seriously af-
fect the removal efficiency of RBC. In general, to obtain appropriate
COD (b60 mg/l) and BOD (b25 mg/l) effluent concentrations, the RBC
must be functioned at 65 g COD/m2-d and 22 g BOD/m2-d of loading
rates respectively (Al-Ahmady, 2005). Moreover, according to Hassard
et al. (2015), the RBC system is also capable enough in removing nutri-
ents from the wastewater as well.
5.6. Moving bed biofilm reactor (MBBR)
Moving bed biofilm reactor (MBBR) is said to be a modification of
ASP system. The process was invented by Norwegian scientist in early
1990s (Zinatizadeh and Ghaytooli, 2015; Bassin et al., 2012). It com-
bines the benefits of both ASP and biofilm reactor. Polyethylene car-
riers having a density close to water are used as media in MBBR
(Borkar et al., 2013; Kermani et al., 2009). Unlike fixed film bioreac-
tors, MBBR involves the movement of bio-carriers in the entire sys-
tem to increase the contact area between substrates and biomass.
The movement can be achieved either by aeration or by mechanical
mixer depending upon type of bioreactor (aerobic or anaerobic)
(Fig. 3(c)). The leading benefits of MBBR are resistant to shock
loads, less volume requirement, no recycling or backwashing re-
quirement, no mechanical intervention required in case of load fluc-
tuations, and sufficient sludge retention time for both heterotrophic
and autotrophic microorganisms (Camp et al., 2001; Joslin and
Farrar, 2005; Zinatizadeh and Ghaytooli, 2015).
The ability of MBBR to resist shock loads was evaluated by Hosseini
and Borghei (2005) at lab scale. The authors concluded that MBBR was
very effective in removing the contaminants from the wastewater, in
spite of the fact that toxicity and hydraulic loading rates were varied
up to an extent. Moreover, it was stated that the problem of sludge
bulking was also prevented as a result of bio-carriers. Microscopic anal-
ysis confirmed the presence of filamentous bacteria only on the poly-
ethylene carrier, and no such bacterial accumulation was observed in
effluent wastewater.
Camp et al. (2001) stated that MBBR is capable enough in degrading
volatile organic compounds (VOC's) such as ethanol, methanol, acetone,
isopropanol, and ethyl acetate. The findings demonstrated that two
pilot stage MBBR systems were effective in removing 90% SCOD from
the wastewater. Joslin and Farrar (2005) on the other hand evaluated
the performance of two stage MBBR's at full scale while treating slaugh-
terhouse effluent. The MBBR's were used as pre-treatment units before
an activated sludge system. Pre-treatment through MBBR resulted in
695
increased treatment capacity, and N95% BOD was efficiently removed.
And that ultimately resulted in increased discharge of treated water
into nearby Norwalk river (US).
MBBR unit was installed in a meat processing plant to meet the new
US discharge standards (Colic et al., 2008). However, because of in-
creased plant capacity and high concentration of contaminants, MBBR
system was unable to perform satisfactorily. To enable the performance
of MBBR, flotation unit was installed to reduce TSS, O&G, and BOD to a
level that could be handled by MBBR. Additionally, about 50–80% of
BOD was removed from the flotation system.
Kermani et al. (2009) used a series of MBBR's (anaerobic, anoxic, and
aerobic) in order to remove both phosphorous and nitrogen at lab scale.
At steady state conditions 81% and 96% removal in total nitrogen and
phosphorous removal efficiency was obtained. Stover-Kincannon
model was used to analyse the behaviour of MBBR's with the experi-
mental results. Excellent regression value was attained from kinetic
analysis for both phosphorous (R2 = 0.9862) and nitrogen (R2 =
0.986) removal.
In order to tackle the quandary of conventional nitrogen removal
(nitrification and denitrification), Bertino (2011) developed partial ni-
trification (nitritation) process in a pilot scale MBBR. The removal effi-
ciencies acquired from the system were 83% and 95% for TN and NH4
respectively. DO pH, ORP, and conductivity proved to be crucial in mon-
itoring the reactor for 120 d.
Bassin et al. (2012) employed two lab scales MBBR's to assess the
time required in the development of microbial film on plastic media.
The first reactor (MBBRA) was inoculated with already acclimatized ni-
trifying sludge in order to estimate the acclimatization time required
when inorganic material is used as substrate. In contrast to that, the sec-
ond bioreactor (MBBRB) was fed with compounds comprising of both
organic and inorganic matter, and without acclimatized sludge.
MBBRA took around 60 d to develop a thin secured microbial film
while MBBRB acquired only 30 d to achieve a stable and thick biofilm
on polyethylene media. However, the rate of nitrification was almost
similar in both the cases, but only after the proper acclimatization and
attachment of the biomass.
Munir Baddour et al. (2016) estimated the performance of MBBR
system in the treatment of poultry slaughterhouse effluent. The study
initially calculated the system's performance in removing suspended
and dissolved impurities over the acclimatized phase. Almost after one
month the reactor was effectively removing 94% COD, 51% NO−3, 34% or-
thophosphate (PO−3 4 ), and 53% total dissolved solids (TDS) from the
wastewater.
Mannina et al. (2016) demonstrated the feasibility of combining
MBBR with membrane bioreactor (MBR) in the removal of nutrients
and carbonaceous compounds. A pilot scale study was done at different
sludge retention times (infinite, 30 d, and 15 d) during the course of re-
search. The pilot plant consisted of anaerobic, anoxic, aerobic bioreac-
tors, and an MBR tank. Only anoxic and aerobic reactors were fed with
plastic media. Despite the variation in SRT's, neither COD removal nor
nutrients removal was affected. The maximum COD, ammonia, total ni-
trogen, and phosphorous removal efficiencies were 99%, 97%, 90%, and
70% respectively. Apart from that, it was inferred that suspended bio-
mass culture was effective in removing carbonaceous compound,
whereas attached microbes were efficient in eliminating ammonia
from the wastewater.
5.7. Intermittent sequencing batch reactor
An intermittent sequencing batch reactor (ISBR) is implemented in
the removal of not only organic compounds but in the abstraction of ni-
trogen and phosphorous as well. It possesses copious advantages over
other conventional aerobic systems. Feeding, reaction, settling, and
decanting all takes place one after the other in one complete cycle. Aer-
obic, anoxic, and anaerobic conditions can be prevailed in a single batch
reactor for the removal of impurities particularly N&P (Fig. 3(d)).
696 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
However, the effluent characteristics depend largely upon aeration rate,
OLRs, HRT, SRT, MLSS, specific oxygen uptake rate (SOUR), temperature,
and F/M ratios. Moreover, COD/TN and COD/TP ratios are also significant
in order to remove nutrients.
Subramaniam et al. (1994) utilized two separate SBR's to treat
slaughterhouse effluent after anaerobic ponds. The sole difference be-
tween the two SBR's was the influent characteristics. The first SBR re-
ceived comparatively higher COD/TKN and SCOD/TP ratios. Thus, the
removal efficiency achieved as a result of that was 90%, 92%, and 95%
for TP, TKN, and COD respectively in the first reactor. In another similar
case study yet again two sequencing batch reactors were employed
after anaerobic ponds (Keller et al., 1997). Intermittent aeration strategy
was adopted for the removal of contaminants. More than 97% ammonia
removal and considerable elimination of nitrate and nitrite was ob-
served from bioreactors. Additionally, around 75–85% phosphorous
was also removed from post aerobic system.
Obaja et al. (2003) conducted an extensive research by installing an
SBR for the treatment of high strength ammonium rich compounds. A
total of four experiments were conducted with varying concentrations
of NH4 and PO−3 4 in a lab scale reactor (3 l). Anaerobic, aerobic, and an-
oxic conditions provided the effluent that was free from nitrogenous
compounds. The maximum percentage removals of ammonium, nitrate,
and phosphate in all the four experiments conducted were 99.7%, 99.9%,
and 97.8% respectively. Furthermore, effect of temperature was also
analysed, and it was concluded that SBR was efficient in removing
NH4 even at 16 °C.
Study on SBR running on SWW at 22 °C was done by
Thayalakumaran et al. (2003). Nitrogen, nitrite, and nitrate concentra-
tions were reduced to a value b10 mg/L, 1 mg/l, and 5 mg/l respectively,
while total phosphorus to a value b1 mg/L. Moreover, around 94%
suspended solids and 99% SCOD removal was also observed. Inverse re-
lationship of pH and alkalinity was reported during initial aerobic and
anaerobic stages. This is due to generation and stripping of carbon diox-
ide gas.
Marcinkowski et al. (2004) estimated the functioning of ISBR in case
of cattle slaughterhouse wastewater. The study demonstrated the feasi-
bility of partial nitrification (nitritation) and denitrification process in
the removal of nitrogenous compounds (200–600 mg/l) from a Danish
slaughterhouse (Denmark). ISBR having a working volume of 3 l was
operated at 35 °C for both aerobic (5 h) and anoxic cycles (3 h).
Ample nitrification and denitrification were observed with an average
removal efficiency of 72% (0.3 g NH4/g VSS-d) and 96% (0.042 g NO−2/g
VSS-d) respectively.
A recent and effective technique for the removal of nutrients is aer-
obic granulation (Sengar et al., 2018b). According to Zhang et al. (2016),
aerobic granules possess compact core like structure that are large in
size, and therefore are beneficial in treating industrial wastewaters. Aer-
obic granulation process has certain advantages such as low operation
expenses, no secondary clarifier requirement, adjustable to sudden
high loadings, and possibility of achieving denitrification in settle and
anoxic phases (Nancharaiah et al., 2016). Gao et al. (2011) also talked
about zonal distribution in granules based on DO gradient. There is ex-
istence of aerobic zone on the outside (for organic matter removal), ni-
trification zone in middle and at centre there is presence of anoxic-
anaerobic zone. Simultaneous phosphate and nitrogen removal is
shown by aerobic granules in many studies (De Kreuk et al., 2005;
Lemaire et al., 2008b; Bao et al., 2009; He et al., 2018).
Cassidy and Belia (2005) achieved simultaneous nitrogen and phos-
phorus removal by using granular sludge from slaughterhouse waste-
water. Settling time was reduced from 60 to 2 min, and granules were
developed within quick interval of 4 d. Granules of size 1.70 mm were
reported having 22 ml/g of sludge volume index (SVI). Removal effi-
ciency of nitrogen and VSS were over 97%, and of phosphate and COD
were beyond 98%.
Aerobic granules formation was also studied by Kishida et al. (2009)
by installing an ISBR (4.5 l) for treating synthetic and livestock
wastewater. Formation of granules was first observed in case of syn-
thetic wastewater. Thereafter, when the livestock wastewater (diluted)
was treated then also the development of granules was examined.
Moreover, removal of nutrients occurred in spite of excessive
suspended solids. However, for undiluted livestock wastewater the
treatment efficiency decreased with decline in granules structure. Nev-
ertheless, the efficiency soared again by improving the excess sludge
discharge techniques, and thus effective removal of nutrients was ac-
quired. Liu et al. (2015) also reported the formation of granules while
treating slaughterhouse wastewater. Maturation of granules was
achieved at lab scale after 90 d of operation. Removal efficiencies re-
ported were 95.1%, 83.5%, and 99.3% for COD, phosphate and ammonia
respectively. Specific oxygen uptake rate (SOUR) analysis was per-
formed, and it revealed that ammonia oxidizing bacteria (AOB) and ni-
trite oxidizing bacteria (NOB) were increased with granulation.
How carbon to nitrogen ratio (C/N) affects simultaneous nitrification
and denitrification (SND) was shown in a study by Chiu et al. (2007).
While having a ratio of 11.1 of COD/NH4, complete ammonium and
COD removal was obtained and nitrite was not present in the effluent.
With increase in the loading of ammonium, removal efficiency of nitro-
gen was found to be decreased. Besides C/N readily biodegradable to
soluble COD ratio also plays a key role in SND (Khursheed et al.,
2018). Hence, it should also be properly considered while removing ni-
trogenous compounds. On the other hand, DO concentration is also the
fundamental controlling factor. For complete nitrification a minimum of
2 mg/l DO is required (Gerardi, 2003; Sriwiriyarat et al., 2008). Micro-
bial consortium can be greatly influenced by the change in DO
(Cabezas et al., 2006).
An ISBR was used for improving water quality of shrimp aquaculture
(Boopathy et al., 2007). Nitrification and denitrification were achieved
by SBR on operation under sequential aerobic (2 d) anoxic (3 d), and
aerobic (2 d) cycles. In the course of research period, complete nitrifica-
tion and denitrification was achieved. Furthermore, the COD removal
efficiency from ISBR was about 97%.
Study was made on SBR running on intermittent mode and treating
SWW (Li et al., 2008b). In the react phase, intermittent aeration was
provided for four times for 50 min, and having an interval of 50 min at
0.80 L/min of air supply rate. Influent concentration of impurities was
reported as, COD - 4672 mg/L, TN - 356 mg/L and TP - 29 mg/L with
minor variation. Removal efficiency achieved was 96% for both COD
and TN, and 99% for TP. Additionally, it was discovered that 66% nitrogen
was removed because of denitrification, while the rest (34%) due to bio-
mass synthesis.
Enhanced denitrification was achieved by using low DO level in lab
scale SBR by Zhan et al. (2009). Study on nitrogen removal was per-
formed by using intermittent and continuous aeration operating strat-
egy. It was found that, 95% of total nitrogen was removed while
operating the SBR on intermittent mode, while continuous aeration
strategy yielded nitrogen removal of 91%. Moreover, in continuous aer-
ation mode, pre-denitrification was done and low DO levels were ap-
plied to achieve nitrogen removal from SWW. Furthermore, 65%
savings were reported in electricity consumption by maintaining low
dissolved oxygen content under intermittent mode strategy. Apart
from that, COD and SS removal efficiencies in both the cases were
over 99%.
SBR was used to treat SWW for producing effluent having desirable
levels of phosphorus and nitrogen for irrigation purpose (Pijuan and
Yuan, 2010). The chief purpose of the study was to accomplish denitri-
fication process by the means of nitrite as an electron acceptor instead
of nitrate. As a result of that, considerable reduction in additional carbon
source and oxygen was observed. The results showed that oxygen and
carbon source requirements were reduced by 25% and 40% respectively.
Additionally, the TCOD (77%), TKN (83%), and TP (66%) were efficiently
removed from the wastewater.
In order to estimate the performance of SBR at different aera-
tion rates, Pan et al. (2014a) carried out an investigation at
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708 697

aeration rates of 0.40, 0.60, and 0.80 l air/min. Three intermittent
SBRs each having 8 l working volumes were operated at an average
loading rate of 0.61 kg COD/m 3 -day. Cycle duration chosen was
12 h, and efficient COD (98%), TN (98%), and TP (96%) removal
was obtained at 0.60 l air/min. Also, elevated nutrients removal
was observed at lower aeration rates (0.40 and 0.60 l air/min).
However, lower dissolved oxygen can influence the production of
nitrous oxide (N 2 O) in conventional nitrification-denitrification
processes. N2O is considered to be the leading cause of ozone de-
pletion, and therefore a primary greenhouse gas (Adouani et al.,
2010). Pan et al. (2014b) demonstrated that the percentage of
N 2O depends upon the influent TN concentration. About 6–11%
N2O was liberated at 576 mg/l TN concentration. Additionally, as
the aeration rates were increased from 0.4 l air/min to 0.8 l air/
min in intermittent SBR, N 2O emission/incoming total nitrogen
ratio was decreased by 48.2%.
Table 9 demonstrates numerous case studies conducted in the treat-
ment of slaughterhouse waste by installing sequencing batch reactors.
6. Sequential anaerobic and aerobic treatment for slaughterhouse
wastewater
Organic and inorganic compounds can be greatly reduced by com-
bining both anaerobic and aerobic processes. Numerous sequential
case studies have been conducted in the treatment of both domestic
and industrial wastewaters (Castillo et al., 1999; Işik and Sponza,
2004; Işik and Sponza, 2006; Tezel et al., 2001; Von Sperling et al.,
2001). Fig. 4 shows some of the schematic diagrams of sequential anaer-
obic and aerobic processes. Anaerobic-aerobic treatment provides the
effluent that can be met with the international design standards. And
thus, can be easily discharged to lands or aquatic bodies. The benefits
of sequential treatment are complete degradation of organic matter,
substantial production of biogas, removal of both nitrogen and phos-
phorous, elimination of heavy metals, phenols, and pharmaceutical
compounds (Armenante et al., 1999; Joss et al., 2004; Ağdağ and
Sponza, 2005; Lemaire et al., 2008a; Shi et al., 2014). Several studies
have been conducted in the treatment of slaughterhouse wastewater
by combining both anaerobic and aerobic reactors (Table 10).
7. Microbial community responsible for slaughterhouse waste
treatment
Analysis of microbial community is essential during biological waste
treatment. However, in case of slaughterhouse waste limited studies are
available in literature. Studies conducted are mostly related to quantifi-
cation of anaerobic microorganisms. Nevertheless, following section il-
lustrates the role of anaerobic and aerobic species in degrading
complex compounds during waste generated from slaughterhouse
industry.
Cabezas et al. (2006) carried out a research on the effectiveness and
diversity of microbial species treating slaughterhouse wastewater
under low DO conditions in SBR. The objective was to supress NOB in
order to make the process more efficient. The DO in anoxic phase was
between 0.7 and 0.9 mg/l, while 2–3 mg/l in the aerobic phase. Under
oxygen limited supply NOB activity were supressed, but after increase
in DO Nitrobacter were again prevalent inside ISBR. AOB bacteria partic-
ularly Nitrosomonas were comparatively stable during the investigation.
Nitrosospira, and Nitrosococcus were also present but in lower fractions.
Thauera and Pseudomonas were the dominant denitrifiers during anoxic
conditions.

Table 9
Removal of COD, BOD, nitrogen and phosphate from SBR at different operating conditions.

Reactor Working HRT SRT Loading rates Temperature COD BOD Nitrogen Phosphate SS MLSS MLVSS F/M SVI References
volume (°C) (%) (%) (%) (%) (%) (g/l) (g/l) (ml/g)
(l)

ISBR 40 12 h – – – 98 99.6 98 (TN) 87 – – – – – Sroka et al., 2004

ISBR 7.9 2d – – 20 ± 2 96 – 97 84 80 – 4.09 – – Filali-Meknassi
(TKN) et al., 2005a
ISBR 7.9 2d 20 d – 20 ± 2 96 – 98 – 88 4.5–7 3.5–5 – 50–100 Filali-Meknassi
(TKN) et al., 2005b
ISBR 7.5 1.5 d 6.8 d 0.264 kg – 94 96 93 72 – 2.5 – 0.091 73 Sirianuntapiboon
BOD/m3-d (TKN) and Yommee, 2006
MSBR – – – – – 98 98 95 (AN) 98 93 – – – – Shengquan et al.,
2008
ISBR 7 42 h 15 d – 18–22 95 – 97 (TN) 98 – – – – – Lemaire et al., 2008a
ISBR 10 – 14.5 d 1.4 kg – 97 – 95 (TN) 97 – 3.85–4.95 – – 90–140 Li et al., 2008a
COD/m3-d
ISBR 10 (TV) 12 h 21–67 0.19 ± 0.03 29 ± 2 64 – 83 25 25 3.3–5.6 1.8–3.5 0.06 118 ± De Nardi et al., 2011
d kg N/m3-d (TKN) ± 35
0.03
ISBR 5 16 h – – 25 ± 1 54 – 84 (TIN) – – – 2.6 – – Mees et al., 2011
ISBR 2 2d N 100 0.15 kg 20 – – 90 (AN) – – 3 2.5 – 110 Li et al., 2011
d N/m3-d
ISBR 20 10 h 20–25 – – 86–95 – 70–98 – – – 1.8–3.2 – 75–85 Kundu et al., 2013
d (SCOD) (AN)
ISBR 4.5 23 h – – – 74–94 – – – – 7 – – – Louvet et al., 2013
ISBR 5 16 h – 0.15 kg 21.5 ± 0.85 – – 91.1 – – – 2.6 – – Mees et al., 2014
N/m3-d (TIN)
ISBR 8 10 d 20 d 0.61 kg 11 98 – 98 (TN) 96 – 4.2 – – – Pan et al., 2014a
COD/m3-d
ISBBR 8 24 h – 1.88–6.77 kg 25–30 98 – 96 (TN) 96 – – – – – Hai et al., 2015
COD/m3-d
IAASBR 12 (An), 48 h 40 d 0.5–4.5 kg 26–28 97% – 98 (AN) – 96 6000 – – 150 Rajab et al., 2017
6 (Ae) (An), (An), COD/m3-d (An),
24 h 15 d 4000
(Ae) (Ae) (Ae)

ISBR - Intermittent sequencing batch reactor; MSBR - Membrane sequencing batch reactor; ISBBR - Intermittent sequencing batch biofilm reactor; IAASBR - Integrated anaerobic/aerobic
sequencing batch reactor; TN -Total nitrogen; TKN - Total kjeldahl nitrogen; TIN - Total inorganic nitrogen; AN - Ammonia nitrogen; SCOD – Soluble COD; TV - Total volume; An - Anaer-
obic; Ae – Aerobic.
698 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708

Fig. 4. Schematic diagrams of sequential anaerobic and aerobic processes: (a) Willers et al., 1993 (b) Bernet et al., 2000; Mutua et al., 2016; Aziz, 2018 (c) Núñez and Martínez, 2001 (d) Del
Pozo and Diez, 2005 (e) Merzouki et al., 2005 (f) López-López et al., 2010 (g) Fongsatitkul et al., 2011 (h) Basitere et al., 2016 (i) Bustillo-Lecompte and Mehrvar, 2017b

Lemaire et al. (2008b) examined the microbial species in aerobic for almost 75%, both of which can perform denitrification.
granules for simultaneous removal of nitrogen and phosphate. Accumulibacter was dominant in the outer 200 μm, while
Accumulibacter (polyphosphate accumulating organism, PAO) and Competibacter was present in the central part of granule having size
Competibacter (glycogen accumulating organism, GAO) accounted N500 μm.
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708 699

Table 10
Execution of different sequential assemblies (anaerobic-aerobic) and their final conclusions in the treatment of high strength industrial wastewater (slaughterhouse).

S.·no Sequential assembly Wastewater composition Conclusion References

1 The sequential configuration consisted of Influent waste comprised of high COD (13 g/l), Nitrogen removal rates varied linearly with Willers et al., 1993
anoxic and aerobic reactors and a clarifier for BOD (7.2 g/l), NH4-N (2.2 g/l), TKN (2.5 g/l), and temperature. Maximum nitrogen removal rate
separating solids from liquid (Fig. 4(a)). TSS (14.4 g/l). (154 mg NH4-N/g VSS-d) was observed at 20 °C.
Moreover, anoxic/aerated volume ratio of 0.25 is
suggested at BOD/NH4-N ratio of 2.4 for
complete denitrification. Additionally, an
increase in recirculation factor from 15 to 30
didn't cause any significant effect on BOD
removal rates.
2 Two sequencing batch reactors were installed The piggery wastewater after preliminary Excellent TOC (81–91%) and TKN (85–91%) Bernet et al., 2000
one after the other. The first was anaerobic treatment consisted of TOC - 5.86 g/l, TKN - removal was observed from anaerobic-aerobic
and the second was aerobic SBR (Fig. 4(b)). 3.69 g/l, NH4-N - 2.94 g/l, TSS - 2.84 to 3.96 g/l. system. Elevated nitrogen removal was
acquired with increased recycling ratios.
Furthermore, biogas was mainly comprised of
N2 and CH4, which demonstrated that methane
production followed denitrification in
anaerobic SBR.
3 An upflow anaerobic sludge blanket reactor Slaughterhouse wastewater comprised of TCOD (85%) removal efficiency was independent Núñez and
coupled with activated sludge system was combination of blood, protein, fats, and manure. from recycling ratios. But TKN and TN removal Martínez, 2001
employed for treating slaughterhouse efficiencies increased to 85% and 70%
wastewater (Fig. 4(c)). respectively at recycling ratio of 2. However, at
that particular ratio carbon removal efficiency in
UASB decreased.
4 A pilot scale anaerobic-aerobic fixed film The average COD, BOD, TKN, TSS, and O&G were At an average loading rate of 0.77 kg COD/m3-d Del Pozo and Diez,
reactor was established for poultry 1820 mg/l, 900 mg/l, 190 mg/l, 430 mg/l, and and 0.084 kg N/m3-d the TCOD and nitrogen 2005
slaughterhouse wastewater (Fig. 4(d)). 170 mg/l respectively. removal efficiencies were 93% and 67%
respectively. Additionally, the biogas generated
consisted of about 58% N2, 37% CH4, and 5% CO2.
5 To reduce nutrients and carbonaceous The wastewater treated was having average The wastewater was prefermented for 14 d in Merzouki et al.,
compounds a combination of TCOD of 7.78 g/l, NH4-N of 88 mg/l, TKN of order to increase phosphate and VFAs 2005
anaerobic-anoxic SBR and aerobic fixed bed 410 mg/l, PO4-P of 18 mg/l. concentrations. The average removal
reactor was used for slaughterhouse effluent efficiencies soared from 83% to 94%, 48.5% to
(Fig. 4(e)). 77%, and 47% to 97% for COD, NH4-N, and PO4-P
respectively.
6 Anaerobic filter and aerobic sequencing batch Slaughterhouse wastewater showed COD Anaerobic filter performed exceptionally at 24 López-López et al.,
reactor were installed for treating high 11000 mg/l, BOD 8360 mg/l, TSS 8150 mg/l, h HRT and 11 kg/m3-d of OLR. In case of SBR 2010
strength industrial wastewater (Fig. 4(f)). ammonia nitrogen 137 mg/l, PO−3 4 -P 83 mg/l, the reactor was proficient at 9 h aeration
and O&G 784 mg/l. period. The combined arrangement removed
about 97% COD, 99% BOD, 99% TSS, 93%
ammonia nitrogen, 80% PO−3 4 -P, and 83% O&G
from the wastewater.
7 A series of anaerobic, anoxic, and aerobic The influent wastewater comprised of high Effect of internal recycle on the removal Fongsatitkul et al.,
reactors were employed for the treatment of organic and inorganic content. The average COD, efficiencies of COD, TKN, and TP was 2011
slaughterhouse wastewater (swine) (Fig. 4 TKN, TP, and TSS were 1551 mg/l, 189 mg/l, 28.6 analysed by changing the discharge from 15
(g)). mg/l, and 521 mg/l respectively. to 40 l/d. At 30 l/d both TKN and TP
achieved excellent removal rate of 97.6% and
89.5% respectively. Furthermore, COD
removal was mostly above 95% at different
flow rates.
8 Anaerobic expanded granular sludge bed Here again the wastewater constitute excessive At different organic loading rates (0.5, 0.7, and 1 Basitere et al.,
(EGSB) reactor attached with sequential amount of TCOD (2133–4137 mg/l), BOD kg COD/m3-d) and hydraulic retention times (7, 2016
anoxic and aerobic reactors was operated for (1100–2750 mg/l), FOG (131–684 mg/l), TKN 4 and 3 d), the removal efficiency of entire
a period of 26 d in order to treat poultry (77–352 mg/l), TP (8–27 mg/l), and TSS system and EGSB reactor was 65% and 51%
slaughterhouse wastewater (Fig. 4(h)). (315–1273 mg/l). respectively. Low COD removal was observed
due to sludge washout from EGSB because of the
presence of elevated suspended solids and fats.
Hence, installation of dissolved air floatation
before EGSB reactor was recommended by
authors.
9 The meat processing wastewater was treated Considerable high concentrations of TCOD The reactors were functioned at an SRT of 5 d, Mutua and
effectively by establishing lab scale anaerobic (15,812 mg/l), BOD (13,659 mg/l), TKN while the HRT was fixed at 2 d and 1 d for Mwaniki Njagi,
and aerobic sequencing batch reactors in (1022 mg/l), and TP (61 mg/l) was obtained anaerobic and aerobic SBR respectively. At an 2016
series (Fig. 4(b)). from meat processing plant. OLR of 12.8 kg COD/m3-d the reactor removed
99% COD and BOD, 96% TKN, and 61% TP
efficiently from the wastewater.
10 Anaerobic baffled reactor coupled with Maximum COD, TOC, TP, TN, and TSS observed At optimal operating conditions maximum TOC Bustillo-Lecompte
activated sludge reactor was implemented at during the research period were 2080 mg/l, (85%) and TN (72%) removal was obtained from and Mehrvar,
lab scale in the treatment of Ontario meat 1694 mg/l, 23 mg/l, 255 mg/l, and 103.5 mg/l the system. About 0.12 m3/d methane or 0.48 2017b
processing wastewater (Fig. 4(i)). correspondingly. kWh daily energy productions was observed
from anaerobic baffled reactor. In addition to
that the projected model can be used in nearby
future in case of anaerobic and aerobic
treatment because of the fact that it provided
eminent results.

(continued on next page)

700 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
Table 10 (continued)
S.·no Sequential assembly Wastewater composition
11 Slaughterhouse wastewater was sequentially The slaughterhouse wastewater comprised of
treated by anaerobic and aerobic sequencing high COD (3800–4700 mg/l), BOD
batch reactors (Fig. 4(b)). (2300–3100 mg/l), TN (210–274 mg/l), PO−3
(140–229 mg/l), TSS (794–1116 mg/l), and
O&G (426–521 mg/l).
Lemaire et al. (2009) established a lab scale SBR in the removal of
phosphorous, nitrogen, and TCOD from slaughterhouse wastewater. Ini-
tially SBR was fed with non-enhanced biological phosphorous removal
sludge, but later on enhanced biological phosphorous removal sludge
was added to SBR. Fluorescence in situ hybridisation confirmed the
presence of Accumulibacter species (70%). After achieving the steady
state the removal efficiencies were 95%, 98%, and 97% for TCOD, total
phosphorous, and total nitrogen respectively.
Rajakumar et al. (2011) employed an upflow anaerobic filter to treat
Indian poultry slaughterhouse wastewater. Maximum removal in TCOD
(78%) was observed at 12 h HRT and 10.05 kg/m3-d of organic loading
rate. Additionally, average methane content was between 46 and 56%
during the investigation. SEM analysis showed granules clumps
comprised of Methanosarcina (dominant) and Methanosaeta cells.
Methanosarcina has higher substrate affinity for acetate than
Methanosaeta at higher acetate concentrations. The acetate concentra-
tion was 980 mg/l, and therefore Methanosarcina presence was abun-
dant inside anaerobic filter. Also Methanosarcina beside acetate can
consume formate, hydrogen, and carbon dioxide as well, and thus was
dominant than Methanosaeta.
Palatsi et al. (2011) assessed the influence of increased loading rates
by mixing different slaughterhouse waste (cattle/pig) on the activity of
microbial species. Syntrophomonas, Coprothermobacter, Anaerobaculum,
and Methanosarcina were responsible for stable reactor performance
in spite of high lipid content. The authors suggested that microbial com-
munity and lipid concentration are the two important reasons for suc-
cessful anaerobic treatment of slaughterhouse waste.
In order to assess the bacterial community present in anaerobic la-
goon (2000 m3), a study was performed by Cardinali-Rezende et al.
(2012). The COD and BOD removal efficiencies were 55% and 58% re-
spectively. Bacteroidetes, Chloroflexi, and Proteobacteria were the domi-
nant bacteria, while archaeal group present in sludge was
Euryarchaeota and Crenarchaeota. Crenarchaeota was responsible for
ammonia oxidation, and Euryarchaeota (Methanomicrobiales and
Methanobacteriales) for producing methane.
Rajakumar et al. (2012) performed anaerobic experiments at
mesophilic conditions (29–35 °C) to evaluate the microbial species in-
volved in the degradation of poultry slaughterhouse wastewater.
Change in species were observed during the course of 225 days. During
startup period Methanobacterium and Methanosaeta were dominant,
while Methanosarcina was prevalent at the end of study.
A study on temperature effect (mesophilic and thermophilic tem-
perature) on COD removal in upflow anaerobic filter was conducted
by Gannoun et al. (2013). 90% (mesophilic) and 72% (thermophilic)
COD reduction was observed at OLRs of 4.5 g COD/l-d and 9 g COD/l-d
respectively. Microbial analysis showed dominant fermentative bacte-
ria, and Clostridiales group contained maximum number of strains.
Three novel strains identified were Macellibacteroides fermentans,
Desulfotomaculum peckii and Defluviitalea saccharophila.
Stets et al. (2014) conducted a study to evaluate the performance of
AF by using three different types of support media (Polypropylene
rings, polyurethane foam, and clay brick) in three different reactors.
All three reactors showed similar microbial composition, but clay
brick reactor showed highest bacterial and archaeal compositions.
Conclusion References
The combined sequential assembly removed Aziz, 2018
about 92% COD, 97% BOD, 90% TSS, 74% PO−3 4 ,
4 and 90% O&G from the wastewater. Moreover,
production of biogas rich in methane was also
observed from ASBR. The average biogas and
methane production at steady state conditions
were 3.95 l/day and 64% respectively.
Proteobacteria and Bacteroidetes were the dominant bacteria, while
Methanomicrobiales and Methanosarcinales were the common archaea
present.
Moestedt et al. (2016) demonstrated the significance of trace
elements (Fe, Co, and Ni) during anaerobic co digestion of slaughterhouse
and municipal solid waste. Real time PCR was performed to
quantify methanogens including Methanobacteriales, Methanococcales,
Methanomicrobiales, Methanosaetaceae, and Methanosarcinaceae. Fe, Co,
and Ni were added to experimental and control anaerobic reactors during
different phases. However, day 0 was set when Co supplementation was
stopped in control reactor. During days 32 and 81, Methanomicrobiales
were dominant (23–41%) in both reactors, while after 90 days
Methanosarcinaceae abundance increased considerably in experimental
reactor when fed with Ni. Moreover, reduction in Methanomicrobiales
and Methanosaetaceae communities was observed as a result of Ni and
Co addition in experimental reactor.
Pagés-Díaz et al. (2015) evaluated methanogenic community during
the operation of four continuously stirred anaerobic digesters treating
different waste mixtures. The reactors were operated at 55 °C with
slaughterhouse waste (SW), slaughterhouse waste manure (SW M),
slaughterhouse waste various crops (SW VC), and slaughterhouse
waste various crops municipal solid waste (SW VC MSW).
Methanomicrobiales, Methanobacteriales, Methanosarcinaceae, and
Methanosaetaceae were targeted initially and at the end of study. M ±
ethanosaetaceae was absent in inoculum as well as in digested sludge.
Methanosarcinaceae presence increased in all four reactors with domi-
nance in SW M reactor. Methanosarcinaceae group are responsible for
directly converting acetate into methane by acetoclastic pathway.
Methanomicrobiales on the other hand was supressed in all reactors be-
cause of elevated pH (N7). Thus, Methanobacteriales were utilizing hy-
drogen to produce methane instead of Methanomicrobiales. Maximum
methane production was 5.3 l/d in SW M reactor, while minimum
was 1.1 l/d in SW reactor.
The bacterial community treating abattoir wastewater was analysed
by Jabari et al. (2016). The anaerobic digester (upflow anaerobic filter)
operated at both mesophilic and thermophilic conditions. Results re-
vealed 27 different phyla comprising mainly of Firmicutes (21.7%),
Proteobacteria (18.5%), Bacteroidetes (11.5%), Thermotogae (9.4%),
Euryarchaeota (8.9%), and mslb6 (8.8%). Clostridium, Bacteroides,
Desulfobulbus, Desulfomicrobium, Desulfovibrio and Desulfotomaculum
were the dominant bacteria in the anaerobic sludge.
Hernández et al. (2016) observed the role of microalgae for the pro-
duction of biofuel in two 75 l high rate algal ponds. One pond was oper-
ated indoors under controlled temperature (25 ± 2 °C) and light supply,
while the other was placed in greenhouse conditions with 20 ± 6 °C and
higher light supply. Initial mix microalgae comprised of Chlamydomonas
subcaudata, Anabaena and Nitzschia species. High COD removal effi-
ciency (92%) was achieved in algal pond kept indoors, whereas high sol-
uble phosphorous (71%) removal was acquired at greenhouse
conditions.
The role of mixed algal species on nutrients removal from slaughter-
house wastewater was examined by Taşkan (2016). After acclimatiza-
tion the photo-bioreactor removed about 90% TOC, 96% total
phosphorous, and 70% total nitrogen. Cyanobacterial species were
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708 701

(a)

Thermotogae

Spirochaetes

WWE1

OP11

Verrucomicrobia

Actinobacteria

WS6

Planctomycetes

Synergistetes

Bacteroidetes

Chloroflexi

Firmicutes

Proteobacteria

Euryarchaeota
0 5 10 15 20 25 30 35

(b)

Fig. 5. (a) Krona chart represents overall anaerobic microbial community of sludge obtained by 16S rRNA sequencing, (b) represents bacterial and archaeal community at the phylum level,
(c) represents bacterial and archaeal community at the class level. (Aziz, 2018).
702 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708

Thermoplasmata
Mollicutes
Thermoleophilia
Unclassified
Coriobacteriia
Bacilli
TM7-3
Verruco-5
Unclassified
Thermotogae
Alphaproteobacteria
[Pedosphaerae]
Spirochaetes
Betaproteobacteria
Actinobacteria
[Cloacamonae]
WCHB1-64
Gammaproteobacteria
Methanobacteria
SC72
Epsilonproteobacteria
Planctomycetia
Synergistia
Bacteroidia
Deltaproteobacteria
Anaerolineae
Clostridia
Methanomicrobia
0 5 10 15 20 25 30

(c)
Fig. 5 (continued).

more efficient than eukaryotic in the removal of nutrients from slaugh-
terhouse wastewater.
A study on the bacterial composition of a full scale UASB reactor
treating slaughterhouse wastewater by two different sequencing ap-
proach (16SrRNA and whole genome shotgun metagenomic) was con-
ducted by Delforno et al. (2017). Different type of sequences were
quantified by the two approaches. At genus level, Clostridium and
Methanosaeta were detected by 16S rRNA and Pseudomonas and
Psychrobacter by whole genome shotgun metagenomics. Methanosaeta
was more abundant than other hydrogenotrophic and methylotrophic
methanogens. Moreover, antibiotic resistant genes (ARGs) were also clas-
sified, and total of 43 different ARGs were present. Multidrug, bacitracin,
tetracycline, lincomycin, and polymyxin genes were abundant (N95%) in
total sludge sample.
Granada et al. (2018) performed a detailed study on biogas produc-
tion and microbial composition during anaerobic digestion of slaughter-
house and dairy industrial waste. At the end of the study about 38 l
biogas comprising of 26 l methane and 12 l other gases was produced.
Samples were collected on day 1, day 7, day 25, and day 42 for microbial
analysis. Phylum Firmicutes and classes Clostridia and Bacilli were abun-
dant in all four sampling days. Clostridia species are responsible for
producing important VFAs such as acetate, butyrate, formate, and
lactate, whereas Bacilli efficiently improves the organic matter
degradation. Apart from that, both of them also act as important denitri-
fiers. In addition to that, particular bacterial and archaeal
species which were actively responsible for methane production were
Porphyromonadaceae, Tissierellaceae, Methanobacteriaceae, Methanosarcina,
Caldicoprobacteraceae, Syntrophomonadaceae, Bacteroidaceae,
Turicibacteraceae, and Dethiosulfovibrionaceae. Porphyromonadaceae and
Tissierellaceae are responsible for degrading complex compounds such as
proteins, carbohydrates, and peptides, and in the production of VFAs.
Methanobacteriaceae utilize CO2/H2 as substrate for methane production,
and Methanosarcina beside active methanogen is also resistant to variation
in temperature, loading rates, and ammonium toxicity.
Yan et al. (2018) studied the effect of change in initial sludge pH (6.5
to 8) during anaerobic digestion of slaughterhouse wastewater sludge.
The authors exhibited that increase in pH resulted in increased biogas
(10%) and methane (64%) production, while decreased hydrogen sul-
phide content (45%). Microbial analysis revealed Euryarchaeota,
Proteobacteria, Bacteroidetes, Proteobacteria, and Firmicutes as dominant
phylum. Methanogens belongs to Euryarchaeota, while sulphate reduc-
ing bacteria belongs to Proteobacteria family. Firmicutes are responsible
for degrading VFAs into hydrogen, and Bacteroidetes converts amino
acids into acetate. Methanogens, sulphate reducing bacteria, and
Firmicutes were higher at pH 6.5 than at pH 8. Bacteroidetes showed con-
trary result, and was 5% higher at pH 8 than at pH 6.5. Methanogens
quantified at genus level were Methanosaeta, Methanobacterium,
Methanosarcina, Methanobreribacter, Methanospirllum, and
Methanolinea. Methanospirllum and Methanosaeta percentage were not
affected by initial pH change, whereas Methanobacterium percentage
was higher at 6.5 than at pH 8. Methanosaeta utilize acetate,
while Methanospirllum and Methanobacterium consume hydrogen to
produce methane. On the other hand, Methanosarcina abundance in-
creased by 25% when pH was increased from 6.5 to 8. Moreover,
Methanosarcina can utilize both acetate and hydrogen to produce meth-
ane. Thus, Methanosarcina presence elevated the methane production at
pH 8.
Aziz (2018) evaluated the performance of anaerobic SBR in the treat-
ment of slaughterhouse wastewater. TCOD, SCOD, BOD, and TSS removal
efficiency acquired from anaerobic digester were 68%, 69%, 71%, and 63%
respectively. The average biogas production and methane percentage was
3.95 l/day and 64% respectively. 16S rRNA sequencing analysis showed
Proteobacteria, Firmicutes, Chloroflexi, Bacteroidetes, Planctomycetes, and
Euryarchaeota abundance at phylum level (Fig. 5(a)). Bacteroidetes and
Firmicutes phylum are responsible for degrading complex compounds
i.e., proteins, lipids, and polysaccharides into acetate, CO2, formate,
LCFAs, and hydrogen (Jabari et al., 2016; Stets et al., 2014). Proteobacteria
classified at class level were alphaproteobacteria, betaproteobacteria,
 A. Aziz et al. / Science of the Total Environment 686 (2019) 681–708
gammaproteobacteria, deltaproteobacteria, and epsilonproteobacteria
(Fig. 5(c)). Gammaproteobacteria group comprises of denitrifiers and
phosphate accumulating organisms. Deltaproteobacteria contains
bacteria which are mainly responsible for sulphate reduction, and
betaproteobacteria community are responsible for nitrification and some-
times in denitrification as well (Jabari et al., 2016). Chloroflexi phylum are
involve in the production of acetic acid, and degradation of both monosac-
charides and polysaccharides (Zheng et al., 2015). They are also effective
in degrading difficult organic compounds during anaerobic digestion.
Planctomycetes utilize glucose, maltose, and ribose (monosaccharides) to
convert them into acetic acid and hydrogen (Zheng et al., 2015).
Methanomicrobia (27%) and Methanobacteria (2%), were the two main
methanogenic groups observed at class level under Euryarchaeota phy-
lum (Fig. 5). The dominant Methanomicrobia class usually comprises of
two important orders i.e., Methanosarcinales and Methanomicrobiales.
Methanosarcinales are sheathed rods, cocci, and pseudosarcina in shape,
and utilize acetate, methanol, methylamine, H2 and CO2 to convert
them into methane. On the other hand, Methanomicrobiales (sheathed
rods, spirals, rods, and cocci) consumes H2, CO2, and formate to produce
methane. The other methanogenic group classified was Methanobacteria,
which comprises of Methanobacteriales at order level. They are in cocci
and rod shapes, and produce methane by utilizing H2, CO2, formate, CO,
methanol, and secondary alcohols (Liu, 2010).
8. Conclusion
The type of treatment generally depends upon wastewater charac-
teristics, effluent guidelines, and the best available technology. Reactors
such as UASB, AF, RBC, ASP, MBBR, and SBR have successfully executed
in the treatment of slaughterhouse effluent. Thus, in order to reduce
both organic and inorganic content either single intermittent SBR or
combined sequential assemblies (anaerobic and aerobic) must to be
implemented.
Execution of single ISBR proves to be beneficial than combined reac-
tors as it has resulted in reduced aeration rates with concurrent elimina-
tion of external carbon source. But certain conditions like anaerobic and
aerobic reaction time, loading rates, mixing rate, DO, HRT, SRT, MLSS, F/
M, and SOUR ought to be controlled and monitored periodically. More-
over, aerobic granulation can also reduce carbon, nitrogen and phos-
phorous in ISBR. Although ISBR is a promising technology, it still needs
to provide its competence by further conducting meticulous research
at both pilot and real scale. Future research must be conducted on meth-
ane production and the role of aerobic and anaerobic microorganism
particularly methanogens in ISBR during SWW treatment.
Acknowledgement
The corresponding author wish to thank the sponsors of this project
“Bio-energy production from high strength industrial wastewater
(slaughterhouse wastewater) with anaerobic SBR combining with aero-
bic SBR for safe discharge of treated water” for their financial support,
namely Early Career Research Award, SERB, Department of Science
and Technology (DST), New Delhi, India. Sanction Order No: ECR/
2016/00162 Dated: 23 June 2017.
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