ARTICLE IN PRESS

WA T E R R E S E A R C H 42 (2008) 1 12

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Review

Chemical and biological technologies for hydrogen sulfide

emission control in sewer systems: A review

Lehua Zhang, Peter De Schryver, Bart De Gusseme, Willem De Muynck, Nico Boon,
Willy Verstraete
Laboratory of Microbial Ecology and Technology (LabMET), Ghent University, Coupure Links 653, B-9000 Ghent, Belgium

art i cle info ab st rac t

Article history: Biogenic corrosion of sewers represents a cost of about 10% of total sewage treatment cost
Received 19 March 2007 in Flanders (Belgium) and is further increasing. In the past, research has resulted in a
Received in revised form number of prevention methods, such as injection of air, oxygen, H2O2, NaClO, FeCl3 and
10 July 2007 FeSO4. The possibility of biological oxidation of sulfide using nitrate as the electron
Accepted 12 July 2007 acceptor has also been explored in sewer systems. However, all of these methods have a
Available online 19 July 2007 problem with the high cost (h1.97.2 kg1 S removal). In this review, new approaches for
hydrogen sulfide emission control in sewer systems are discussed. The control of hydrogen
Keywords:
sulfide emission by using a microbial fuel cell (MFC) can be cost-effective while the BOD is
Concrete corrosion
removed partially. The use of phages that target sulfate-reducing bacteria (SRB) can
Thiobacillus
possibly inhibit sulfide formation. Novel inhibitors, such as slow release solid-phase
Sulfate attack
oxygen (MgO2/CaO2) and formaldehyde, warrant further study to control hydrogen sulfide
Sewage
emission in sewer systems.
Iron salts
& 2007 Elsevier Ltd. All rights reserved.
Nitrate
Microbial fuel cells

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2. Biogenic corrosion of sewer systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.1. Sulfur cycle in sewers and the environmental parameters . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2
2.2. Sewer corrosion by hydrogen sulfide emission . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3. Increasing redox potential to control sulfide formation . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.1. Air or oxygen injection. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 4
3.2. Addition of nitrate . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
4. Inhibition of SRB activity . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5. Chemical removal of sulfide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5.1. Precipitation by metal salts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5.1.1. Insoluble metal sulfides in sewage . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5
5.1.2. Addition of iron salts . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 5

Corresponding author. Tel.: +32 9 264 59 76; fax: +32 9 264 62 48.
E-mail address: Willy.Verstraete@UGent.be (W. Verstraete).
0043-1354/$ - see front matter & 2007 Elsevier Ltd. All rights reserved.
doi:10.1016/j.watres.2007.07.013
 ARTICLE IN PRESS
2 WAT E R R E S E A R C H 42 (2008) 1 12

5.1.3. Operation conditions and costs . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6

5.2. Addition of oxidizing chemicals. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.2.1. Hydrogen peroxide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.2.2. Chlorine . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 6
5.2.3. Potassium permanganate. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
6. Biological oxidation of sulfide . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 7
7. Outlooks . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
7.1. Formaldehyde or para formaldehyde . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
7.2. Slow release solid-phase oxygen (MgO2/CaO2). . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
7.3. Microbial fuel cells (MFCs) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 8
7.4. Phages. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
8. Summary and conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 9
Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 10

1. Introduction sulfide (Cadena and Peters, 1988; US EPA, 1991). Addition of

Hydrogen sulfide emission in sewer systems is associated
with several problems, including biogenic corrosion of con-
crete, release of obnoxious odors to the urban atmosphere
and toxicity of sulfide gas to sewer workers (ASCE, 1989;
Nielsen and Keiding, 1998; Nielsen et al., 1998; US Environ-
ment Protection Agency (US EPA), 1974). Minor problems of
concrete corrosion have been reported when the concentra-
tion of total sulfide in the wastewater is within the range of
0.10.5 mg S L1. Severe concrete corrosion may occur at
sulfide concentrations from 2.0 mg S L1 on (Hvitved-Jacobsen
et al., 2002). In Los Angeles County, approximately 10% of the
sewer pipes are subject to significant sulfide corrosion, and
the costs for the rehabilitation of these pipelines are roughly
estimated at h400 million (Sydney et al., 1996). The restoration
of the overall damaged sewer systems in Germany is
estimated to cost about h100 billion per year (Kaempfer and
Berndt, 1998). In Flanders (Belgium), biogenic sulfuric acid
corrosion of sewers is approximated at h5 million per year,
representing about 10% of total cost for wastewater collection
and treatment (Vincke, 2002).
To solve the biogenic corrosion problem, several methods
have been investigated, i.e. (1) optimizing the sewer hydraulic
design to minimize sulfide generation, (2) sulfate source
control technologies such as urine separation or pretreat-
ment, (3) improving the resistance of sewer pipes to biogenic
corrosion and (4) decreasing hydrogen sulfide emission from
sewage (De Belie et al., 2004; Monteny et al., 2000, 2001;
Nielsen et al., 2006a; Scrivener et al., 1999; Yamanaka et al.,
2002; US EPA, 1991). This review focuses on chemical and
biological technologies that prevent or decrease hydrogen
sulfide emission in sewer systems (Fig. 1).
One category involves increasing redox potential, thus
decreasing sulfide production. Increasing redox conditions
involves addition of thermodynamically favorable electron
acceptor compounds such as oxygen, nitrate or nitrite (Bentzen
et al., 1995; Hobson and Yang, 2000; Londry and Suflita, 1999).
iron salts or precipitation of ferrous sulfide removes dissolved
sulfide from the sewage (Nielsen et al., 2005c; Padival et al.,
1995; Tomar and Abdullah, 1994). Addition of H2O2 or
chlorines chemically oxidizes sulfide, thereby decreasing the
amount of dissolved sulfide (Tomar and Abdullah, 1994;
Waltrip and Snyder, 1985). Addition of nitrate and nitrite
may also favor biological oxidation of sulfide by means of
nitrate-reducing, sulfide-oxidizing bacteria (NR-SOB) (Garcia
De Lomas et al., 2005; McInerney et al., 1996; Nemati et al.,
2001a, b; Shelley et al., 2005).
In recent years, significant increase in the knowledge on
biological and chemical technologies for hydrogen sulfide
emission control in existing sewer systems has been made.
This paper summarizes the current state and explores future
research possibilities.
2. Biogenic corrosion of sewer systems
2.1. Sulfur cycle in sewers and the environmental
parameters
Several processes are associated with the sulfur cycle in
sewer networks (Sand, 1997; Lens and Kuenen, 2001). The
conceptual models for simulation of the sulfur cycle process
and prediction of sulfide buildup in sewers have been
developed recently (Lahav et al., 2004, 2006; Hvitved-Jacobsen
et al., 1998; Matos and Aires, 1995; Nielsen et al., 2005ac;
Yongsiri et al., 2003, 2004b). Fig. 2 outlines the major processes
and environmental parameters associated with the sulfide
cycle in sewer systems, including the bulk wastewater,
biofilms, sediments, atmosphere and surface exposed to the
atmosphere. These processes are (1) formation of sulfide, (2)
volatilization of hydrogen sulfide, (3) chemical and biological
oxidation of sulfide and (4) precipitation of metal sulfides.
For domestic wastewater, the main source of sulfur is
sulfate (SO24 ) in a concentration range of 40200 mg L
1

Alternatively, SRB activity can also be inhibited by pH elevation
or inhibitors such as biocides and molybdate (Jayaraman et al.,
1999; Nemati et al., 2001c; Reinsel et al., 1996).
Another category is chemical and biological removal of
sulfide (e.g. addition of iron salts, H2O2, chlorines or nitrate)
that may be considered as ultimate treatments to remove
(Araujo et al., 2000; Kalogo and Verstraete, 1999; Paing et al.,
2000). Sulfate can be reduced to sulfide by sulfate-reducing
bacteria (SRB) (Fig. 2). This biological process mainly occurs in
biofilms and sediments under anaerobic conditions in the
submerged part of sewers (Beardslay et al., 1956; Carpenter,
1932; Parande et al., 2006). It is readily observed in areas with
 ARTICLE IN PRESS
WA T E R R E S E A R C H 42 (2008) 1 12 3

H2S control methods in sewer systems

Inhibition of Elimination of
H2S generation H2S formed

General Specific Biological Chemical Chemical

inhibition of prevention of oxidation oxidation of precipitation
biological SRB activity of H2S H2S formed of H2S
activity formed formed

pH Addition Addition of Addition of Addition

elevation, of alternative chemical oxidants of iron
addition of biocides electron (O2, H2O2, Cl2, salts
NaOH acceptors (O2, NaClO, KMnO4, (Fe2+,
or Ca(OH)2 NO3-, NO2-) CaO2, MgO2) Fe3+ )

Fig. 1 Chemical and biological technologies for H2S emission control in sewer systems (modified from Garcia De Lomas et
al., 2005). SRB: sulfate-reducing bacteria.

Environmental Environmental
parameters Major sulfide processes parameters

SOB, pH, Corrosion of Odor nuisance and

Material sewer health related
of sewers problem

H2S(g) in the urban

Sulfuric acid atmosphere

H2S(g) in the air

phase of sewers
pH,
Turbulence Air-water interface Air-water interface
Temperature
Emission
Metal sulfides Sulfur and its
(e.g.FeS) oxidized forms

Precipitation
Chemical and
pH, Sulfide species biological
Conductivity, in bulk oxidation
ORP wastewater

SRB, ORP,
Sulfide formation by DO, pH,
sulfate reducing bacteria Temperature

Sulfur resources,
mainly sulfate

Fig. 2 Major sulfide processes and their effect factors associated with the sulfur cycle in the sewer system (modified from
Yongsiri et al., 2003). SOB: sulfide-oxidizing bacteria; SRB: sulfate-reducing bacteria; ORP: oxidation reduction potential;
DO: dissolved oxygen.
 ARTICLE IN PRESS
4 WAT E R R E S E A R C H
slow flow rates and insufficient reaeration potential at
relatively high temperature (Hvitved-Jacobsen et al., 2000;
Nielsen et al., 1992).
Hydrogen sulfide in sewage is primarily present as two
sulfide species, depending on the pH (Yongsiri et al., 2003).
Because the pH in sewage is about 7.0, these two species are
H2S(aq) and HS (Eq. (1)) (Yang et al., 2005). The S2 species is
not taken into account because of its insignificant presence
even at very high pH (Eq. (2)) (Fu and Shen, 1990).
H2 Saq 2H HS ; pKa1 E7:04; (1)
HS 2H S2 ; pKa2 E11:96;
H2 Saq 2H2 Sg ; kc E4681 atm mole fraction1 : (3)
Only H2S(aq) can be transferred across the airwater interface,
giving rise to the emission of hydrogen sulfide from wastewater
to the sewer atmosphere (Eq. (3)) (Fu and Shen, 1990) (Fig. 2).
Hydrogen sulfide emission is a physico-chemical process
involving both the water and air phases of sewer networks
(Elmaleh et al., 1998). It is dependent of temperature, pH,
hydraulic conditions of the water phase and ventilation of the
air phase (Yongsiri et al., 2004a, b, 2005). Field investigations in
the USA by Pomeroy and Bowlus (1946), in Australia by
Thistlethwayte and Goleb (1972) and in Portugal by Matos and
Aires (1995) showed clear evidence of hydrogen sulfide being
present in concentrations of up to about 300 mg m3 in the
atmosphere of gravity sewers and sewer structures.
The main transformation and fate of hydrogen sulfide are
precipitation of metal sulfides and chemical/biological oxida-
tion (Fig. 2). The presence of metals such as iron, zinc, lead and
copper in the wastewater leads to precipitation of metal sulfides
and thereby decreases sulfide emission. Oxidation of sulfides in
sewer networks can occur both chemically and biologically,
making the total oxidation processes complex (Gadekar et al.,
2006). Biological oxidation of hydrogen sulfide can take place at
the sewer surfaces exposed to the sewer atmosphere. The
aerobic and autotrophic Thiobacillus sp. growing on the moist
surface can oxidize hydrogen sulfide to sulfuric acid (Devereux
et al., 1989; Gadekar et al., 2006; Islander et al., 1991). The
sulfuric acid generated will subsequently attack the sewers and
their structures by reacting with corrodible compounds, such as
cement and metals.
2.2. Sewer corrosion by hydrogen sulfide emission
H2 S 2O2 ! H2 SO4 :
Hydrogen sulfide in the sewer gas phase diffuses into the thin
liquid film present at sewer surfaces. At the surface, chemoau-
totrophic bacteria will oxidize the sulfide to sulfuric acid (Eq. (4)).
The corrosion process occurs by the reaction of the biogenic
sulfuric acid with the cementitious material of the concrete and
results in the eventual structural failure of sewers (Wiener et al.,
2006). This is characterized by the production of a corroding
layer on the surface of the concrete. This layer consists of
gypsum (CaSO4 of various hydration states) and moisture (Mori
et al., 1992). The thickness of this layer expands into the
1 be resistant to SOB.
This is Henrys constant at 20 1C.
42 (2008) 1 12
concrete, as more and more acid is produced to react with the
concrete. The formation of ettringite (3CaO  Al2O3  CaSO4  12H2O
or 3CaO  Al2O3  3CaSO4  31H2O) during the acid reaction process
causes another facet of the problem (Redner et al., 1991, 1994).
Ettringite is expansive and causes internal cracking and pitting,
which provides a larger surface area for the chemical reaction to
occur. This will also provide further sites of penetration of the
acid into the concrete. The conversion of concrete to gypsum
and ettringite weakens the structural integrity of the concrete
pipe (Yamanaka et al., 2002). This decreases the load-bearing
capacity of the concrete and can result in the eventual collapse
of the sewer.
(2)
Table 1 presents a summary of the literature concerning the
sewer corrosion rates and the lifetimes. The US EPA investi-
gated 131 cities and 66 of them were reported to have
corrosion problems. The US EPA (1991) reported that the
concrete corrosion rate in sewer pipes is 2.510 mm year1
based on the investigation of 34 cities. Other references
pointed out that the average concrete corrosion rate is about
3 mm year1 and that the lifetime of sewer pipes is only about
50 years (Davis et al., 1998; Ismail et al., 1993; Morton et al.,
1991; Mori et al., 1992). In Belgium, severely corroded sewer
pipes were examined in the district of Bruges; corrosion rates
of 1.11.8 mm year1 were observed (Vincke et al., 2002).
Monteny et al. (2001) reported that a concrete corrosion rate
of 1.01.3 mm year1 was found for Portland fly ash concrete
that was believed to be resistant to sulfide-oxidizing bacteria
(SOB). The lifetime of Portland fly ash concrete sewer pipes
was estimated to be 90160 years.
3. Increasing redox potential to control sulfide
formation
3.1. Air or oxygen injection
Sulfide can be produced in a slime layer depth of 1 mm and
more in sewers containing aerobic wastewater, because the
layer containing oxygen is only 0.4 mm deep (Yu et al., 1998).
If dissolved oxygen (DO) is present around the slime layer,
chemical and biological oxidation of the sulfide will take place
Table 1 Corrosion rate and lifetime of sewer pipes
Corrosion rate Lifetimea References
(4) (mm year1) (year)
2.510 2070 US EPA (1991)
2.7 65 Morton et al. (1991)
4.34.7 3545 Mori et al. (1992)
24 4590 Ismail et al. (1993)
3.1 55 Davis et al. (1998)
1.01.3b 130170 Monteny et al. (2001)
1.11.8 90160 Vincke et al. (2002)
a
The lifetime is the ratio of concrete sewer pipes thickness to
corrosion rate. The thickness of concrete sewer pipes is 68 inches
(1 inch 25.4 mm) (University of Virginia, 2006).
b
The material of sewer pipes is Portland fly ash that is believed to
 ARTICLE IN PRESS
WA T E R R E S E A R C H
as it passes into an aerobic environment (Nielsen et al., 2003,
2005b, 2006a, b). If DO is not present, dissolved sulfide will
enter the bulk wastewater where it can be present as
dissolved hydrogen sulfide gas (H2S). DO levels above
0.5 mg L1 can generally prevent sulfide occurrence (US EPA,
1991). A DO level of 0.21.0 mg L1 at the terminal point of
sewers has been reported when air injection was used to
control sulfide emission (Ochi et al., 1998; Tanaka and
Takenaka, 1995). Air injection is most commonly applied to
force mains and wet wells (Tanaka et al., 2000). Advantages of
air injection include a decrease of BOD in sewage and its non-
toxicity. A disadvantage of air injection is the limited oxygen
transfer (US EPA, 1992).
Because pure oxygen is five times more concentrated than
air, it is possible to achieve higher DO levels (57 mg L1) in
sewage by injecting pure oxygen instead of air (DO levels is
35 mg L1) (Chen and Leung, 2000; Delgado et al., 1998). Pure
oxygen may therefore be a more effective method of sulfide
control for cases where the total oxygen requirement exceeds
that which can be transferred using air injection. Use of pure
oxygen as a sulfide control method is particularly advanta-
geous in a pressurized sewer system, because dissolution of
oxygen is greater at higher pressures. The disadvantages are
that it is applicable only to the high-pressure force mains and
that it represents fire risks (US EPA, 1992).
3.2. Addition of nitrate
The preventive effect of nitrate on sulfide production has
been reported (Allen, 1949; Yang et al., 2005). Both transient
and long-term preventions of sulfide production have been
found (Allen, 1949; Beardslay et al., 1956; Carpenter, 1932;
Heukelelekian, 1943; Poduska and Anderson, 1981). Carpenter
(1932) reported that sodium nitrate was used to control odor
nuisance. Heukelelekian (1943) observed that in oxygen-
deficient systems, nitrate was reduced preferentially over
sulfate, thus diminishing H2S formation. Allen (1949) found
that the addition of 1.0 g L1 of nitrate to sewage sludge
prevented sulfide production for at least 29 days. This
prevention was attributed to the increase in redox potential
caused by the presence of nitrate. Poduska and Anderson
(1981) showed that nitrate addition could control sulfide
generation in a wastewater lagoon as long as enough nitrate
was added initially to raise the redox potential of the lagoon
above 300 mV. The addition of nitrate as a biological oxidation
strategy by means of NR-SOB will be discussed in Section 6.
4. Inhibition of SRB activity
Considering inhibition of biological activity, pH elevation is the
most common method, but other inhibitors (e.g. biocides and
molybdate) have also been considered (Jayaraman et al., 1999;
Nemati et al., 2001c; Reinsel et al., 1996). At a pH above 9.0, the
amount of H2S(aq) in solution is negligible since
the sulfide present is nearly entirely in its ionic form (HS)
(Eq. (1)). However, continuous feeding of sodium hydroxide
(NaOH) to maintain an elevated pH (more than 9) is expensive
and may disrupt downstream treatment processes. The most
effective use of sodium hydroxide is shock treatment to produce
42 (2008) 1 12 5
a pH of 12.513.0 in wastewater for a period of 2030 min (US
EPA, 1991). Such a high pH inactivates SRB in the slime layer for
a period of a few days to 2 weeks. The wastewater of the high
pH section has to be isolated at the wastewater treatment plant
(WWTP) and fed slowly into the system if it is not diluted in the
collection system (US EPA, 1991).
5. Chemical removal of sulfide
5.1. Precipitation by metal salts
5.1.1. Insoluble metal sulfides in sewage
Precipitation of metal sulfides removes dissolved sulfide from
the wastewater, thereby decreasing the amount of sulfide
available for release to the sewer atmosphere. At conditions
of low or moderate sulfide concentrations in the wastewater,
a significant fraction of the total amount of sulfide may be
present as insoluble metal (e.g. ferrous, zinc, copper, nickel
and manganese) sulfides (Nielsen et al., 2005a, b). Field
investigations conducted by the Brisbane City Council in
1980 demonstrated the importance of metal sulfide precipita-
tion for the sulfur cycle (ASCE, 1989). This study showed that
generally no dissolved sulfide was present when the total
sulfide concentration was approximately 0.12 mg S L1. Pre-
cipitation with metals present in the wastewater is therefore
believed to play a central role in controlling the dissolved
sulfide concentration and the extent of associated problems.
5.1.2. Addition of iron salts
Iron is typically one of the dominant metals present in
municipal wastewater. The concentration level of iron, which
is typically 0.41.5 mg L1, suggests the formation of iron
sulfide to be an important process of the sulfur cycle in
wastewater (Henze et al., 1997; Nielsen et al., 2005a). Because
of its effectiveness in controlling the dissolved sulfide
concentration, iron has been widely used to control sulfide
buildup in sewer networks (ASCE, 1989; Hvitved-Jacobsen
et al., 2002; Jameel, 1989). Iron salts of chloride (Jameel, 1989;
Nielsen et al., 2005a, b), sulfate (US EPA, 1974) or nitrate
(Padival et al., 1995) have been added to wastewater either in
ferric or ferrous forms. Fe (II) can remove sulfide by
precipitation as ferrous sulfide (FeS) according to Eq. (5). Fe
(III) can remove sulfide by oxidizing it chemically to elemental
sulfur while being reduced to Fe (II), which can subsequently
produce FeS (Eqs. (5) and (6)).
Fe2 HS ! FeS H ; DG : 21:0 kJ mol1 HS ; (5)
2Fe3 HS ! 2Fe2 S0 H ; DG : 160:9 kJ mol1 HS :
(6)
The precipitation of ferrous sulfide in wastewater is
believed to be a rapid process. However, Nielsen et al.
(2005a) found that iron sulfide precipitation in anaerobic
wastewater spiked with ferric chloride could take a few hours.
The formation of iron phosphate and complexation of iron
byligands (e.g. EDTA) can compete with the formation of iron
sulfide in wastewater (Araujo et al., 2000; Nielsen et al.,
2005a). Further investigation is needed to explore the sulfur
 ARTICLE IN PRESS
6 WAT E R R E S E A R C H 42 (2008) 1 12

and phosphorus transformation and the effect of iron of iron to sulfide is 1.22.5:1 (w/w) and average eliminations of
byligands (e.g. EDTA) on formation of iron sulfide in sewers. 88100% have been found (Nielsen et al., 2005a; Padival et al.,
Whether ferrous or ferric ion is more effective in controlling 1995; Tomar and Abdullah, 1994). The range in cost is
the dissolved sulfide concentration remains controversial h3.77.2 kg1 S. The costs are dependent on sulfide removal,
from the literature. Jameel (1989) reported ferrous chloride dosage of chemicals and current prices of the chemicals. In
to be more than twice as effective in controlling the dissolved Table 2, the costs are calculated from the ratio of chemicals to
sulfide concentration compared to ferric chloride. In contrast, sulfide multiplied with the current price of the chemicals.
Tomar and Abdullah (1994) reported a ferric salt solution to be
slightly more effective than a ferrous salt solution, i.e. the
5.2. Addition of oxidizing chemicals
iron dosage for complete sulfide control was 20% lower for the
ferric salt solution than the ferrous salt solution. Field studies
5.2.1. Hydrogen peroxide
however indicated that a mixture of ferrous and ferric iron
When hydrogen peroxide (H2O2) is added to wastewater, it
salts is most effective in controlling the dissolved sulfide
oxidizes dissolved sulfide and decomposes to water and
concentration (Padival et al., 1995; US EPA, 1974). They also
oxygen, thus keeping conditions aerobic. The proper ratio of
showed that despite the very low solubility of iron sulfide,
H2O2 is 1.34.0 mg H2O2 L1 to 1 mg S L1 and average elimina-
complete control of dissolved sulfide is difficult and that iron
tion of sulfide is 85100% (Table 2). The disadvantage is the
salts must be added in excess to obtain adequate control. In
short lifetime of H2O2 (less than 90 min) (US EPA 1991).
practice, it is difficult to decrease the dissolved sulfide
Therefore, it may be necessary to add the chemical at several
concentration to less than 0.2 mg L1(ASCE, 1989).
points along the sewers.

5.1.3. Operation conditions and costs 5.2.2. Chlorine

Table 2 presents a summary of the literature concerning the use Chlorine will oxidize sulfide to sulfate or to elemental sulfur,
of iron salts for hydrogen sulfide precipitation. The proper ratio depending on the pH (US EPA, 1992). Its effectiveness is

Table 2 Summary of literature related to chemical and biological technologies for hydrogen sulfide emission control in
sewer systems

Chemicals Ratio of Scale and Sulfide Average Costb References

chemicals volume of concentration elimination (h kg1 S)
to S (w/w)a reactor in upstream (%) of
(mg S L1) sulfide

FeCl2  4H2O 6.07.0:1 Plant scale, More than 4.0 90 22.426.1 US EPA (1992)
59, 000 m3c
FeSO4  7H2O 1.7:1 Plant scale, 18.025.0 9597 4.8 Tomar and
25,000 m3 d1 Abdullah (1994)
FeClSO4 1.2:1 Plant scale, 18.025.0 8898 4.5 Tomar and
25,000 m3 d1 Abdullah (1994)
FeCl2 and 2.5:1 Plant scale, 6.4 97 7.2 Padival et al. (1995)
FeCl3d 75,000 m3 d1
FeCl3 1.5:1 Lab scale, 3.8 100 3.7 Nielsen et al. (2005c)
3.00 L
H2O2 4.0:1 Plant scale, 15.0 8590 10.6 Waltrip and Snyder
76,000 m3 d1 (1985)
H2O2 1.51.6:1 Plant scale, 8.5 9095 4.04.2 US EPA (1991)
2000 m3c
H2O2 1.3:1 Plant scale, 20.0 87100 3.5 Tomar and
25,000 m3 d1 Abdullah (1994)
Cl2 9.0:1 Plant scale, 18.0 100 2.7 Waltrip and Snyder
90,000 m3 d1 (1985)
Cl2 10.015.0:1 2.84.2 US EPA (1991)
NaClO 2.0:1 Plant scale, 20.0 96100 2.6 Tomar and
25,000 m3 d1 Abdullah (1994)
Ca(ClO)2 1.8:1 Plant scale, 20.0 93100 1.9 Tomar and
25,000 m3 d1 Abdullah (1994)
NaClO and 1.0:1 Plant scale, 18.2 100 1.9 Tomar and
NaOHd 25,000 m3 d1 Abdullah (1994)
KMnO4 6.07.0:1 18.922.0 US EPA (1991)
NaNO3 6.7:1 Lab scale, 54.0 100 12.2 Jenneman et al.
0.05 L (1986)
NaNO3 0.18:1 Lab scale, 35.0 65 0.4 Okabe et al., (2003a)
1.37 L
 ARTICLE IN PRESS
WA T E R R E S E A R C H 42 (2008) 1 12 7

Table 2 (continued )

Chemicals Ratio of Scale and Sulfide Average Costb References

chemicals volume of concentration elimination (h kg1 S)
to S (w/w)a reactor in upstream (%) of
(mg S L1) sulfide

NaNO3 1.37:1 Lab scale, 10.2 100 2.5 Okabe et al. (2003b)
1.00 L
NaNO3 1.44.6:1 Lab scale, 2.53.5 9095 2.58.3 Yang et al. (2005)
3.00 L
NutrioxTMe 0.88:1 Plant scale, 5.1 6395 2.1 Bentzen et al. (1995)
3700 m3 d1
NutrioxTMe 0.60:1 Pilot scale, 9.6 95 1.5 Hobson and Yang
200 L (2000)
NutrioxTMe 2.50:1 Plant scale, 70.0 95100 6.0 Einarsen et al.
15,000 m3 d1 (2000)
NutrioxTMe 0.36:1 Plant scale, 70.0 6895 0.9 Garcia De Lomas et
50,000 m3 d1 al. (2005)
Ca(NO3)2 1.92:1 Plant scale, 2.6 100 4.4 Rodrguez-Gomez
2000 m3 d1 et al. (2005)

FeCl2  4H2O: h105 (100 kg)1; FeSO4  7H2O: h80 (100 kg)1; FeClSO4: h111 (100 kg)1; FeCl3: h85 (100 kg)1; H2O2 (27.5%): h73 (100 kg)1; Cl2 (99.6%):
h28 (100 kg)1; NaClO: h127 (100 kg)1; Ca(ClO)2: h101 (100 kg)1; NaOH: h205 (100 kg)1; KMnO4: h315 (100 kg)1; NaNO3: h35 (100 kg)1; UutrioxTM:
h21 (100 kg)1; Ca(NO3)2  4H2O: h34 (100 kg)1.
a
For the iron salts, it is the ratio of Fe to S (w/w); for the nitrate salts, it is the ratio of NO
3 -N to S (w/w); for other chemicals, it is the ratio of
chemical to S (w/w).
b
The prices of chemicals are provided by Brenntag NV Co. Ltd., VWR Inc., Belgium, Wuhan industrial Co. Ltd., China and Yara Industrial
Limited, Ireland.
c
The total volume of sewer pipes.
d
The ratio of FeCl3 to FeCl2 is 1.9:1. The ratio of NaClO to NaOH is 3.5:1.
e
NutrioxTM is the concentrated calcium nitrate, a commercially available solution of 8.8% NO +
3 , 0.6% NH4 and a density of 1.5 kg L
1
.

frequently low because of its reactions with other compo-
nents in sewage. It may be added as an aqueous solution (e.g.
sodium hypochlorite) or directly as a gas. The chemical
oxidation reaction is slower at lower sulfide concentrations,
particularly below 1 mg L1. Added directly as a gas, a ratio of
9.015.0:1 (w/w) is suggested (Tomar and Abdullah, 1994; US
EPA, 1991). Added as an aqueous solution (NaClO or Ca(ClO)2),
the proper ratio of chemicals to sulfide is 1.82.0:1 (w/w)
(Tomar and Abdullah, 1994).
5.2.3. Potassium permanganate
Potassium permanganate (KMnO4) is a strong oxidizing agent,
which converts sulfide to sulfate. It is normally supplied in a
dry state, but is fed as a 6% solution in water (US EPA, 1991).
The disadvantage is the high cost (h18.922.0 kg1 S) (Table 2).
The costs for H2O2 and chlorine are in the range of
h1.94.2 kg1 S (Table 2).
6. Biological oxidation of sulfide
Recently, it has been shown that sulfide emission control
after addition of nitrate can be explained by the action of NR-
SOB oxidizing the H2S produced by the SRB. Some studies
have been carried out in oil reservoir environments (Myhr
et al., 2002; Nemati et al., 2001a, b), and in sewage environ-
ments (soy et al., 2002; Bentzen et al., 1995; Jenneman et al.,
1986; Jobbagy et al., 1994; Okabe et al., 1999, 2003a, b). Most
experiments have been conducted using pure cultures of SRB
(Jenneman et al., 1986; Nemati et al., 2001a, b). Some experi-
ments have been done at pilot (Hobson and Yang, 2000) or
plant scale (Bentzen et al., 1995; Einarsen et al., 2000; Moody
and Riek, 1999; Garcia De Lomas et al., 2005). Studies
performed on oil reservoirs have pointed out the highly
significant role of NR-SOB as important components of the
microbial communities in experimental research on the
inhibition of sulfide production by addition of nitrate (Jenne-
man et al., 1986; Nemati et al., 2001b). Among the micro-
organisms suspected to play a critical role in these processes,
Thiomicrospira denitrificans, an e-Proteobacterium, and Thioba-
cillus denitrificans, a b-Proteobacterium, have been reported
(Kodama and Watanabe, 2003; Voordouw et al., 1996). These
two bacterial species are only able to oxidize sulfides in the
presence of nitrate, of which the reduction is associated with
the oxidation of sulfides and sulfur (Kelly et al., 1997; Kodama
and Watanabe, 2003). Anoxic sulfide oxidation with nitrate as
the electron acceptor was also observed in the presence of
Beggiatoa enrichment (Anja et al., 2006).
Sayama et al. (2005) demonstrated that marine Beggiatoa
oxidizes HS to S0, which can be stored as intracellular
globules, and subsequently to SO2 4 . Buisman et al. (1990)
demonstrated that S0 accumulates as end product in a
biological oxidation reactor when O2 is the electron acceptor.
Gadekar et al. (2006) demonstrated that S0 accumulates as
product in oil reservoir environments when NO 3 is the
electron acceptor. For the sewage environment, Nielsen
et al. (2005c) and Yang et al. (2005) discussed the process
kinetics of biological sulfide oxidation in wastewater and
 ARTICLE IN PRESS
8 WAT E R R E S E A R C H
hypothesized that S0 can be an important end-product under
anoxic conditions when O2 or NO 3 is the electron acceptor
(Eqs. (7) and (8)). Formation of sulfate was observed as soon as
the sulfide concentration reached a negligible level (Eqs. (9)
and (10)). When NO 3 is used as the electron acceptor, the
oxidation of HS to S0 increases the pH, while the oxidation S0
to SO2
4 decreases the pH (Eqs. (7)(10)) (Gadekar et al., 2006).
HS NO3  H ! S0 NO2  H2 O; (7)
HS 0:4NO3  1:4H ! S0 0:2N2 1:2H2 O; (8)
S0 3NO3  H2 O 3H ! SO4 2 3NO2  5H ; (9)
S0 1:2NO3  0:4H2 O 1:2H ! SO4 2 0:6N2 2H : (10)
The theoretical nitrate demand for sulfide oxidation to
sulfur is estimated to be 0.180.44 mg NO 1
3 -N (mg S) (Yang
et al., 2005). However, the dosages varied with the nature and
concentration of organic matter, biomass activity and ionic
strength in the different sewages (Luis et al., 2005). The
stoichiometry reported in most literature ranged from 0.6 to
4.5 mg NO 1
3 -N (mg S) , with an average sulfide elimination of
90100% (Table 2). Okabe et al. (2003a), and Garcia De Lomas et al.
(2005) reported a nitrate demand of 0.180.36 mg NO 1
3 -N (mg S) ,
with an average sulfide elimination of 6595%. The range in cost
is h1.58.3 kg1 S and the average cost in the literature is about
h2.12.5 kg1 S.
7. Outlooks
7.1. Formaldehyde or para formaldehyde
It was reported that inhibitors such as molybdate can be used
to control hydrogen sulfide emission in sewer systems
(Nemati et al., 2001c). Formaldehyde is widely used as an
inhibitor of bacteria, even in food producing processes such
as aquaculture, while it can be biodegraded in WWTPs (Heck
et al., 2001; Kajitvichyanukul and Suntronvipart, 2006; Ped-
ersen et al., 2007; Pedersen and Pedersen, 2006). Paraformal-
dehyde (n 8100) is a cheap and safe chemical and is used
as an alternative for formaldehyde in many industrial
applications (Helander, 2000). Paraformaldehyde is converted
into formaldehyde at room temperature at neutral pH in
aqueous solutions (McMurry, 2003). It is worthwhile to explore
whether formaldehyde and paraformaldehyde could be used
to lower hydrogen sulfide generation in sewers (Fig. 3).
A preliminary investigation has shown that a formaldehyde
concentration of 1020 mg L1 was sufficient to inhibit hydro-
gen sulfide generation in the sewage (Zhang et al., unpub-
lished results). Formaldehyde is readily soluble in water and
reacts substantially and reversibly with water to form
methanediol [CH2(OH)2] (Seyfioglu and Odabasi, 2007). More-
over, the sewer systems are closed so the exchange between
urban atmosphere and gas phase in sewer systems is limited.
Toxicity to sewer workers is another concern when formal-
dehyde or paraformaldehyde is used as an inhibitor. For-
maldehyde is commonly used to treat external fish parasites
and fungal diseases (Pedersen and Pedersen, 2006; Pedersen
et al., 2007). Concentrations frequently used are 2540 mg L1
formaldehyde as an indefinite bath treatment or 250 mg L1
42 (2008) 1 12
New Approaches
Novel inhibitor, MgO2 Sulfide Phages
e.g. or oxidized used to
formaldehyde or lyse SRB
CaO2 as in MFCs
urea inhibitor
formaldehyde
Fig. 3 New approaches for hydrogen sulfide emission
control in sewer systems. MFCs: microbial fuel cells; SRB:
sulfate-reducing bacteria.
formaldehyde for a 1-h bath (Wooster et al., 2005). In our
preliminary investigation, 1020 mg L1 formaldehyde was
found as the optimum dosage to control sulfide generation
in sewage. With protection equipment, the operation envir-
onment thus should be acceptable for sewer workers.
However, further study is necessary to investigate the risk
of formaldehyde to both the urban environment and the
health of sewer workers.
The price of formalin (3640% formaldehyde) is
h59 (100 kg)1 (Brenntag NV, Belgium). The range in cost for
this method, h1.33.6 kg1 S removal, is in the same range as
the biological oxidation technology (h2.12.5 kg1 S removal).
7.2. Slow release solid-phase oxygen (MgO2/CaO2)
For oil wells and river sediments, many different technologies
have been developed, which have never been used in
hydrogen sulfide emission control in sewer systems. Lee et
al. (2005) reported a CuO/MgO catalyst developed for oxida-
tion of hydrogen sulfide to sulfur in oil wells. Chang et al.
(2007) reported the use of slow release solid-phase oxygen,
such as magnesium peroxide (MgO2) and calcium peroxide
(CaO2), injected to sediments of lakes or rivers to inhibit
anaerobic biological activity. They react with water to release
oxygen slowly to produce magnesium hydroxide and calcium
hydroxide (Mg(OH)2 and Ca(OH)2). Chemical oxidation of
sulfide and biotic inhibition of SRB are two major mechan-
isms by which slow release solid-phase oxygen may be able to
decrease sulfide concentration in water (Chang et al., 2007).
After a series of lab-scale batch tests, 0.4% MgO2 was found to
be able to inhibit the formation of H2S for more than 40 days
in an SRB-enriched environment (Chang et al., 2007). By
providing long-term inhibition of the SRB activity, slow
release solid-phase oxygen provides a good alternative means
of controlling the generation of H2S in water. It might be
interesting to evaluate the effectiveness and economic
possibility of these oxidizers to control hydrogen sulfide
emission in sewer systems (Fig. 3). The challenge is how to
make the solid-phase oxygen stay in the sewers without
being flushed away. The fate of such products under normal
dry weather conditions should be sufficiently high to
guarantee full effect.
7.3. Microbial fuel cells (MFCs)
A fuel cell is an electrochemical device that continuously
converts chemical energy to electrical energy for as long as
 ARTICLE IN PRESS
WA T E R R E S E A R C H
Fig. 4 Schematic of a microbial fuel cell in a sewer system converting the sulfide to sulfur.
fuel and oxidant are supplied to it. Several researchers have
demonstrated the use of hydrogen sulfide as a fuel in a solid
oxide fuel cell (Aguilar et al., 2004; Kirk and Winnick, 1993;
Peterson and Winnick, 1996). Microbial fuel cells (MFCs) are
devices capable of directly transforming chemical to electrical
energy by electrochemical reactions involving biochemical
pathways. MFCs function on different carbohydrates but also
on complex substrates present in wastewaters. In the last 10
years, scientists devoted a lot of research and development
concerning MFCs. Rabaey et al. (2006) reported that dissolved
sulfide can be converted to elemental sulfur by MFCs. Sulfide
oxidation in the anodic compartment resulted in electricity
generation with power outputs up to 101 mW L1 net anodic
compartment. The MFCs were connected with an upflow
anaerobic sludge reactor, providing removal of up to 98% and
46% of the sulfide and acetate, respectively. It might be
interesting to control hydrogen sulfide emission by using a
MFC in sewer systems (Fig. 3). Sulfide can be oxidized when it
functions as a mobile carrier of electrons from bacteria to
electron acceptors. A scheme of a possible design of a MFC in
sewer systems is shown in Fig. 4. If the device can be
successfully developed, it should be cost-effective while the
formed sulfur can be precipitated and potentially harvested
(Krishnakumar et al., 2005). The concomitant electricity
generation can be an additional advantage.
7.4. Phages
The first phage was isolated in 1947, and since that time over
250 of these viruses have been identified (McNerney, 1999).
Phages have made a significant contribution to our knowl-
edge of bacteria (McNerney, 1999). It has been reported that
42 (2008) 1 12 9
phages can be technically used to kill bacteria, e.g. Escherichia
coli, Enterobacter aerogenes (Randerson, 2003; Verthe and
Verstraete, 2006; Verthe et al., 2004). Randerson (2003)
reported that phages could help eliminate the putative
pathogenic bacteria in farm animals, greatly lowering the
chance of human infections. The phage decreased numbers
of the unwanted bacterium by 99% in just 2 days. Verthe and
Verstraete (2006) and Verthe et al. (2004) assessed phage-
mediated removal of Enterobacter aerogenes under varying
conditions of temperature and nutrient availability. It has
been reported that phages are far more discriminating than
antibiotics (Randerson, 2003). Also, the numbers of the phage
rise exponentially as long as there are host bacteria left to
infect. The phages continue to replicate in a harmless E. coli
strain after all the target bacteria have been destroyed.
Finally, while bacteria can develop resistance as they do to
antibiotics, the phage can out-evolve them. The question
arises whether one could find the phages that can lyse SRB
efficiently (Fig. 3). If so, the method could possibly be cost-
effective because the phages may reproduce in sewer systems
where the hosts or co-hosts, SRB or E. coli, respectively, are
present. However, one will have to show that the phage will
not have an adverse effect on bacteria in activated sludge
systems, receiving water bodies, soil and human gut micro-
biota if they happen to be passed to people via water.
8. Summary and conclusions
The main problem of current hydrogen sulfide emission
control technologies is the cost (h1.97.2 kg1 S removal).
A cost-effective and efficient method is needed to control
hydrogen sulfide emission in sewer systems. This review
 ARTICLE IN PRESS
10 WAT E R R E S E A R C H
provides some new points that might be helpful for future
research, e.g. applications of formaldehyde, MgO2/CaO2, MFCs
and phages. Formaldehyde is a cost-effective chemical
(h1.33.6 kg1 S removal) to inhibit the sulfide generation in
sewers. Solid-phase oxygen is interesting because it can
provide long-term inhibition of SRB activity. For the sewer
MFCs, concomitant electricity can be generated while sulfide
occurrence can be prevented. The phages that can lyse SRB
efficiently could be cost-effective because they may reproduce
in sewers.
Acknowledgments
This work was supported by project grant G.O.A. 1205073
(20032008). The authors thank Yu Zhang and Zhiguo Yuan for
their critical reading of the manuscript.
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