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Ammonia Emissions, Impacts, and Mitigation Strategies For Poultry Production: A Critical Review

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67 views31 pages

Ammonia Emissions, Impacts, and Mitigation Strategies For Poultry Production: A Critical Review

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Version of Record: https://www.sciencedirect.

com/science/article/pii/S0301479722024926
Manuscript_b68899136ef150209c8e170eb7528c3f

Ammonia Emissions, Impacts, and Mitigation Strategies for Poultry


Production: A Critical Review
Ramesh Bahadur Bist, Sachin Subedi, Lilong Chai*, Xiao Yang

Department of Poultry Science, College of Agricultural and Environmental Sciences,


University of Georgia, Athens, GA 30602, USA.

*Corresponding author: [email protected]

ABSTRACT
Confined animal feeding operations (CAFOs) are the main sources of air pollutants such
as ammonia (NH3) and greenhouse gases. Among air pollutants, NH3 is one of the most concerned
gasses in terms of air quality, environmental impacts, and manure nutrient losses. It is
recommended that NH3 concentrations in the poultry house should be controlled below 25 ppm.
Otherwise, the poor air quality will impair the health and welfare of animals and their caretakers.
After releasing from poultry houses, NH3 contributes to the form of fine particulate matters in the
air and acidify soil and water bodies after deposition. Therefore, understanding the emission
influential factors and impacts is critical for developing mitigation strategies to protect animals’
welfare and health, environment, and ecosystems. This review paper summarized the primary NH3
emission influential factors such as how poultry housing systems, seasonal changes, feed
management, bedding materials, animal densities, and animals’ activities can impact indoor air
quality and emissions. A higher level of NH3 (e.g., >25 ppm) results in lower production efficiency
and poor welfare and health, e.g., respiratory disorder, less feed intake, lower growth rates or egg
production, poor feed use efficiency, increased susceptibility to infectious diseases, and mortality.
In addition, the egg quality (e.g., albumen height, pH, and condensation) was reduced after laying
hens chronically exposed to high NH3 levels. High NH3 levels have detrimental effects on farm
workers’ health as it is a corrosive substance to eyes, skin, and respiratory tract, and thus may
cause blindness, irritation (throat, nose, eyes), and lung illness. For controlling poultry house NH3
levels and emissions, we analyzed various mitigation strategies such as litter additives,
biofiltration, acid scrubber, dietary manipulation, bedding materials. Litter additives were tested
with 50% efficiency in broiler houses and 80-90% mitigation efficiency for cage-free hen litter at
a higher application rate (0.9 kg/m2). Filtration systems such as multi-stage acid scrubber have up
to 95% efficiency on NH3 mitigation. However, cautions should be paid as mitigation strategies
could be cost prohibitive for farmers, which needs assistances or subsidies from governments.

Keywords: Poultry production; waste management; air emissions; mitigation strategy

© 2022 published by Elsevier. This manuscript is made available under the Elsevier user license
https://www.elsevier.com/open-access/userlicense/1.0/
1. Introduction
Confined animal feeding operations (CAFOs) are important sources of atmospheric air
pollutants that impact the environment and ecosystems (Zhao et al., 2015; Ni et al., 2017a, 2017b;
Chai et al., 2014, 2016; Bist and Chai, 2022). The primary air pollutant emissions from animal
operations include ammonia (NH3), particulate matter (PM), hydrogen sulfide (H2S), nitrous oxide
(N2O), methane (CH4), carbon dioxide (CO2), and volatile organic compounds (VOCs), which
pose a high potential risk to the health and welfare of animals and their caretakers (Figure 1; EPA,
2004; Ritz et al., 2004; Ni et al., 2012, 2017a, 2017b; Swelum et al., 2021). Among these
pollutants, NH3 is a major harmful pollutant. The total national NH3 emission from livestock and
poultry wastes accounted for over 60% of total atmospheric NH3 emissions in North America
(EPA, 2004; Liang et al. 2005b; Chai et al., 2014). By 2030, NH3 emissions to the atmosphere
from animal farming (e.g., beef, dairy, swine, and poultry) are predicted to reach 2.67 million
metric tons year-1 (EPA, 2020). Poultry production (e.g., laying hens and broilers) is one of the top
contributors to atmospheric NH3 emissions in the United States (EPA, 2004; Ni et al., 2017a,
2017b).

Figure 1. Air emissions from poultry production systems.


Ammonia emissions from the poultry sector are mainly linked to the increased poultry and
egg production required to supply a growing food demand for a growing population (Galloway et
al., 2003; Xin et al., 2011). Higher production of poultry products results in a higher amount of
nitrogen-containing manure (i.e., feces and uric acid). The amount of nitrogen in manure
significantly impacts NH3 production, so rations may be prepared with reduced dietary crude
protein and supplemented with limited amino acids to match avian dietary requirements to
minimize N concentration in feces (Ferguson et al., 1998; Gates et al., 2000; Wu-Haan et al., 2010;
van Emous et al., 2019). Ammonia levels tend to be high in poultry houses as fresh manure
contains about 75% moisture, which favors the generation of NH3 from manure-N. Exceptionally,
high levels of NH3 are seen during the winter season in all kinds of houses because of the decreased
airflow or ventilation rates (David et al., 2015; Zhao et al., 2015). High indoor NH3 levels in
poultry houses have generated global and public concerns due to harmful impacts on caretakers'
health and animal well-being (Broom and Johnson, 1993; Frank et al., 2004; Ni, 2015; EPA, 2022).

2
Chickens are very sensitive creatures that require precisely controlled indoor climate
conditions inside poultry houses, and thus it is critical to reduce NH3 emissions or suppress indoor
NH3 concentration (Dawkins et al., 2004; Liu et al., 2019). Producers are suggested to either reduce
chicken count or discover strategies to reduce NH3 emissions to meet government and industry-
group guidelines and avoid health concerns for chickens (Roberts et al., 2007; Oliveira et al.,
2019). Ammonia monitoring and mitigation have been widely conducted worldwide in different
poultry houses. However, it’s hard to compare results directly because no tests were conducted
under the same situation spatially and temporally. Therefore, it’s critical to previous group studies
in a new way that allows readers to understand findings directly. This review article aims to
summarize detailed information about NH3 emission sources, influential factors, impacts on
animals’ health and welfare, and mitigation strategies. The primary objectives were to 1)
summarize factors that affect NH3 levels in the poultry houses, 2) conclude potential mitigation
strategies to reduce its emission, and 3) discuss the pros and cons of different methods and
expectations on new strategies.
2. Governmental and Industry Guidelines for NH3 Control
Chickens and caretakers exposed to a high level of NH3 (e.g., >25 ppm) may irritate
mucous membranes (eyes and respiratory system), increase susceptibility to respiratory disorders,
and may affect food intake, food conversion ratio, growth rate, and even causes death (McLean et
al., 1979; Kristensen et al., 2000; Roney & Llados, 2004; Xin et al., 2011). According to the
production guidelines of United Egg Producers (UEP), NH3 concentration in laying hen houses
should generally remain below 10 ppm and not exceed 25 ppm (UEP, 2006, 2017). Moreover,
atmospheric NH3 concentration should ideally be below 25 ppm and should not exceed 50 ppm.
At concentrations of 25 ppm, laying hens perceive ambient NH3 to be highly unpleasant
(Kristensen et al., 2000). The suggested NH3 threshold for pullet housing and layer housing should
be 25 ppm (18 mg m-3) (UEP, 2017).
The current NH3 exposure limit of 25 ppm is based on human safety (e.g., animal
caretakers) rather than animals’ welfare. The National Institute for Occupational Safety and Health
(NIOSH) suggested using the occupational exposure limit (OEL) of 25 ppm for 8 hours and 35
ppm for 15 minutes, respectively (Barsan, 2007). However, European laws (COMMISSION
DIRECTIVE 2000/39/E.C., Council Directive 98/24/E.C.) recommends 20 ppm or 14 milligrams
per cubic meter (mg/m3) for an 8-hour NH3 exposure (CDC, 2018). The general guidelines on NH3
concentrations are summarized in Table 1. It’s challenging to control NH3 levels during the winter
season in poultry houses (Liang et al., 2005a; Green et al., 2009; Chai et al., 2012), therefore,
specific mitigating strategies are needed considering the health and welfare of chickens and their
caretakers.
Table 1. Recommended NH3 occupational exposure limit in different countries.
Country Occupational exposure limit References
3 3
Australia, New Zealand, Peru, 25 ppm (17 mg/m ) for 8 hours, 35 ppm (24 mg/m )
Japan for short-term exposure
Belgium, Denmark, European 20 ppm (14 mg/m3) for 8 hours, 50 ppm (36 mg/m3)
Commission, Finland, Hungary, for short-term exposure
Iceland, Republic of Egypt
India, Korea, Mexico, Sweden, 25 ppm (18 mg/m3) for 8 hours, 35 ppm (27 mg/m3) CDC, 2018
Norway, for short-term exposure
Sweden 25 ppm (18 mg/m3) for 8 hours, 50 ppm (35 mg/m3)
for short-term exposure

3
United Kingdom 25 ppm (18 mg/m3) for 8 hours, 35 ppm (25 mg/m3)
for short-term exposure
Russia 20 mg/m3 for short-term exposure
USA Pullet and layer housing shall be 25 ppm (18 mg m- UEP, 2017
3
)
Below 10 ppm and does not exceed 25 ppm inside
USA the house. UEP, 2006
Ideally, be below 25 ppm and should not exceed 50
ppm in the atmosphere
USA 35 ppm (27 mg/m3) and 25 ppm (18 mg/m3) for 15 Roney and Llados
minutes and 8 hours, respectively 2004; Barsan, 2007;
NIOSH, 2007;
OSHA 2020
Sweden A threshold is 25 ppm, but in winter, it reaches 80 Carr et al., 1990
ppm
Note: UEP – United Egg Producers (an agricultural cooperative in the United States which represents the interests of
American egg producers); NIOSH - National Institute for Occupational Safety & Health (a research agency focused
on the study of workers’ safety and health under CDC (Centers for Disease Control and Prevention) in the USA).
3. Emissions processes and influential factors in poultry houses
Ammonia is a highly irritating, colorless gas produced from microbial decomposition of
nitrogen-containing substances like manure (feces and urine) and litter (Moum et al., 1969; EPA,
2022). Nitrogen found in animal feces is mainly unabsorbed protein and uric acid (poultry) or urea
(mammals) (EPA, 2004). Unabsorbed protein and uric acid are the two primary nitrogen
components found in poultry feces contributing 70% and 30% of total nitrogen, respectively
(Koerkamp, 1994). Once excreted, nitrogen in excreta present in the form of urea (4-12%), uric
acid (40-70%), and nitrogen of feed protein (10-40%) are quickly hydrolyzed to form NH3 through
a series of microbial degradation in the presence of microbial enzymes in the manure (EPA, 2004;
Drozdz et al., 2020) as shown in Figure 2.

Figure 2. Process of NH3 production from poultry houses.


Water (H2O or moisture) plays a key role in the reproduction of microorganisms and the
functioning of enzymes that convert uric acid (C5H4N4O3) to urea,. Bacillus pasteurii is considered
one of the most important uricolytic bacteria facilitating NH3 production in the litter (Ni, 2015;
Schefferle, 1965; Ritz et al., 2004). In addition, higher pH, moisture content, and temperature
generally favor NH3 emissions from the poultry manure or litter (Dunlop et al., 2016; EPA, 2022).

4
Ammonia emissions in poultry houses can be affected by climatic circumstances,
geographical location, and the wide variety of management strategies that apply (Morgan et al.,
2014; Ni, 2015). Emission influential factors can differ dramatically from one operation to another
due to differences in diets, housing systems, and management procedures (Figure 3). Housing and
management factors including housing style, bird density, litter conditions, handling methods, and
ventilation rate are reported critical to indoor NH3 levels (Dawkins et al., 2004). In addition, indoor
environmental parameters such as temperature, relative humidity, manure/litter pH level, air
velocity can be correlated to the NH3 emissions directly or indirectly (Faulkner & Shaw, 2008).

Figure 3. Key influential factors for NH3 emissions in poultry houses.


3.1 Effect of housing systems on NH3 emissions
The amount of NH3 emission depends on the types of housing system (Table 2). Studies
have shown that the hen houses with manure belts (MB) result in the lowest NH3 emissions
compared to high-rise (HR) and cage-free (CF) (Liang et al., 2003, 2005b; Green et al., 2009; Chai
et al., 2012). Similarly, houses with slats may gather manure under feeding, whereas some houses
(like HR) feature a pit where fans dry the manure. According to Zhao et al. (2015) found that daily
mean NH3 emission is much higher in CF hen houses compared to the conventional cage (CC) and
enriched colony (EC) housing systems. In addition, CF houses tend to have higher NH3 levels
during the winter season due to reduced ventilation (Zhao et al., 2015; Winkel et al., 2016; Ni et
al., 2017a).

5
Table 2. Comparison of ammonia emission/concentration from different housing system.
Housing Location Monitoring Temperatur NH3 NH3 Reference
system device e (°C) emission level (ppm)
(g day-
1
bird-1)
MB Ohio, U.S. PMA 13.3 – 29.1 0.099 ± N/A Tong et al., 2021
0.004*
MB Indiana, U.S. PMA 26.7 ± 2.3 0.28* N/A Ni et al., 2017 a

MB Milan, Italy PMA N/A N/A 4.95 Costa et al., 2012

MB1 Indiana, U.S. PMA 20.0 - 31.0 N/A 13.3 ± 9.1 Ni et al., 2012
MB2 14.9 – 31.2 12.9 ± 10.5
MB North-central Iowa, PMU 22.8 N/A 1–7 Liang et al., 2003
U.S.
MB Iowa, U.S. Drager N/A N/A 2.8 Liang et al.,
Pennsylvania, U.S. sensor 5.4 2005b
MB Milan, Italy PMA N/A N/A 4.95 Costa et al., 2012

MB Iowa, U.S. PMU 20.6 N/A 9 – 24 Green et al., 2009


HR 24.6
HR 1 Indiana, U.S. PMA 25.8 ± 2.6 N/A 52.0 ± 41.8 Liu et al., 2019
HR 2 27.5 ± 2.8 48.9 ± 40.6
HR Indiana, PMA 26.7 ± 2.4 1.08 ± 0.42* N/A Ni et al.,
U.S. 2017b
HR Indiana, PMA 27.5 ± 2.5 N/A 48.9 ± 39 Chai et al.,
U.S. and 25.8 ± and 51.9 ± 2012
2.3 40.7
HR Iowa, U.S. Drager sensor N/A N/A 44.8 Liang et al.,
Pennsylva 35.9 2005b
nia, U.S.
HR North- PMU 22.8 N/A 9 – 108 Liang et al.,
central 2003
Iowa, U.S.
HR Midwest, PMA N/A N/A 4.0 Zhao et al.,
U.S. 2015
EC Midwest, PMA N/A N/A 2.8 Zhao et al.,
U.S. 2015
FR Norway Drager gas 19.7 ± N/A 66 – 120 Nimmermar
detection sensor 0.34 k et al.,
2009
FR Iowa, U.S. PMU 15.5 N/A 85 – 89 Green et al.,
2009
AV Midwest, PMA N/A N/A 6.7 Zhao et al.,
U.S. 2015
AV Milan, PMA N/A N/A 3.85 Costa et al.,
Italy 2012
AV Beek Chemiluminesce 22 N/A 1 – 16 Koerkamp
Bergen, nt analyzer &
Dutch Bleijenberg,
1998
AV England Chemiluminesce 12.5 N/A 12.3 Wathes et
nt analyzer al., 1997

6
AV Norway Drager gas 17.9 ± N/A 21 – 42 Nimmermar
detection sensor 0.79 k et al.,
2009
Broiler England Chemiluminesce 17.5 N/A 24.2 Wathes et
nt analyzer al., 1997
Broiler Netherland Chemiluminesce N/A 0.27 N/A Groot
s nt analyzer Koerkamp
et al., 1998
Broiler USA PMU N/A 0.47-0.98 N/A Wheeler et
al., 2006
Turkey USA PMA N/A N/A 8.6 ± 10.0 Li et al.,
grow-out 7.3 ± 7.9 2011
Note: N/A= Not available or no data found; HR- high rise layer house; MB – manure belt layer house; AV -aviary
cage-free layer house; EC -enriched colony layer house; PMA- Photoacoustic multi-gas analyzer; PMU - Portable
monitoring unit.
3.2 Effect of bedding, litter moisture, pH, and temperature
3.2.1 Bedding materials and litter moisture
The floor-based poultry house (e.g., broilers or cage-free hen houses) uses bedding
materials as basis in forming litter to meet birds' health and welfare criteria. The litter quality
changes with the change of bedding materials that are either organic (plant-based material like
wood) or inorganic (stone, clay, and sand) aims to provide comfortable, nontoxic, and suitable
moisture absorbent medium for chickens (Viegas et al., 2012, Munir et al., 2019). According to
Bist et al. (2022), pullets (young layers) raised in dryer bedding materials (pine shavings with
<10% moisture content) result in lower NH3 concentrations (< 5 ppm). Among different bedding
materials, wood shavings (WS) have been extensively used as bedding materials because of
humidity-regulating characteristics and antibacterial properties, which affect the culturing of NH3-
generating bacteria (Cabrera et al., 2018). Miles et al. (2011b) reported that chicken houses litter
floor using WS had less NH3 levels than sand and vermiculite. Besides, the WS litter floor was
reported with 50% lower NH3 than rice hulls litter floor. It has been suggested that optimal
management of bedding materials not only reduce NH3 emissions but also decrease odor emissions
from barns (Dunlop et al., 2016).
Table 3. Effects of bedding materials and moisture content on NH3 emissions or concentrations.
Bedding Moisture NH3 concentration (ppm) NH3 emission rate Reference
materials content (%)
Sawdust 12.39 15.44 N/A Tan et al., 2019

Sawdust 56.2 N/A 54 # Atapattu et al.,


2008
Pine shaving 25 1,377 N/A Lien et al., 1998

Wood shavings NF 54.0 ± 0.56 N/A Sahin and Celen,


2021
Wood shavings 9.7 N/A 12.3 g/hen Van Harn et al.,
2012
Wood shavings 33.3 N/A 7.0 * Garces et al.,
2013
WS & Rice 7.1 & 10.0 N/A 0.9 – 2.6* Miles et al.,
hulls 2011b

7
Rice hulls NF 56.3 ± 0.72 N/A Sahin and Celen,
2021
Rice hulls 13.94 13.36 N/A Tan et al., 2019

Rice hulls 34.5 N/A 7.8* Garces et al.,


2013
Peanut hulls 27 1,195 N/A Lien et al., 1998

Straw 9.38 15.09 N/A Tan et al., 2019

Wheat straw 9.2 N/A 13.6 g/hen Van Harn et al.,


2012
Rapeseed straw 10.9 N/A 12.0 g/hen Van Harn et al.,
2012
Grass 30.8 N/A 21.2 Garces et al.,
2013
Maize silage 10.2 N/A 7.8 g/hen Van Harn et al.,
2012
Coconut husk 50.0 N/A 7.6 * Garces et al.,
2013
Paddy husk 58.6 N/A 44 # Atapattu et al.,
2008
Corn cob 24.0 N/A 11.1* Garces et al.,
2013
Tea leaves 11.70 35.21 N/A Tan et al., 2019

Refused tea 57 N/A 13 # Atapattu et al.,


2008
Newspaper 25.7 N/A 15.7 Garces et al.,
2013
Vermiculite 1.0 N/A 9.1 * Miles et al.,
2011b
Sand 7.2 N/A 24.0* Garces et al.,
2013
Sand 0.1 N/A 5.3 * Miles et al.,
2011b
N/A= Not available or data found, * mg NH3-N per 100 g manure; # mg/kg litter per hour.
Fresh poultry manure contains about 75% moisture, which may result in the loss of most
manure nitrogen in the form of NH3 gas in a short period if no mitigation strategies are applied
(Ni, 2015). Management practices like manure belt drying, frequent cleaning/removing, and
ventilation rate adjustment affect NH3 emissions and indoor air quality. Manure qualities and
handling procedures significantly influence the generation of aerial components and their outcome
during aerial transport from CAFOs (Xin et al., 2011). Ammonia emissions and concentrations in
high-rise (HR) houses are substantially higher than those from manure belt (MB) because HR
houses are not cleaned until the end of the egg production flock, and thus manure in pit tends to
contain a higher percentage of moisture (Liang et al., 2005b; Green et al., 2009; Chai et al., 2010;
Ni et al., 2012). It was found that daily manure removal in MB houses released 74% less NH3 than
semi-weekly removal of fresh manure on the belt. For cage-free (CF) hen houses, manure dropped
on the floor is often cleared between flocks resulting in higher NH3 emissions in winter due to
condensed water from the ceiling to the floor (Chai et al., 2019).
Poultry house litter moisture is affected by many other factors, such as dietary factors,
ventilation condensation, drinker spillage and malfunctioning (Patterson, 2005). Drinker

8
management is vital since simple leak checks and height modifications can significantly influence
LMC. It has been demonstrated that using nipple drinkers instead of bell drinkers reduces LMC
and NH3 generation (Elwinger & Svensson, 1996). However, the area near the nipple drinker had
higher LMC than other locations within the same house (Miles et al., 2011; Yang et al., 2022).
3.2.2 Effect of pH on NH3 emissions
The pH of excreted poultry manure and litter is found between 7.5 and 8.5 (alkaline pH)
on average, which is optimal for the NH3 production bacteria (Elliott & Collins, 1982; EPA, 2004;
Chen et al., 2021). Therefore, lowering pH levels in manure or litter prohibits the decomposition
of uric acid as urea and the conversion of ammonium into NH3 gas (Warren, 1962; Li et al., 2013).
The equilibrium (NH3 + H+ ⇆ NH4+) shifts toward the less volatile NH4+ ion after acidification
(Roberts et al., 2007; EPA, 2022). Ammonia emissions were reported lower when the manure or
litter was in acidic conditions (i.e., pH<7.0) (Carr et al., 1990; Reece et al., 1979; Zhang et al.,
2011, 2020; Wang et al., 2021). For instance, reducing the pH of poultry litter from 7 to 3 resulted
in NH3 reduction of 60-80% (Ashtari et al., 2016; Chai et al., 2017). Details are summarized in the
Table 4.
Table 4. Volatilization of NH3 from manure at various litter pH levels.
Litter pH Results References
9 Uric acid decomposition/ NH3 productions reach maximum Li et al., 2013
8.5 Bacteria require optimum growth Elliott & Collins, 1982; Chen
et al., 2021
8 or >8 Highest NH3 productions Reece et al., 1979
7.5 – 8.5 Rapid NH3 volatilization EPA, 2004
>7 The NH4+: NH3 ratio increases, favoring uric acid decomposition Warren, 1962; Li et al., 2013
=7 Start to increase NH3 productions Carr et al., 1990
<7 NH3 production is negligible or the lowest. Reece et al., 1985
Reduces the uricolytic bacterial population Ferguson et al., 1998
3 vs. 7 NH3 emissions from pH 7 was 2-3 times of litter of pH 3 Chai et al., 2017
3 Lowest NH3 emissions and PM reduction by 60% to 70% Chai et al., 2017
2 NH3 concentrations decreased by 84.3% Ashtari et al., 2016

3.3 Feed nutrition contents


Broilers and layers in commercial houses are fed with high crude protein (CP) diet to meet
their daily nutritional needs for growing and production (meat or eggs) (Summers, 1993; Beer,
2009; van Emous et al., 2019). Higher CP feed tends to result in increase nitrogen in manure and
a higher NH3 emission, because undigested proteins and uric acid are primary NH3 emission
sources (Koerkamp, 1994). Similarly, the use of fibrous diets like distiller dried grains plus soluble
(DDGS) in diet had shown reduced NH3 emission without negative impact on egg production
(Matterson et al., 1966; Wu-Haan et al., 2010). The diet formulation with 20% DDGS resulted in
an NH3 reduction of 26%. That’s why it is very important to have an improvement in nutrient
utilization efficiency. Precision diet management is critical for mitigating NH3 emissions and
nitrogen nutrition losses, then more nitrogen nutrients will be used for land application and crop
production.

9
Table 5. Effect of poultry diet manipulation on NH3 concentrations.
Diet Type Ammonia References
concentrations/emissions
Basal diet (16.52% CP) 7.29 mg/m3
2% & 4% Beechwood biochar 6.20 and 6.25 mg/m3 Kalus et al., 2020
3% and 6% BC-glycerin-aluminosilicates mix 6.05 and 6.22 mg/m3
High CP (13%) 113.8 mg/h-m2 van Emous et al.,
Low CP (11.5%) 103.6 mg/h-m2 2019
Standard industry diet (SID, 18.6% CP) -
7% EcoCal (18.5 % CP) 39.2% lower than SID Li et al., 2012
10% DDGS (18.3% CP) 14.3% lower than SID
0% DDGS (18.3% CP) 3.1 mg/g*
10% DDGS (18.3% CP) 2.7 mg/g* Wu-Haan et al., 2010
20% DDGS (18.3% CP) 2.4 mg/g*
Control diet 3.9 mg/g
(corn & Soybean hulls)
10% DDGS 1.9 mg/g Roberts et al., 2007
7.3% Wheat middling (WM) 2.1 mg/g
4.8% soybean hulls (SH) 2.3 mg/g
215 g/kg CP 31% higher than 196 g/kg CP Ferguson et al., 1998
196 g/kg CP
19% to low 5% dietary protein 50% higher than 5% CP
11% & 17% dietary protein 40% higher than 11% dietary Summer, 1993
protein
*Daily NH3 emission of feed intake, mg/m3 = milligram per cubic meter unit.

3.3 Effect of seasons and temperature


The emissions of NH3 across the year are varying periodically due to change of seasons
(temperature) and house ventilation (Chai et al., 2012; Ni et al., 2017a, 2017b; Liu et al., 2019).
The degree of seasonal change varies according to geographical area, animal housing, and animal
production practices (EPA, 2004). The seasonal change may be less noticeable in moderate
temperature zones, such as the Mediterranean area (Calvet et al., 2011). The outdoor and indoor
environmental temperatures in poultry houses can significantly influence levels of NH3. Zhao et
al. (2015) discovered an inverse association between outside temperatures and NH3 concentration
within the house. Furthermore, significant fluctuations in indoor NH3 concentration can be caused
by rapid weather conditions and house management practices (EPA, 2004). For instance, high
temperature and lower ventilation rate enhance the volatilization of NH3 and affects NH3 emission.
During the winter, the ventilation rate is reduced to minimize additional heating expenses
associated with higher humidity caused by condensation (Nimmermark et al., 2009). Similarly,
reduced ventilation resulted in higher concentrations of NH3 (50-100 ppm) in the atmosphere of
poultry housing systems seen in the north-central states (Anderson et al., 1964). The housing
system like HR and MB were more temperature-friendly, and the NH3 levels were more
pleasurable than the CF houses (Green et al., 2009). However, the CF houses had the lowest
temperature in summer, while NH3 levels were similar in all housing types (mean 3 to 9 ppm). The
emissions of NH3 from HR layer houses were diurnal and seasonal, which results indicated a
coefficient variation of between 12 and 58 percent during the day, 34 percent in the daytime, 27
percent in months, and 24 percent in seasons (Liang et al., 2005 b). Diurnal fluctuations were found
to have elevated NH3 emissions when the chicken in a CF system was active on the littered floor

10
(Xin et al., 2011). Details about the effect of diurnal and seasonal change were summarized in
Table 6 in the supplementary materials.
3.4 Bird age, stocking density, and activities
The density of chickens is varying from country to country. In the USA, a standard broiler
house with floor areas of 2000 m2 grows about 20,000-25,000 chickens (5 flocks per year)
(Shahbandeh, 2022). Ammonia production is affected by birds' density that a higher stocking
density house results in higher moisture content of litter and NH3 emissions (Zhang et al., 2011).
According to Abouelenien et al. (2016), NH3 emissions are significantly increased after the
stocking density of broilers was increased from 10 birds/m2 to 20 birds/m2. It is found that the
birds having a stocking density of 10 birds/m2 had an averaged NH3 level of 3.5 mg L-1 at 28-36
days old, while birds with a stocking density of 20 birds/m2 had 20.28 - 31.4 mg L-1 at 28-36 days
old, respectively. In laying hen houses, high stocking density (413-620 cm2 per bird) had 51%
higher NH3 emissions (mg bird-1day-1) than low density (155-206 cm2 per bird) for 4 to 5 WOA
pullets and averaged 22% higher NH3 emission for laying hens (Mendes et al., 2012). These results
showed that with increasing stocking density, NH3 emissions are significantly increased higher. In
addition, Bist et al. (2022) reported that NH3 production in CF housing is higher with the increase
in birds’ age, where pullets were provided with more litter floor space.

4. Effects of NH3 on the health and welfare of animals and caretakers


4.1 Impacts on chickens’ health and welfare
High levels of NH3 have negative impacts on animals’ health and welfare. Young animals
were found more susceptible to high level of NH3 exposure than adult animals (Hoang et al., 2016).
Ammonia with a concentration greater than 25 ppm damages the chickens’ eyes
(keratoconjunctivitis or ocular damage) and the respiratory system (Olanrewaju et al., 2007).
Ocular damage could be caused by over 7 days of NH3 exposure at 25–50 ppm. Long-term
exposure to NH3 can cause abnormalities in the spleen, kidneys, and adrenal glands (Quarles &
Caveny, 1979). The primary harmful impacts of high concentrations of NH3 in chicken houses
include lower growth rates, reduced egg production, damaged air tract, and poor egg quality (Xin
et al., 2011). The egg quality (albumen height, pH, and condensation) was shown to be lowered
when laying hens were chronically exposed to NH3 > 50 ppm, which was linked to production loss
(Xin et al., 2011). Similarly, high concentrations (> 75 ppm) not only impair the development and
production rate but also decrease the meat quality of broilers (Piorkowska et al., 2016). Broiler
chicks exposed to various levels of NH3 (3, 25, and 75 ppm) were found to have several
differentially expressed genes in their muscles. The current genetic study with RNA sequencing
analysis discovered that NH3 caused gene changes in breast muscle (Piorkowska et al., 2016; Yi
et al., 2016a). In addition, broiler exposure to the higher concentration of NH3 led to lower body
weight, lower muscle antioxidative capability, and higher mortality rates (Miles et al., 2004; Wei
et al., 2014).
Extreme high NH3 levels (e.g., >100 ppm) in poultry houses could result in severe effects
on the respiratory system and cause the deciliation of the upper epithelium region of the trachea in
broiler chickens (Oyetunde et al., 1978). Inhaling gaseous NH3, aerosols containing NH3 dissolved
in water, or NH3 linked to dust particles causes intimate contact with the respiratory epithelia.
Macroscopic and microscopic lesions in air sacs were seen as early as 12 hours after broiler hens

11
were subjected to 100 ppm NH3. In hens (Anderson et al., 1966) and turkeys (Nagaraja et al.,
1983), these consequences include the loss of tracheal cilia and histological alterations to the
tracheal epithelium. The absence of tracheal cilia reduces the efficiency of the respiratory system's
physiological defense mechanism (David et al., 2015). Ammonia exposure increases the chances
of infections or diseases. According to Anderson et al. (1964), NH3 exposure for 72 hours
significantly enhanced the chicken infection rate of Newcastle disease virus (NDV). The chicken
exposed to NH3 (> 25 ppm) was tested against the control group (0 ppm) with low levels of
hemagglutination antibodies for NDV, which resulted in reduced immunity (Wang et al., 2010).
Even the response to live vaccinations for infectious bronchitis and NDV appears to be more
severe, with the bursa Fabricius atrophying (Valentine, 1964; Quarles & Kling, 1974). Similarly,
when turkeys were exposed to 10 to 40 ppm NH3 and subsequently challenged with E. coli, they
had more germs in their lungs than animals that were not exposed (Nagaraja et al., 1984). The
effects of different NH3 concentrations on birds' health are listed in Table 7 in supplementary
materials.
4.2 Birds’ behaviors restriction
Ammonia concentration has a direct influence on bird behaviors. Birds prefer fresh air to
display behavioral reactions to discomfort, indicating that a high amount of atmospheric NH3 is
unpleasant (Kristensen, 2000, David et al., 2015). When laying hens were given the option of
choosing between compartments with 0, 10, 20, 30, or 40 ppm NH3, they picked the fresh air
(Wathes et al., 2002). In comparison to the NH3-polluted surroundings, hens spent most of their
time foraging (30.3%), resting (24.6%), and preening (14.3%) (Kristensen et al., 2000). These
actions accounted for 69.2 % of the overall time budget. Hens performed more frequent behaviors
at 0 ppm than at 25, 35, and 45 ppm. In addition, there was individual variance in their occupancy
of the various NH3 concentrations. Individual occupancy variation was more extensive at 45 ppm
than lower concentrations (Kristensen et al., 2000). Similarly, when broiler breeders are given a
free option to choose between 4, 11, 20, and 37 ppm ambient NH3 over 16 days, they avoid the
two higher concentrations. Broilers suspected of keratoconjunctivitis due to NH3 were seen
huddling in groups, rubbing their eyes against their wings, keeping their eyes closed, and
expressing signs of hypersensitivity to light (Bullis et al., 1950). Ammonia-containing feathers
may have developed an unpleasant taste or odor and substantially affected preening behaviors
because preening necessitates direct contact between the head and the feathers' surface (Kristensen,
2000). In addition, NH3 exposure can harm poultry welfare in several ways linked to the FAWC's
five freedoms such as freedom from a) hunger, thirstiness, & undernutrition, b) pain, injury, &
disease, c) discomfort, d) normal behaviors expressions, and e) fear & distress (Brambell, 1965;
FAWC, 1992; Kristensen, 2000). The behavioral effects of elevated NH3 on birds were
summarized in Table 8 in supplementary materials.
4.3 Poultry caretaker’s health and welfare
Exposure to high NH3 environment is risky for the health of both chickens and their
caretakers, the primary concerns include severe burning of skin, eyes, throat, or lungs. These burns
may be sufficiently serious to result in continuous blindness, lung illness, or even death of a person
(Roney & Llados, 2004). Inhalation or dermal exposure to NH3 usually results in blurred vision.
However, more severe exposures result in a significant increase in blood NH3 levels
(hyperammonemia) which can cause diffuse nonspecific encephalopathy, muscle weakness,
decreased deep tendon reflexes, and loss of consciousness (Roney & Llados, 2004). Acute NH3
exposure can cause immediate mortality due to airway obstruction.

12
Exposure to toxic levels of NH3 could result in chemical burns or swelling of sensitive
tissues such as the respiratory tract, eyes, and exposed skin. The sensory fragrance and the irritating
impact on the eyes and the mucous membranes of the upper respiratory system are typically
human-detected at concentrations of 100 ppm when introduced for 5 to 30 seconds (McLean et al.,
1979). Odors start to be detected around 5-50 ppm (Roney & Llados, 2004). After prolonged or
frequent exposures, humans may acquire chronic sinusitis that desensitizes them to the odor of
NH3, which could affect the smelling of NH3 before it reaches much higher levels (Laciak, 1977).
Table 9 (in supplementary materials) summarizes various characteristics of NH3 exposure on
human health and welfare.
4.4 Impacts on production efficiency
The main toxic gas linked to the loss of poultry production is NH3. High concentrations of
NH3 in poultry houses reduce feed intake, inhibit bird growth (Charles & Payne, 1966), reduce
egg production (Charles & Payne, 1966), damage the respiratory tract (Nagaraja et al., 1983),
increase susceptibility to infectious diseases (Anderson et al., 1964) and the incidence of air
sacculitis (Oyetunde et al., 1978) and Mycoplasma gallisepticum (Sato, 1973; Green et al., 2009).
High amounts of atmospheric NH3 can also harm egg quality by lowering albumen height, raising
albumen pH, and causing albumen condensation in eggs in poultry houses (Cotterill & Nordskog,
1954). The consequences of NH3 exposure on pullets may have a long-term impact on laying hens
(Amer et al., 2004). High NH3 environment (e.g., 100 ppm) was also reported to cause hens to lay
eggs later and produce fewer eggs (Charles & Payne, 1966). During the growth stage (young birds
<17 weeks), birds exposed to 78 ppm NH3 would take a longer period to attain 50% egg production
and had fewer egg-producing days during laying state (>20 weeks). Amer et al. (2004) reported
that hens exposed to 100 ppm NH3 for four weeks resulted in significant less food and water
consumptions, fewer eggs, reduced egg weight, and decreased body weight. A substantial drop in
egg production and an increase in mortality were revealed by NH3 exposure at 200 ppm for 17
days (Deaton et al., 1984). In addition, NH3 with concentrations of 50 ppm over 7 to 8 weeks has
resulted in lower appetite and, thus, more inadequate food consumption efficiency and, in turn,
causes lower body weight in broilers (Caveny et al., 1981). The researchers noted that NH3 levels
of 25 and 50 ppm from day one reduced feed conversion ratio in broiler cockerels and raised
production costs (Caveny et al., 1981). The impact of NH3 concentrations on production efficiency
was summarized in Table 10 in the supplementary materials.
5. Emission Mitigation Strategies
There are mainly two approaches to control emissions of air pollutants in animal houses:
pre-excretion (i.e., reduction at the source before manure is produced, e.g., diet manipulation and
feed additive) and pre-release (i.e., removal from the flow of gases before dispersing in the
environment, e.g., litter additives, management, and new house design) (Ritz et al., 2004; Ni, 2015;
Chai et al., 2018a, 2018b). Based on their working principles, mitigation technologies can also be
divided into microbiological, biochemical, chemical, managerial, physical, and physiological
methods, elaborated in Figure 4.

13
Figure 4. Overview of NH3 and odor mitigating strategy from poultry housing.

5.1 Liquid spray


The liquid spray (oil and acidic water) may be administered manually with a handheld
sprayer or mechanically with a permanently installed technology to reduce NH3 emissions.
According to Zhang et al. (1998), liquid spray (a mixture of a small quantity of plant oil with
water) has shown an NH3 reduction of 30%. Ammonia is reduced by oil spray due to the scrubbing
action of the droplets, which collect NH3 due to its high-water solubility. Ammonia absorption
into a water droplet rises as the radius and velocity of the droplet decrease (Eremin et al., 2007).
Oil spraying also coats surfaces and prevents NH3 from volatilizing into the air space above the
litter (Zhang et al., 1998). However, spraying a high dosage of acidic electrolyzed water (AEW)
may result in high amounts of NH3 emission due to an increase in LMC (Chai et al., 2017). As
LMC increases, the microbial breakdown of nitrogenous substances in the litter increases and thus
increases NH3 production from the litter (Koerkamp, 1998; Liu et al., 2007). For instance, Ogink
et al. (2012) sprayed water at 150 to 600 mL m-2 on the top layer of litter, and that reduced PM10
and PM2.5 levels by 18-64% in an aviary hen house but increased NH3 emissions by up to 65%.
Similarly, spraying 25 to 75 mL kg-1 dry litter d-1 immediately after spraying resulted in 5 to 6
times more NH3 emissions than spraying 25 mL kg-1 dry litter d-1 (Chai et al., 2017). Additionally,
spraying acidic electrolyzed water (AEW) with a pH of 7 resulted in 2 to 3 times more NH3
emission than spraying AEW with a pH of 3. Chai et al. (2017) discovered that a dose of 25 mL
AEW kg-1 dry litter d-1 at a pH of 3 could control PM levels in poultry litter by 50% without
creating extra NH3. Overall, oil and acidic water spray had shown NH3 reductions up to 30%

14
(Table 11 in the supplementary materials). Although applying a low pH liquid to the litter would
assist in NH3 reduction while decreasing PM but emits a concern about the acidic liquid's possible
corrosive effect on the housing equipment and metal facilities (Chai et al., 2018a).
5.2 Aeration and ventilation system
Aeration is a well-established method for reducing odor in animal waste storage facilities
(Ni, 2015). However, the technology's limited adoption by animal producers is partly due to its
expensive capital and operating expenses. The device aerated the top liquid in a lagoon to form an
oxygenated layer that acts as a cover, allowing odorous molecules to break down before reaching
the atmosphere, resulting in lower odor emissions. The field-scale studies evaluated the system's
efficacy and efficiency in transporting oxygen into the liquid under aeration in a swine facility
(Zhu et al., 2008). Aeration with an acid scrubber has shown 80 – 87% NH3 reduction from the
pig barn with slurry storage (Mostafa et al., 2020). Aeration with a proper ventilation system can
reduce NH3 from the barns.
The ventilation system plays a vital role in removing NH3, moisture, and PM from the
CAFOs. Early research in the United Kingdom recorded NH3 concentration in broiler houses as
high as 160 ppm and associated this with humidity and ventilation (Chai et al., 2012). The NH3
emission rate is more sensitive to the ventilation rate variation inside the house because the
ventilation rate is inversely proportional to the outside ambient temperature (Chai et al., 2012).
Ammonia concentrations in the exhaust air were considerably decreased at greater outside
temperatures and ventilation rates. Vranken et al. (2003) found that balancing the ventilation rate
with the thermal neutral zone of the animals at higher ambient temperatures can result in an 8-13
percent reduction in NH3 emissions. Ventilation systems (mechanical and natural ventilation) used
in farms help dilute NH3 and PM concentrations by delivering fresh air into the indoor environment
(Van Wicklen and Allison, 1989). Similarly, ceiling and pit ventilation used in pig-slatted floor
systems having ventilation rates of 98.3 and 11.5 m3h-1pig-1 had shown NH3 reductions by 42.6 %
(Saha et al., 2010).
5.5 Biofilter
Filtration typically occurs through dry methods (without adding water), including
diffusion, interception, impaction, electrostatic and gravitational deposition (Wood & Van Heyst,
2016). They are usually used to remove dust particles from CAFOs, while filters that utilize water
as a scrubber media may catch NH3 gas from the air in poultry houses and clean it. For many years,
water filters, also known as trickling filters, have eliminated PM, NH3, sulfur compounds, and
nitrous oxides in commercial operations (Patterson, 2005). Many NH3 nitrification bio-trickling
filters have begun to add a denitrification stage to the facility to reduce water outflow by converting
NH3 into nitrogen gas (Melse & Mosquera, 2014). Biofilters convert pollutants by driving polluted
air through a moist packing material, usually wood chips or a combination of compost and wood
chips that supports a colony of bacteria (Nicolai & Janni, 2001). Biofiltration can reduce odor and
H2S emissions by up to 95% and NH3 by 65%. (Nicolai et al., 2008). Overall, the filter and biofilter
had shown NH3 reductions from 36-97%. This mitigation strategy and demonstrations proceeded
with other items, new designs, and partial ventilation air treatment had shown high efficacy in
reducing NH3 (Lim et al., 2012), as shown in Table 12 in the supplementary materials.
5.6 Acid scrubber

15
Acid scrubbers have been utilized to reduce NH3 emissions and odor generation from
poultry and pig houses (Wood & Van Heyst, 2016). Controlling odor is becoming increasingly
vital as urbanization increases. Emission control methods usually have high porosity and a wide
specific area. Applying the acid solution on the top of litter with the exhaust air flowing either
cross-current or counter-current cause high solubility and air contact, allowing the NH3 to move
to the liquid phase. Recirculating a part of the contaminated solution while replacing the rest with
a new acid solution is standard. The contaminant's mass transfer rate is mainly determined by the
concentration gradient, contact area, and contact duration between the liquid and gas phases for
any given compound (Melse & Ogink, 2005). Spray acid wet scrubbers that are efficient in
recovering NH3 has a minimal pressure drop and are suitable for poultry operations. The average
NH3 scrubbing effectiveness was 70% in the field and 81% in a lab study (Zhao et al., n.d.). In
addition, NH3 scrubbing effectiveness of NH3 concentrations ranging from 100 to 400 ppm ranged
from 75% to 87% in the lab. However, the field's efficiency ranged from 63 to 80 %, depending
on the season. Overall, the acid scrubber showed NH3 reductions from 69-100% and odor
reduction from 26-64%, as mentioned in Table 13 in the supplementary materials.
5.7 Dietary manipulation
Diet manipulations play an essential role in NH3 production and show potential for
reducing air pollution (Xin et al., 2011). Feed additives can alter the microbiological environment
of an animal's digestive tract and the nutrition content of feces, and the gaseous emissions it
produces (Roberts et al., 2007). For example, the DDGS, fiber, or probiotics can help reduce NH3
emissions by lowering excessive nitrogen excretion or changing the pH of manure. DDGS is a by-
product of the beverage and ethanol industries that long been used in animal diets in the US,
including poultry (Xin et al., 2011). Feeding laying hens 20% or less DDGS in their meals has
been demonstrated to have no negative impact on egg production and help broilers grow faster. It
has also been proven that the inclusion of DDGS reduces the NH3 emissions from excreta (Wu-
Haan et al., 2010). Similarly, feeding chickens with 20% DDGS for 21- to 26-week-old diets
reduces 24% of daily NH3 emissions and 58% of H2S. Compared to manure from hens given the
control diet, the nutritional addition of 10 % maize DDGS, 7.3 %, WM, or 4.8 % SH reduced NH3
emissions by 50% when assessed per kilogram of manure over 7 days. The NH3 emissions rate
from manure was mainly accomplished by lowering the pH of the manure. However, the DDGS
test combined with several best management practices demonstrated decreased NH3 emissions, but
the DDGS impact alone was found not significant (Liu et al., 2019).
Decreased crude protein levels in feed, amino acid supplementation, or dietary
supplementation with DDGS and other feed additives can help minimize NH3 emissions (Xin et
al., 2011). When dietary fiber and low CP content are added to the diet, it minimizes NH3 emissions
from laying hen manure (Roberts et al., 2007). Decreases in nitrogen excretion by up to 50% were
seen when dietary protein levels were reduced from 19 to as low as 5% (Summers, 1993).
Similarly, dietary protein levels as low as 11 % compared to a standard diet (17 % protein maize
and soybean meal) resulted in up to a 40% reduction in nitrogen excretion with a minimal drop in
egg mass yield. In addition, when the dietary CP level in layer diet reduced from 17 to 13.5%, then
a 30 to 35 % drop in N output in manure and a higher dry matter content in the excreta were found
(Blair et al., 1999). Excessive high dietary protein consumption is necessary to increase the size of
the egg. However, it is worth improving the egg mass rather than maximizing it. Diet formulation
with high-fiber diets also helps to reduce NH3 emissions. Roberts et al. (2007), found that using
high-fiber components in laying hen diets reduced NH3 emission significantly, resulting in no

16
negative impact on egg production. Overall, NH3 emission reduced by applying various diet
formulations was found to be 10-50%. The effect of dietary manipulation on NH3 emissions
mitigation was summarized in Table 14 in the supplementary materials.
5.8 Manure handling strategies
5.8.1 Manure cleaning
Best management practices play an important role in reducing NH3 emissions from poultry
houses (Koerkamp et al., 1998). According to many studies, furnished cages may have better air
quality than CF housing systems (David et al., 2015; Zhao et al., 2015; Wang et al., 2019). It might
be because of the different production systems (CC, MB, HR) or different management schemes
(e.g., manure removal frequency or drying method in MB & HR housing systems), and different
manure handling practices or systems that exist in poultry facilities (Li et al., 2006). Manure
qualities and handling procedures significantly influence the generation of aerial components and
their outcome during aerial transport from barns (Xin et al., 2011). Typically, hen manure is stored
at the lower level of HR houses or collected from buildings in MB to manure storage facilities.
Furthermore, the frequency with which manure is removed from MB affects NH3 emission rates,
with semi-weekly removal releasing 74% less NH3 than daily removal. The concentrations of NH3
and its emission rates from MB house were substantially lower than HR (Liang et al., 2005b) and
CF (Wang et al., 2019). The CF housing with litter floor management considerably impacts NH3
and PM concentrations in the barns. New manure removal technologies and enhanced management
practices must be designed and implemented to decrease NH3 emissions because manure is the
primary source of NH3. The difference in manure management on NH3 emissions have clearly
shown in Table 15 in the supplementary materials.
5.8.2 Litter amendments
Bacterial fermentation produces NH3 naturally from poultry litter by converting the uric
acid present in bird excreta (Mendonca et al., 2021). The uricase enzyme regulates reaction speed,
litter pH, and the presence of water and oxygen. If manure pH is lower than 7, the ionized molecule
(ammonium) has no significant bactericidal effect (Warren, 1962). Thus, conventional litter
disinfection techniques, including lime addition, windrowing, and shallow fermentation, are less
effective. However, NH3 emission can be reduced by the application of minerals like calcium
hydroxide, aluminum sulfate, and ferrous sulfate (Moore et al., 1995; 2000). Alum
supplementation with 2% and 4% alum treatments in chicken excreta lowered pH from 8.06 to
5.27 and 3.62, respectively which reduced the NH3 emissions by 73.0 and 75.8%, respectively
(Zhang et al., 2011). In commercial broiler houses, alum treated litter (1 kg alum m-2 floor) reduced
NH3 levels by 30%. However, increasing the application rate of alum above 1 kg m-2 didn’t further
efficiency in NH3 control (Li et al., 2017) For economic consideration, it is not recommended to
over apply litter treatments. Li et al. (2017) tested three different litter amendments, i.e., ferric
sulfate, aluminum sulfate, and sodium bisulfate, to reduce NH3 emissions and found 58%, 51%,
and 48% mitigation efficiency, respectively. It is also identified that using poultry litter treatment
(a mixture of 93.2% sodium hydrogen sulfate and 6.5% sodium sulfate) could improve broilers'
health and body weight (Terzich et al., 1998). Thus, using litter amendment helps to reduce NH3
and some litter amendments have up to 99% mitigation efficiency, as shown in Table 16 (in the
supplementary materials).
5.9 Immunization and Lighting

17
Immunization: Ammonia is primarily produced by the microbial breakdown of uric acid present
in manure. Uricase and urease enzymes help decompose uric acid into NH3 (Ni, 2015). Microbial
uricase in poultry manure is a crucial target enzyme for reducing NH3 production (Visek, 1962).
The possibility of immunizing birds against the enzyme that causes NH3 gas generation has been
explored to reduce NH3 production. When birds are immunized with jack bean urease enzymes, it
secretes antibodies and passes them on to their offspring maternally (Pimentel & Cook, 1988). The
antibodies produced against jack bean urease enzymes have cross-reacted and suppressed NH3
productions with the help of gastrointestinal tract bacteria present in animals (Visek, 1962). Thus,
NH3 concentrations and urease activities are reduced in animals immunized with jack bean urease.
Immunized animals had urea-splitting activities that averaged 40% less than control in the
gastrointestinal tract content (Kornegay et al., 1965). Similarly, hens are immunized against
uricase-generated eggs containing uricase-specific egg yolk antibodies (Kim & Patterson, 2003).
Antibodies against uricase activity may be isolated from egg yolk and can be used as inhibitors.
Treatment with uricase-specific antibodies inhibited uricase-mediated nitrogen breakdown by up
to 58 %. These antibodies might be used as manure amendments or food supplements to inhibit
uric acid degradation. However, a lack of information demonstrates a direct relation between
vaccination and the impacts on gaseous NH3 emitted by poultry operations.
Light adjustment: In a series of laboratory-scale tests, the possibility of implementing ultraviolet
(UV) treatment to reduce NH3 in cattle and poultry barns was investigated, and found that
irradiation of 185 nm light significantly or entirely decreased NH3 emissions (Rockafellow et al.,
2012). Under the absence of considerable water concentrations, complete removal (> 99 percent)
of 50-10 ppm NH3 was recorded in the lab study. According to Lee et al. (2020b), NH3 reductions
varied from 2.6 – 18.7% based on relative humidity (RH) and light intensity. Maximum NH3
reductions were achieved with high light intensity, 12% RH, and increased treatment duration.
Furthermore, the combination of UV-A (black light) and a specific photocatalyst (TiO2) lowered
the concentrations of various air pollutants (e.g., CO2, N2O, O3) and NH3 emissions by 5-9% (Lee
et al., 2020a). According to Guarino et al. (2008), photocatalytic TiO2 coating reduced NH3
emissions by 30%. Moreover, photocatalysis based on TiO2 with UV-A in poultry farms has
improved indoor air quality by reducing odor, greenhouse gases (GHGs), and O3 (Lee et al.,
2020b). When light intensity and treatment duration was increased, VOCs and animal odor were
reduced by 26-62 % and 18%, respectively. Photocatalysts, relative humidity, increased light
intensity, longer treatment duration, and minimal dust formation of the photocatalyst's surface
using substantially more active dose-driven parameters have typically reduced target gasses. Thus,
light adjustment shows significant results for NH3 reductions.
6. Discussions

Ammonia is considered as a primary indirect source of N2O by the Intergovernmental Panel


on Climate Change (IPCC, 2006). The global warming potential of N2O is 265-310 times that of
CO2 for a 100-year timescale. Countries in different regions have varying attributes and regulations
on emissions control from animal housing systems. As over 60% of atmospheric NH3 are
contributed by animal productions in the North America, and thus USA and Canada governments
have sponsored several national studies on monitoring, modeling, and mitigation of NH3 emissions
from poultry and livestock housing systems in past decades (Chai et al., 2010, 2014, 2016; Ni,
2015). The poultry production is the largest single player in the US animal farming systems (i.e.,
27.5% of total animal NH3 emissions) (EPA, 2022). After rejoining the Paris Agreement in 2021,
the U.S. government plans to cut emissions by 50% or more by 2030 and sets a long-term goal of
18
net-zero emissions by no later than 2050 (Rogelj et al., 2021). To fulfill the target and goal, actions
from all the sectors in the US economy are demanded. Agriculture, among many others, is a
significant GHG contributor (11% total GHGs in the US) (EPA, 2022). The U.S. has been the
world’s largest broiler production country for years. In 2021, US produced 9.2 billion broiler
chickens together with 10-15 billion kg fresh manure, which is one of main sources of agricultural
nitrous oxide (N2O) and ammonia (NH3) (USDA, 2022). Therefore, our summarized information
regarding poultry production emissions and mitigation strategies are critical for the poultry
industry to think of net-zero emission operations in the future. Mitigating ammonia emissions can
be achieved through feed adjustment and manure management practices, which were summarized
in this study. For instance, using litter acidifiers can reduce 50-80% emissions from broiler houses
and cage-free hen litter because litter acidifiers can control litter pH level lower, which inhibits the
activities of enzyme and micrograms that favor the generation of NH3 gases. Besides, drying
manure timely can reduce NH3 emissions efficiently because high litter moisture content favors
the decomposition of manure and the conversation of manure nitrogen into NH3 gas.

Although NH3 mitigation strategies have been tested in poultry houses in different
countries, no method has been widely considered sustainable so far because most methods have
side effects. For instance, poultry litter additives (acidifiers) such as poultry litter treatment (PLT),
granular Al+ Clear (Aluminum Sulfate or Alum), and Klasp™ (Ferric Sulfate) are common
commercially available products that have shown significant mitigation efficiencies for NH3. An
inherent challenge is corrosive character (Chai et al., 2017). Due to high moisture environment,
chicken houses tend to have acidic air environment after using litter additives.

In addition, mitigation strategies could be cost prohibitive. For controlling NH3 generation
from litter in poultry houses, tons of litter additives will be used each house. The litter additive,
Poultry Litter Treatment (PLT) for instance, costs about $800 per metric ton (Chai et al., 2018a).
The operational cost (PLT + labor cost) for a commercial cage-free layer house with 50,000 hens
(litter floor areas = 2400 m2) is estimated to be $0.356 bird-1 yr-1 at the PLT application rate of 0.9
kg m-2 once a month (Chai et al., 2018a). For mitigating emissions from poultry houses to ambient,
the acid scrubber has been tested with over 80% or higher efficiency in NH3 mitigation for poultry
manure composting facility on a commercial poultry farm in Ohio, USA (Hadlocon et al., 2015).
However, the cost for installing the acid scrubber system will be US$200,000 for proceeding
manure generated by 1 million layers (US$0.2 bird-1). The annual operation and maintenance costs
are close to $150,000 (US$0.15 bird-1). The equipment (acid scrubber) requires more space/land
to install on the farm. The space/land requirement and cost of construction and operation may
prevent farms from implementing these practices. A trade-off between NH3 reduction and the
mitigation strategies should be evaluated in the future for different types of chicken productions
because mitigating NH3 emissions will increase chickens’ growing rate and egg production
efficiencies, and enhance nitrogen nutrient use efficiency for crop production, and results in lower
environmental impacts (Chai et al., 2014). Assistances should be considered by government bodies
because mitigating NH3 has long-term merits in terms of environmental footprints and nitrogen
nutrition recycling. For instance, the USDA Nature Resource and Conversation Service has been
assisting farmers in implementation of new technologies through Environmental Quality
Incentives Program (EQIP). These programs offer financial incentives and cost-share funds to
offset the costs of implementation of new equipment.

19
7. Conclusions
In this review study, we summarized the primary reasons that affect NH3 emission in
poultry houses, analyzed how high levels of NH3 may impair the health and welfare of animals
and their caretakers, and discussed the mitigation strategies that have been tested on poultry farms
in different regions and countries. Common animal production and health concerns as caused by
long term high NH3 exposure (e.g., >25 ppm) include low broiler growth rates, burning of skin
and eyes, and infections in respiratory system. In the worse situation (NH3 level ≥ 200 ppm),
animal mortality will increase. For controlling NH3 levels, various mitigation strategies, including
biochemical, chemical, managerial, physical, and physiological practices, were analyzed,
compared, and discussed. For instance, using litter additives to control NH3 is a common method
in broiler chickens’ houses, which has yet to be used in cage-free hen houses, an emerging housing
system transited from conventional cage systems due to public concern on animal freedom.
However, emission mitigation strategies could be cost-prohibitive and thus need government
assistance programs to facilitate sustainable poultry production.
Acknowledgments
This project is supported by Egg Industry Center; USDA-NIFA (2022-33610-37532); USDA-
Hatch projects: Future Challenges in Animal Production Systems: Seeking Solutions through
Focused Facilitation (GEO00895; Accession Number: 1021519) & Enhancing Poultry Production
Systems through Emerging Technologies and Husbandry Practices (GEO00894; Accession
Number: 1021518).

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