Abstract
Due to greater consumption of poultry products and an increase in exports, more poultry houses will be needed. Therefore, it is important to investigate ways that poultry facilities can coexist in close proximity to residential areas without odors and environmental challenges. Ammonia (NH3) is the greatest concern for environmental pollution from poultry production. When birds consume protein, they produce uric acid, ultimately converted to NH3 under favorable conditions. Factors that increase production include pH, temperature, moisture content, litter type, bird age, manure age, relative humidity, and ventilation rate (VR). NH3 concentration and emissions in poultry houses depend on VR; seasons also have effects on NH3 production. Modern ventilation systems can minimize NH3 in enclosed production spaces quickly but increase its emissions to the environment. NH3 adversely affects the ecosystem, environment, and health of birds and people. Less than 10 ppm is the ideal limit for exposure, but up to 25 ppm is also not harmful. NH3 can be minimized by housing type, aerobic and anaerobic conditions, manure handling practices, litter amendment, and diet manipulation without affecting performance and production. Antibiotics can minimize NH3, but consumers have concerns about health effects. Administration of probiotics seems to be a useful replacement for antibiotics. More studies have been conducted on broilers, necessitating the need to evaluate the effect of probiotics on NH3 production in conjunction with laying hen performance and egg quality. This comprehensive review focuses on research from 1950 to 2018.
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Introduction
The USA is the second largest egg producer in the world after China. According to data published by the USDA in the World Agricultural Supply and Demand Estimate (June, 2017, WASDE), total egg production in the USA was 104.988 billion (8.749 billion dozen) which was 2.1% more than 2016. According to this report, US egg production is expected to increase by 1.6% to 8.890 billion dozens in 2018. USDA also expects an increase in egg exports in 2017 and 2018. It was predicted that 302.8 million dozen (8.5% more than previous year) and 320.0 million dozen (up 5.7% from 2017) would be exported. If these trends in the US continue, more laying hens will be needed to meet the demand for eggs, prompting the need for more poultry houses. Historically, people living in close proximity to poultry houses have complained about associated foul odors. Gases such as ammonia (NH3), hydrogen sulfide, and volatile sulfur compounds are responsible for some of these complaints. Odorless methane is often associated with the volatile gases.
Presently, NH3 produced in poultry houses is a concern for the health of poultry, human, and environment. In this comprehensive review, we discuss major factors leading to formation of NH3. These factors include determinants of NH3 in poultry facilities, seasonal and geological effects, NH3 in the environment, its effects on human and poultry health, and techniques for NH3 reduction in poultry production including housing type, aerobic and anaerobic conditions, litter amendments, and diet manipulation. We conclude by discussing the most important strategies to reduce NH3 in poultry production.
Formation of NH3 in poultry
Uric acid is the major source of NH3 formation in poultry, mostly occurring in the ceca. The microbial breakdown of large amounts of uric acid in feces and urine results in urea in the presence of an enzyme, uricase, and eventually into NH3 (Almuhanna et al., 2011; Schefferle 1965; O’Dell et al. 1960; Mahimairaja et al. 1994; Whyte 1993; Kim and Patterson 2003a,b; Bachrach 1957; Moore 1998; Anderson et al. 1964; Li et al. 2013; Santoso et al. 1999; David et al. 2015; Creek and Vasaitis 1961).
The hydrolysis of urea to NH3 and carbon dioxide (CO2) by urease activity is shown in the following reaction (Figs. 1 and 2).
Formation of NH3
Probable pathway of aerobic breakdown of uric acid by the pseudomonads used (Bachrach 1957)
Bachrach (1957) showed the following schematic representation of degradation of uric acid into NH3.
The following is the overall reaction suggested by Bachrach (1957).
Bacillus pasteurii (a ureolytic bacteria that facilitates NH3 production) has no growth in acidic conditions. Thus, NH3 formation from uric acid is more favorable at a pH higher than 7 (Li et al. 2013; Elliott and Collins 1982).
Several studies have shown that NH3 formation depends on the amount of urea, urease activity, pH, temperature, relative humidity (RH) air velocity/ventilation rate (VR), manure handling practice, litter, bird age, and moisture content (MC).
Determinants of NH3 formation in poultry facilities
Table 1 is a compilation of results for effects of various determinants of NH3 production.
Results of all studies in Table 1 are in agreement with findings of Almuhanna et al. (2011), Schefferle (1965), O’Dell et al. (1960), Mahimairaja et al. (1994), Whyte (1993), Kim and Patterson (2003a), Bachrach (1957), Moore (1998), Anderson et al. (1964), Li et al. (2013), Santoso et al. (1999), David et al. (2015), and Creek and Vasaitis (1961).
For instance, a 2-year study was conducted to find the relationship between pH and NH3 volatilization. Three different diets [a control, EcoCal (natural mixture of zeolite and gypsum) and DDGS (corn-dried distiller grain with solubles)] were fed to laying hens. Results showed a direct relationship between pH and NH3 emissions. EcoCal, DDGS and the control had a pH of 8.0, 8.9, and 9.3, respectively. The acidifier (gypsum) content of EcoCal decreased the pH and ultimately less N to convert into aerial NH3. MC also had an important role in NH3 production. Based on the results of this study, it was illustrated that EcoCal had a higher MC (50.2%) than the control (46.1%) and DDGS (43.5%). As shown in Table 2, no significance difference in organic nitrogen (Org-N) and total Kjeldahl nitrogen (TKN) was recorded for all three diets while on a dry matter (DM) basis, 68% more NH3-N was measured in the EcoCal diet than in the control (Li et al. 2012).
Generally, they show the direct relationship between pH and NH3 production. pH at more than 7 is responsible for NH3 production and its volatilization from poultry manure while nitrogen (N) stays in the form of ammonium (NH4+) when pH is less than 7.
The relationship between NH3 and hydrogen ion concentration ([H+]) was elucidated by Xue et al. (1998) who trapped NH3 from manure storage facilities. Calculations showed that less [H+] produced more free NH3 as shown in the following equation. pH is the negative log of [H+]; therefore, a higher pH indicates higher free NH3 (Xue et al. 1998).
Bird age is also important in NH3 production. As the chicken’s age increase, they produce more NH3; this is clearly shown in Table 1.
Results of another study revealed the relationship between bird age and NH3 production. Laying hens of three different age groups (21-, 38-, and 59-week-old) were housed to observe the effect of bird age on NH3 volatilization. Manure from the youngest hens volatilized less NH3 as compared to other two groups (Wu-Haan et al. 2007).
VR also affects NH3 concentration and emissions. Various studies reported a positive relationship between VR and emissions while an inverse relationship was reported for concentration and VR. This means that NH3 emissions increases with the increase of VR in summer and vice versa in winter. Ultimately, greater water content is associated with more NH3 production.
Seasonal and geological effects
It has been reported that NH3 production also depends on seasons and geological sites. Weather and temperature cause various seasons and seasonality affects volatilization. Eighteen consecutive flocks of broilers were studied for seasonal effects. These birds were observed until 40–42 days of age and consumed a commercial diet. Significant difference in volatilization for winter and summer were observed as shown in Table 3 (Coufal et al. 2006).
The dependence of NH3 reduction on seasons was observed in a 2-year study. NH3 volatilization by the EcoCal diet varied from − 7.1% in September 2008 to 72.2% in February 2009 while it varied from 16.3% in September 2008 to 51.0% in October 2009 with the DDGS diet. More (p < 0.01) NH3 concentration was found in winter than in summer (Li et al. 2012).
NH3 in the environment
Adverse effects of NH3 on environment; ecosystem; and health of humans, animals, and birds were revealed in many studies. Environmental groups/agencies have also pressured producers to lower NH3 emissions (Li et al. 2013; Liang et al. 2005).
NH3 is a precursor of secondary particulate matter (PM2.5) and contributes to the production of PM2.5 (Xin et al. 2011; Baek and Aneja 2004). It produces these particles when combined with oxides of N and sulfur. These very small particles affect human health as discussed below (NH3 effects on human health). As well as producing PM2.5, atmospheric NH3 can alter oxidation rates in clouds and can also elevate acid rain production (Xin et al. 2011; Baek and Aneja 2004; Baek et al. 2004; van Breemen et al. 1982; ApSimon et al. 1987; Sharma et al. 2007).
NH3 contributes to acidification in soil and N deposition in ecosystem (Li et al. 2013; Liang et al. 2005; Jones et al. 2013). Moreover, nitrifying bacteria in the soil convert it into nitrates which lower pH of ground water and increase concentrations of nitrates in drinking water (Santoso et al. 1999; Adams et al. 1994). Van Breemen, 1988 and Angus et al. (2003) reported N contribution in eutrophication, acidification, and nitrification of groundwater and leaching.
NH3 effects on human health
NH3 is a known irritant of the mucous membranes in the upper respiratory tract, nose, and eyes (Santoso et al. 1999; Ihrig et al. 2006; Almuhanna et al. 2011; Pratt et al., 1998); thus, it can damage the respiratory system of workers (Fig. 3) at all levels (Nararaja et al. 1983; Whyte 1993; Charles and Payne 1966). This was confirmed in an epidemiological study by Hartung (2005).
Effects on respiratory system (http://hotnewsnaija.ng/wp-content/uploads/2016/10/Respiratory.png)
As mentioned above, NH3 is responsible for the production of PM2.5 which can penetrate deeper into the respiratory system of humans and animals where they damage tissues. Birds (feather and skin dander), feed particles, litter, and feces can also be responsible for production of different sizes of inhalable PM2.5. Higher concentrations of NH3 in air affect the respiratory system of humans while cough, nose, and throat irritation can also be caused by lower concentrations. Sundblad et al. (2004) also found increased symptoms of irritation and central nervous system effects upon NH3 exposure. Poultry workers are adversely affected by NH3 as compared to non-poultry workers; this is supported by many epidemiological studies. Workers exposed to NH3 in poultry confinements experienced burning and watery eyes, sneezing, stuffy and running noses, and also coughs (Sanderson et al. 1995; Rees et al. 1998).
Respiratory symptoms during and after work in poultry houses has increased in recent years. All studies showed acute and chronic effects on poultry workers’ health (Kirychuk et al. 2003; Zuskin et al. 1995; Reynolds et al. 1993; Santoso et al. 1999; Close et al. 1980; Morris et al. 1991). It was also reported that respiratory symptoms were greater in winter months and pulmonary function also decreased the number of work days (Reynolds et al. 1993). Extensiveness of chronic cough, chronic phlegm, chronic bronchitis, and chest tightness were higher in poultry workers and chicken catchers than the control and non-exposed blue-collar workers (Zuskin et al. 1995; Morris et al. 1991). A recent study revealed that a water-based sprinkler cooling system did not reduce NH3 concentration nor did it improve worker health (Ischer et al. 2017).
NH3 effects on the health of poultry
Almuhanna et al. (2011) reported that NH3 is the most abundant toxic gas in poultry houses (Fig. 4).
Measured concentration of toxic gases (NH3, SO2, NO2, H2S) (Almuhanna et al. 2011)
NH3 is a colorless gas with a characteristic pungent smell. It is the most common, noxious, and highly water-soluble gas. NH3 is alkaline and corrosive, adversely affecting the chicken’s nasal cavity and eyes. It reacts with nasal moisture to produce the corrosive effect shown below.
As shown in the equation, the NH4+ solution formed corrodes the respiratory system of chicken and consequently results in paralyzed or lost cilia. Mucus on the mucosal surface of the trachea becomes unclear due to corrosion of cilia which leads trapped bacteria to air sacs and lungs and ultimately causes infection (Aziz and Barnes 2010; Maliselo and Nkonde, 2015; Quarles and Kling 1974; Anderson et al. 1964; Oyetunde et al. 1978; David et al. 2015; Nararaja et al. 1983). Contradictory results were reported by Al-Mashhandani and Beck (1985) who noted no observable effects of NH3 on the appearance of lungs and trachea. As shown in Fig. 5, production of NH3 also affects both the performance and health of birds by preventing mobility.
Different levels of NH3 affect birds’ health and performance as shown in Table 4.
Beker et al. (2004) mentioned that no significant differences were recorded in final body weight, body weight gain, and feed consumption when 1-day-old broiler chicks were exposed to 0, 30, and 60 ppm NH3 concentrations. In addition, or perhaps related to health, Yi et al. (2016b) found insignificant differences in average daily gain, average daily feed intake, and feed conversion ratio when chicken were exposed to 3 and 25 ppm NH3. No significant differences in feed conversion and mortality with 25 and 50 ppm NH3 exposure were reported by Reece et al. (1981). Average body weight, air sac scores, lung weights, and Bursa of Fabricius did not differ significantly in ammoniated birds when compared to the control (Caveny et al. 1981).
Many experiments on the effects of NH3 on birds’ health were conducted in the middle of twentieth century and continue. While reviewing the literature, it was difficult to discern the meaning of low, medium, and high because actual quantities in ppm were not provided.
Generally, recommendation of NH3 concentration in poultry houses is less than 25 ppm. Ideally, NH3 exposure should be less than 10 ppm but temporarily exceeding the limit to 25 ppm is not harmful (NOISH, 2016; Animal Husbandry Guidelines for US Egg Laying Flocks, 2010; Miles et al. 2006; Kristensen et al. 2000). According to the Occupational Safety and Health Administration (Aziz and Barnes 2010), 50 ppm for 8-h exposure is the recommended concentration of NH3 in a poultry house or OSHA has recommended no more than 35 mg/m3 for 8-h daily exposure (EPA 2016). It is the lowest concentration which can irritate eyes, nose, and throat.
Techniques for NH3 reduction in poultry production
Modern ventilation systems in the poultry houses can reduce NH3 concentration quickly but also increase its emissions in the atmosphere simultaneously. Poultry health is improved by exhausting NH3 to the outside; however, exhausted NH3 affects the surrounding environment and, ultimately, the ecosystem. Therefore, actions are necessary to control both concentration and emissions of this toxic gas. A review of the literature discusses many techniques to reduce N production and consequently, NH3.
Mitigation, without affecting birds’ production performance, includes housing type (Fig. 6a–j), bird age, manure age or handling practices, building VR, and diets [low crude protein (CP), synthetic amino acids, addition of fiber, and use of probiotics]. These strategies are discussed below.
a Cross section of high-rise (https://www.researchgate.net/figure/221971812_fig2_Figure-2-Cross-section-view-of-the-monitored-high-rise-laying-hen-houses-and-sampling). b Manure-belt (https://www.alibaba.com/product-detail/poutry-Manure-belt-conveyor-belt-for_60499340942.html). c Cross section of manure-belt (https://www.researchgate.net/figure/274345115_fig1_Figure-1-Cross-section-of-the-aviary-hen-house-one-side-of-the-double-house-monitored). d Deep-pit (http://www.thepoultrysite.com/poultrynews/37795/midwest-deep-pit-layer-house/). e Cage free (https://lpelc.exposure.co/layer-chicken-housing-and-manure-management, http://www.onegreenplanet.org/animalsandnature/think-you-know-free-range-and-cage-free-chicken-think-again/). f Stilt house (https://www.pinterest.com/pin/368521181983914852). g Conventional cage (http://www.thepoultrysite.com/articles/3543/the-laying-hen-housing-research-project/). h Enriched colony (http://www.thepoultrysite.com/articles/3543/the-laying-hen-housing-research-project/). i Aviary house (http://www.thepoultrysite.com/articles/3543/the-laying-hen-housing-research-project/). j Broiler house (https://www.wright.ie/case-study/modern-poultry-house-facility-broiler-house-co-monaghan/)
Housing type
There are two common house styles - [high-rise (HR) (Fig. 6a) and manure-belt (MB) (Fig. 6b, c)] in the US egg industry. Manure is removed once a year in HR while in MB, it is removed two to seven times per week. A study was conducted to measure the concentration and emissions rate in both house styles. Commercial layer houses in Iowa and Pennsylvania were used in this study. After 1 year, it was concluded that MB significantly lowered both NH3 concentration and its emission rate as compared to HR. In addition, a comparison between daily and semi-weekly removal was made. Daily removal showed 74% less NH3 emission rate in comparison to semi-weekly (Liang et al. 2005). Findings from Green et al. (2009), Koerkamp (1994), Li and Xin (2010), Ni et al. (2012, 2017a), Keener et al. (2002), Roumeliotis and Van Heyst (2008), and Mendes (2010) also support these results. Appropriate temperature and NH3 levels were found both in HR and MB in winter while in summer, no difference was observed in NH3 level in all house types. House temperature was slightly, though not significantly, higher than the ambient temperature (Liang et al. 2005).
A review conducted by Xin et al. (2011) also reported less NH3 release from MB houses due to less surface area and less MC.
Green et al. (2009) conducted a field study to determine the best housing type for reduction of NH3. Cage-free floor-raised (FR) (Fig. 6e), HR (Fig. 6a), and MB (Fig. 6b, c) were used in this study. Results illustrated that NH3 emissions was higher in FR (46 ppm) than HR (14 ppm) and MB (7 ppm). Similar findings were noted by Nimmermark et al. (2009), Koerkamp and Bleijenberg (1998), and Costa et al. (2012).
Three houses were used to accommodate laying hens by Nicholson et al. (2004). One of three houses had a belt-scraped design (Fig. 6b, c). Deep-pit (Fig. 6d) and stilt designs (Fig. 6f) were used for the second and third houses, respectively. Daily removal of manure for the belt-scraped design reduced NH3 more than 2× when compared to weekly removal; these results were confirmed by Koerkamp et al. (1996). In the deep-pit house, more NH3 was volatilized than in the belt-scraped and stilt houses. Koerkamp et al. (1996) and Keener et al. (2002) also reported comparable findings. Additionally, Fournel et al. (2012) reported lower NH3 concentration and emissions from manure for the belt-scraped design than for the HR house (Nicholson et al. 2004; Zhao et al. 2013; Fabbri et al. 2007).
The effect of housing type on NH3 emission rate (ER) was observed in the study of Shepherd et al. (2015). Three different houses [conventional cage (CC) (Fig. 6g), enriched colony (EC) (Fig. 6h), and aviary house (AV) (Fig. 6i)] were used to monitor gas volatilization. The results indicated that NH3 in CC and EC was significantly less compared to AV.
Housing type with other factors
Nicholson et al. (2004) conducted a study to find the relationship between manure handling practices and NH3 volatilization in both broiler and laying hen houses. It was reported that NH3 emissions was greatly influenced by housing type, manure removal, drinker (Fig. 7a, b), and litter type. Housing type and land spreading are the most important factors in NH3 losses. In broiler houses, two different types of litter (straw and wood shaving) were used. There was no difference in NH3 losses in summer from both types of litter, and similar findings were also discussed by Elwinger and Svensson (1996) and Tasistro et al. (2007). Moreover, it was mentioned that houses with bell drinkers emitted more NH3 (numerically) than houses having nipple drinkers, and these results were also similar to that of Elwinger and Svensson (1996) and Da Borso and Chiumenti (1999). It was reported that most of the gas lost occurred during transportation, but no differences were recorded during storage and land spreading.
a Bell drinker (http://www.wesstron.pl/drob.php?lang=en&id_strony=82). b Nipple drinker (https://www.indiamart.com/proddetail/poultry-nipple-drinker-system-)
Aerobic and anaerobic conditions
Mahimairaja et al. (1994) performed an experiment to investigate the effect of four carbon-rich bedding materials, one acidifying material, and two adsorbents on N transformation and its loss in poultry manure under aerobic and anaerobic conditions. Anaerobic conditions showed a significant reduction in NH3 volatilization in comparison to the aerobic environment after 12-week incubation period of poultry manure (Table 5). Bachrach (1957) also discussed the similar results.
Findings for NH3 production in aerobic and anaerobic environments were also supported by Kirchmann and Witter (1989). A study was conducted on fresh chicken manure combined with oat straw for both aerobic and anaerobic conditions. Less NH3 was volatized in an anaerobic condition due to low pH; possibly NH3 losses to some extent, were dependent on quantity of straw present in aerobic condition but no effect was observed in an anaerobic environment. Significantly higher NH3 volatilization in aerobic versus anaerobic decomposition was also reported by Kirchmann and Lundvall (1998).
Litter amendments
A review of several studies reported that NH3 emissions can be minimized by litter amendment. It was helpful in all poultry houses, especially in laying hen facilities (Roumeliotis and Van Heyst 2008). As shown in Table 6, significant effects of litter amendments on NH3 reduction were observed.
In addition to the negative effect of acidic electrolyzed water, several studies showed that litter amendment was the best way to control NH3 concentration and emissions. Different types of adsorbents, inhibitors, and bedding materials were applied in poultry houses. Alum and zeolite were used most commonly. When these materials were added to the litter, they lowered pH and produced more NH4+ rather than NH3. Some inhibitors reduced urease activity, responsible for NH3 production.
Uricase-specific antibody (IgY) from hens immunized with uricase by triplicate injections suppressed microbial uricase activity (Kim and Patterson, 2003b). The investigators suggested that more work was needed to ascertain the effect of the uricase-specific IgY on microbial uricase, possibly reducing NH3 volatilization from poultry manure. In contrast to results of Nakaue et al. (1981), no effect of clinoptilolite (zeolite) on ammonia reduction was observed when laying hens were fed in a 28-day study (Nakaue and Koelliker 1981). Litter amendment does not commonly affect birds' performance and production. Ali et al. (2000) reported contradictory results indicating that alum affected broilers performance.
Figure 8a–c shows the different types of litter amendments in poultry houses.
a Litter amendment with gypsum (https://www.usagypsum.com/gypsum-products/gypsum-poultry-litter-amendment). b Litter amendment with pine shaving (http://www.thepoultrysite.com/articles/3554/alternatives-to-pine-shavings-for-poultry-bedding/). c Litter amendment with wood shaving and poultry additive, zeotec (https://www.bpmnz.co.nz/en/products/zeotec/)
Diet manipulation
Several studies showed that NH3 production can be decreased by diet manipulation (Hale 2005; Roberts et al. 2015). Positive results without affecting birds’ performance and production were obtained in most of them.
Low crude protein
High protein in the diet of layers is mainly responsible for elevated production of NH3. Poultry cannot store excess amino acids, resulting in released N, mostly in the form of uric acid (Kristjan and Roberts 2006).
Liang et al. (2005) explained the influence of reduced CP on NH3 emissions. Birds were fed a diet containing 1% low CP and essential amino acid supplements. There was significantly lower NH3 concentration and its emissions was low in houses with low CP. Liang et al. (2003), Gates (2000), Ji et al. (2014), Meluzzi et al. (2001), and Nahm (2007) found similar results. Contradictory findings were shown in the study of Burley (2009).
Results of another study revealed that by adding low CP (and lysine), NH3 gas concentration decreased by 31% and litter N by 16.5% (DM basis) as shown in Table 7. Broilers were fed with three different diets: high CP (High), low CP with additional synthetic amino acids (Low), and an equal blend (1:1) of High and Low CP treatments (Medium). Low CP reduced NH3 and litter N by lowing pH and MC (Ferguson et al. 1998). Similar results were obtained in studies by Blair et al. (1999), Gates et al. (2000), and Namroud et al. (2008).
Direct relationships between dietary protein and NH3 emissions, litter N, or total N were found in several other studies. Results showed that these factors increased with the increase of CP (Elwinger and Svensson 1996; Summers 1993; Keshavarz and Austic 2004; Robertson et al. 2002; Aletor et al. 2000; Rezaei et al. 2004).
The effects of dietary protein were also observed in laying hen houses. A 2-year study was conducted using three commercial HR houses (Fig. 6a). Three different diets included a control, 7% EcoCal, and DDGS. Results showed that Ecocal and DDGS significantly lowered NH3 volatilization compared to a control diet. EcoCal and DDGS had 39.2% and 14.3% less NH3 emissions, respectively. Manure obtained from the EcoCal diet had higher NH3-N retention (68%) than the control. NH3 emission rates are shown in Table 8 (Li et al. 2012). The findings of Roberts (2009) showed contrasting results for DDGS.
Wu-Haan et al. (2007) confirmed findings of others when two different diets were fed to three different age groups of hens. Diets were a reduced-emission (RE) diet, containing a mixture of 6.9% of CaSO4-zeolite and slightly reduced CP and a commercial diet (CM). Laying hens (21-, 38-, and 59-week-old) were used in this study. Significant reduction (p < 0.01) in NH3 emissions was observed when hens were fed the RE diet. Other investigators reported similar findings (Romero et al. 2012; Xin et al. 2005; Cabuk et al. 2004, Wu-Haan 2006). Lon-Wo (2010) also reported less NH3 volatilization when hens were fed a diet containing 3% natural zeolite (Clinoptilolite) instead of a control diet. After 10 days, NH3 emissions from manure of hens fed zeolite was only 30.6 ppm while 937 ppm NH3 emissions was reported for the control (Nakaue et al. 1981; Hale 2005).
Findings of Nakaue and Koelliker (1981) and Karamanlis et al. (2008) were not in agreement with the results discussed above. Ferguson et al. (1998) also reported an insignificant effect of dietary protein on NH3 gas emissions, MC, and pH; but, litter N was lowered significantly by adding low CP and P in a broiler diet. Results also showed that gaseous NH3 production was inversely proportional to dietary P, and this relationship was previously explained by Taraba et al. (1980) as well. Based on the results, it was suggested that NH3 concentration depended on pH and litter surface moisture which were not sensitive response variables as compared to chemical analyses (Ferguson et al. 1998; Taraba et al. 1980). Analysis by Burley et al. (2013) showed no significant difference in NH3 emissions when laying hens were fed diets containing different levels [low, intermediate, and high (control)] of CP.
Fiber
According to Roberts et al. (2007b), NH3 emissions can be diminished by feeding a fibrous diet because (1) amino acids in ingredients of a highly fibrous diet are less digestible as compared to that of those in a low fibrous diet and (2) amino acids in a fibrous diet are not available to degrade to urea and consequently to NH3. Additionally, investigators stated that fermentable fiber can change the form of N excretion from urea (urine) to microbial protein (feces). Microbial protein is more stable and less degradable to NH3. Fiber also helps in minimizing pH of the manure by production of volatile fatty acids. This is important because low pH retards production of NH3 and produces more NH4+ ions which are not volatile (Roberts et al. 2006, 2015).
Roberts et al. (2006) also reported that hens digest less fiber, so diets with high fiber decrease protein digestibility and increase excretion of N (Fig. 9). In this study, three types of fiber (soy hulls, wheat middlings, and DDGS) were added to the diet. Inclusion rate for DDGS was 10% and wheat middlings were also included to obtain the same neutral detergent fiber. Researchers found no difference in N excretion both in the control and the diet with fiber. Wheat middlings caused a significant reduction in uric acid excretion which is the main source of NH3 production in birds. pH is also important in NH3 production, and addition of fiber decreased pH of the manure without affecting hen production performance. Reduced uric acid and decreased pH were factors in minimizing NH3 volatilization (Pineda et al. 2008).
Total ammonia emission from manure over 7 days. Data are means ± pooled SEM, n = 6. *Different from control (p < 0.05) (Roberts et al. 2006)
Roberts et al. (2007a) also supported findings in Fig. 10. This study was conducted with 17-week-old laying hens. Hens were fed eight different diets [normal crude protein = corn and soybean meal control diet, control with 10% DDGS, 7.3% wheat middlings (WM), and 4.8% soybean hulls (SH); reduced CP = corn and soybean meal control diet, control with 10% DDGS, 7.3% wheat middlings (WM), and 4.8% soybean hulls (SH)] . Addition of higher fibers lowered NH3 emissions from manure over 7 days in comparison to the control. Reduced CP by 1% did not lower NH3 emissions as supported by results from previous studies with reduced CP (Bregendahl et al. 2002; Roberts et al. 2007b; Bregendahl and Roberts 2007).
Ammonia emission rate from manure. Data are means ± pooled SEM, n = 6 (Roberts et al. 2006)
One possible high fiber dietary addition for reduction of NH3 is meal made from sunflower seed, a globally grown oil crop having high fiber and fat. Meal is the by-product of seed processing (with or with part of the hull) left after oil extraction and could be an important protein source in animal diets (Kalmendal et al. 2011; Laudadio et al. 2014; Selvaraj and Purushothaman 2004, Ditta and King, 2017). Although it provides very low utilizable carbohydrate and low lysine, 25% sunflower seed meal (SFM) could be used in a balanced diet without affecting weight gain or feed efficiency of growing chicks (Rodriguez et al. 1998). It contains linoleic acid which is a fat source for laying hens (San Juan and Villamide 2001). Abdelrahman and Saleh 2007 reported that SFM can be effectively used rather than soybean meal. It contains about the same average CP (30–32%), a higher quantity of methionine, and less lysine as compared to soybean meal. SFM (10%) could be used to improve average body weight and lessen feed cost for production. Another advantage of SFM is that it is free of most antinutritional factors (Senkoylu and Dale 1999; Deaton et al. 1979; Rose et al. 1972; Walter et al. 1959; Villamide and San Juan 1998).
Bamboo charcoal
Maliselo and Nkonde (2015) recommended the use of bamboo charcoal particles in diet manipulation to minimize NH3 emissions. These results indicated that bamboo charcoal had adsorption properties to bind NH3.
Probiotics
Along with decreasing CP, feeding essential synthetic amino acids, and adding fiber to reduce N excretion, use of antibiotics also created positive results; but, consumers have concerns as antibiotics are deposited in eggs and thereby, may cause antibiotic resistance in humans. Odors may be decreased by administration of live microorganisms (probiotics), which are non-pathogenic and non-toxic. They help hosts maintain health by (1) fortifying the digestive system and (2) lowering NH3 concentration by competitive exclusion of other bacteria.
Several studies have been conducted to analyze the effect of probiotics on humans. Along with humans, many investigations were conducted to reduce NH3 production without affecting birds' health and performance.
Probiotic (Lactobacillus casei) suppressed NH3 production in the GI tract of broiler chicken in a 6-week study. Lactobacillus casei at 0.1%, chloroxytetracycline (antibiotic) at 0.1%, and yucca extract at 0.2% were added in the diet. Two-day-old broiler chicks were randomly assigned to a control and treated diets. Diets containing probiotic showed significant effects on feed intake and weight gain. Urease activity also decreased in the GI tract of broilers which were fed the diet containing probiotic. These findings concluded that dietary probiotic restrained bacterial growth which was responsible for urease activity and, ultimately, NH3 production (Yeo and Kim 1997). Isshiki (1979) also found positive effects of dietary Lactobacillus casei on reduction of non-protein N and urea N which resulted in decreased uric acid and NH3 level (Isshiki 1979).
Environmental NH3 levels in the broiler house were decreased by feeding a lactobacilli probiotic (ecozyme). Two experiments were conducted on 56-day-old-male broilers. Probiotic contained Lactobacilli ecozyme with a minimum of 6.0 CFU per gram of the product in experiment 1 while 3.0 CFU per gram of the product was added in experiment 2. Birds in one treatment were fed a control diet without any probiotic while birds in the other treatment were fed a control diet containing 5% ecozyme. There was a significant difference in NH3 concentration between two treatments after week 3 (Fig. 11).
Environment ammonia concentration of broiler room as affected by ecozyme diet supplementation. Exp. 1: log 6 Lactobacilli cfu/g feed; exp. 2: log 3 Bactobacilli cfu/g feed (Chang and Chen 2003)
Statistically similar results were obtained by feeding ecozyme with 3.0 CFU/g. Earlier studies illustrated that NH3 production depended on pH and MC, so lower pH and lower MC in both experiments were observed in the fecal matter of treated birds (Chang and Chen 2003).
Ahmed et al. (2014) also conducted a study to analyze the effect of dietary probiotics (Bacillus amyloliquefaciens, BAP) on NH3 production. Four hundred 1-day-old male broiler chicks were fed with commercial broiler feed containing five different levels of BAP (0, 1, 5, 10, and 20 g/kg of BAP). Table 9 shows the relationship between different levels of BAP and NH3 volatilization. Higher NH3 emissions from the control at all the incubation times were recorded. It was also observed that NH3 volatilization reduced as the probiotic level (20 g/kg of BAP) was increased. BAP lowered the pH and ultimately NH3 volatilization (Ahmed et al. 2014).
Santoso et al. (1999) conducted two experiments on 65-week-old Hyline W36 and 2-week-old broiler chicks to determine the effect of dried Bacillus subtilis culture (DBSC) on body weight, feed intake, protein intake, feed conversion ratio, NH3 gas, total N, urate N, NH3-N, N utilization, and serum urea-N. It was reported that DBSC significantly decreased NH3 gas without affecting chicken body weight, feed intake, and egg production. It was also observed that DBSC did not decrease total N in feces. Possibly, DBSC produced subtilin which helped to inhibit urease producing microflora in the gastrointestinal lumen and eventually NH3. DBSC also produced a substance which helped to reduce NH3 gas by binding N present in the feces.
The above findings were also supported by the results of Tanaka and Santoso (2000) in a 3-week study. Seven-day-old female broiler chicks were fed different levels of fermented product from Bacillus subtilis. A significant decrease in NH3 production was recorded in treated chicks when compared to the control; but, there was no difference in total N, urate N, NH3-N in fecal matter, pH, and NH3-N of cecum in both groups of chicks.
Dried Bacillus subtilis natto reduced NH3 level in chicken blood when it was fed at different levels in two experiments. Diets having 0, 0.5, 1, and 3% levels of Bacillus subtilis natto were fed to White Leghorn chickens for 3 days in experiment 1 and 0, 0.2, 0.5, and 1% levels were fed for 28 days in experiment 2. It was reported that 0.5% dietary Bacillus subtilis natto depressed the NH3 concentration in chicken blood in experiment 1 and in all levels in experiment 2. It was concluded that Bacillus subtilis natto restrained the growth of urease-producing bacteria and consequently NH3 concentration (Samanya and Yamauchi 2002).
Hmani et al. (2017) reported less NH3 production when Bacillus subtilis HB2 was fed to chicken. Bacillus subtilis UBT-MO2 was found to be effective in decreasing NH3 emissions in broiler fecal matter. Mixed sex broilers were fed two levels of enramycin (0 or 5 ppm) and Bacillus subtilis (0 or 105 cfu/kg). The NH3 gas was significantly (p = 0.03) lowered in broilers fed diets containing Bacillus subtilis in contrast to that for bird sans Bacillus subtilis. Enramycin or Bacillus subtilis did not impact Escherichia coli and Lactobacillus in ceca and small intestine. Bacillus subtilis showed more effective results when added alone as shown in Table 10 (Zhang et al. 2013).
Zhang and Kim (2013) reported less NH3 emissions when 40-week-old laying hens were fed a diet supplemented with 0.01% probiotic (Enterococcus faecium DSM 7134). It was reported that probiotic improved intestinal microbial balance of treated hens and ultimately less NH3 volatilization. Excreta of probiotic treated hens had more lactobacillus counts and less Escherichia coli counts in comparison to that of hens fed no probiotics.
According to the literature, multistrain probiotics provided better results and improved functionality when compared to monostrain (Timmerman et al. 2004; Chapman et al. 2011). Yoon et al. (2004) reported the effect of multiple probiotics on NH3 gas emissions in broiler chicks. One-day-old male broiler chicks were fed with two levels of diets containing probiotics (0 and 0.2%) and three levels of drinking water containing probiotics (0, 0.01, and 0.1%). Drinking water with a 0.1% level significantly decreased NH3 gas volatilization from broiler fecal matter in contrast to the 0% level. Overall, it was noticed that dietary probiotics reduced this noxious gas emissions from fecal matter. In a similar manner, Hassan and Ryu (2012) illustrated the effect of multiprobiotics [Lactobacillus plantarum (5 × 107 cfu/g), Saccharomyces cerevisiae (6 × 107 cfu/g), and Bacillus subtillis (2 × 107 cfu/g)] on NH3 gas emissions. The work of Chiang and Hsieh (1995) supported these findings. There was no indication in reduction of malodor by their results, but NH3 level in fecal matter was lowered by feeding probiotics containing Lactobacillus acidophilus, Streptococcus faecium, and Bacillus subtilits. The effect of dietary probiotics on NH3 emissions was also observed when broilers were fed Bacillus subtilis and Lactobacillus acidophilus versus the control and antibiotics. NH3 emissions was measured after feeding probiotics and antibiotics for 15 and 35 days. The results showed significant difference in NH3 reduction in fecal matter of broilers fed probiotics after 15 and 35 days as compared to the control plus antibiotics. Malodor in probiotic fecal matter was detected as lighter than the control and antibiotics. The findings of this study proved the importance of probiotics’ use in NH3 reduction (Chen et al. 2012).
Zhang and Kim (2014) conducted a study to examine the effects of multistrain probiotics on excreta odor for broilers. Lactobacillus acidophilus, Bacillus subtilis, and Clostridium butyricum were added in the control diet with different levels [control diet + 1 × 105 cfu of multistrain probiotics/kg of diet (P1) and control diet + 2 × 105 cfu of multistrain probiotics/kg of diet (P2)]. In another treatment, antibiotic avilamycin (5 mg/kg of avilamycin) was added to the control diet. P2 significantly lowered NH3 concentration in contrast to all other treatments. P1 also decreased NH3 concentration as compared to the control. At days 3 and 5, both P1 and P2 reduced NH3 production in broiler fecal matter over that for the control as shown in Table 11.
Results from Hossain et al. (2015) supported the above findings when tri-strain probiotics (TSP, Bacillus subtilis, Clostridium butyricum, and Lactobacillus acidophilus) were fed to chicken. DM and N digestibility were improved by feeding TSP which led to less NH3volatilization.
In 1999, probiotic consisting of Bacillus, Lactobacillus, Streptococcus, Clostridium, Saccharomyces, and Candida species were fed to both male and female broilers to analyze their effect on caecal flora and metabolites, lipid metabolism, meat components, productivity, and raising environment. In the probiotic group, NH3 in the cecum was significantly (p < 0.05) lower than that for the control group. Additionally, it was reported that pH in cecum was decreased significantly in the probiotic group which was responsible for NH3 production according to earlier studies (Endo and Nakano 1999).
Conclusion
The following are the most important strategies used to reduce NH3 production in poultry houses (Table 12).
NH3 is the most noxious gas in poultry houses needing control. pH, moisture content, litter, bird age, manure age, relative humidity, ventilation rate, and temperature play important roles in NH3 production. Seasonality and geological sites are also responsible for its production.
Housing type, manure handling practices, aerobic and anaerobic conditions, and litter amendment are postdigestive strategies. Dietary manipulation for reduction of NH3 uses low crude protein, synthetic amino acids, supplementation of fiber, and probiotics (single and multistrains).
Many studies have been conducted to evaluate the effect of probiotics on broilers and less with laying hens. More laying hens are needed to fulfill the demand for eggs; therefore, there will be more malodor and environmental pollution produced by NH3. One possibility includes use of a combination of strategies for reducing NH3 in layer house. Researchers need to conduct studies on laying hens to minimize the NH3 production and emissions in poultry houses to protect animal and human health and also to protect the environment from its harmful effects.
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Naseem, S., King, A.J. Ammonia production in poultry houses can affect health of humans, birds, and the environment—techniques for its reduction during poultry production. Environ Sci Pollut Res 25, 15269–15293 (2018). https://doi.org/10.1007/s11356-018-2018-y
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DOI: https://doi.org/10.1007/s11356-018-2018-y