Environment International 107 (2017) 111–130

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Environment International
journal homepage: www.elsevier.com/locate/envint

Review article

Environmental and human health challenges of industrial livestock and MARK

poultry farming in China and their mitigation
Yuanan Hua, Hefa Chengb,⁎, Shu Taob
a
School of Water Resources and Environment, China University of Geosciences (Beijing), Beijing 100083, China
b
MOE Key Laboratory for Earth Surface Processes, College of Urban and Environmental Sciences, Peking University, Beijing 100871, China

A R T I C L E I N F O A B S T R A C T

Keywords: Driven by the growing demand for food products of animal origin, industrial livestock and poultry production
Concentrated animal feeding operations has become increasingly popular and is on the track of becoming an important source of environmental pollution
(CAFOs) in China. Although concentrated animal feeding operations (CAFOs) have higher production efficiency and
Environmental pollution profitability with less resource consumption compared to the traditional family-based and “free range” farming,
Human health risk
they bring significant environmental pollution concerns and pose public health risks. Gaseous pollutants and
Manure disposal
bioaerosols are emitted directly from CAFOs, which have health implications on animal producers and neigh-
Sustainable animal farming
Healthy diets boring communities. A range of pollutants are excreted with the animal waste, including nutrients, pathogens,
natural and synthetic hormones, veterinary antimicrobials, and heavy metals, which can enter local farmland
soils, surface water, and groundwater, during the storage and disposal of animal waste, and pose direct and
indirect human health risks. The extensive use of antimicrobials in CAFOs also contributes to the global public
health concern of antimicrobial resistance (AMR). Efforts on treating the large volumes of manure generated in
CAFOs should be enhanced (e.g., by biogas digesters and integrated farm systems) to minimize their impacts on
the environment and human health. Furthermore, the use of veterinary drugs and feed additives in industrial
livestock and poultry farming should be controlled, which will not only make the animal food products much
safer to the consumers, but also render the manure more benign for treatment and disposal on farmlands. While
improving the sustainability of animal farming, China also needs to promote healthy food consumption, which
not only improves public health from avoiding high-meat diets, but also slows down the expansion of industrial
animal farming, and thus reduces the associated environmental and public health risks.

1. Introduction
Important changes in the food consumption of over 1.3 billion
people in China have taken place over the past three decades, and the
demands for foods of animal origin, including milk and dairy products,
aquatic products, and poultry eggs and meats, have experienced high
rates of growth. As shown on Fig. S1, the per capita consumption of
meat (pork, beef, and mutton) and poultry increased from 22.5 and
12.0 kg/year to 34.7 and 19.6 kg/year for urban and rural populations,
respectively, while that of aquatic products, eggs, milk, and dairy
products had more than tripled over the period of 1985 to 2009 (Zhou
et al., 2012). The fast growth in consumption of dietary animal protein
has been driven by the sustained urbanization and rising disposal in-
come in China, and similar shift from plant- to animal-based foods with
socioeconomic development has been well observed globally (FAO,
2012).
Driven by the growing demands, production of foods of animal
origin in China has been expanding significantly over the past several
decades. Fig. 1 depicts the growth in the country's production of major
animal food products between 1980 and 2015. The production of pork,
poultry meat, beef, mutton, milk, and poultry eggs increased by 3.1,
10.2, 11.9, 7.1, 13.0, and 5.4 times over the period of 1996 and 2015.
Pork is the most important type of meat products consumed in China
(> 60%), followed by poultry meat (> 20%). Along with the fast in-
crease in the supply of animal food products, the production model of
livestock and poultry has undergone significant changes to increase the
capacity and efficiency of production. Livestock and poultry used to be
produced predominantly in backyard farms and small-scale, “free
range” farms in China. However, such production model was incapable
of multiplying the production capacity. Instead, a steady shift from
family farms and “free range” farms to more specialized and much
larger concentrated animal feeding operations (CAFOs) has occurred
since the late 1970s. Industrial livestock and poultry production
achieves high output of meat, milk, and eggs by confining thousands or

⁎
Corresponding author.
E-mail address: hefac@umich.edu (H. Cheng).

http://dx.doi.org/10.1016/j.envint.2017.07.003
Received 15 March 2017; Received in revised form 5 July 2017; Accepted 10 July 2017
Available online 15 July 2017
0160-4120/ © 2017 Elsevier Ltd. All rights reserved.
Y. Hu et al.
more animals, almost always a single species, at high stocking densities
in localized areas. Advances in animal breeding, mechanical innova-
tions, and the use of formulated animal feed and feed additives have
helped increase the production efficiency of meat and dairy products in
CAFOs, and consequently reduced their cost to the consumers (Hribar,
2010). In particular, the modernization of China's food animal industry
was boosted by the Law on Animal Husbandry that took effect on July
1, 2006. This milestone legislature encourages the development of
large-scale and intensive animal farms, restricts the use of veterinary
drugs and feed additives to ensure the quality and safety of animal
products, and requires proper disposal of waste from livestock pro-
duction to protect the environment (NPCSC, 2005).
Large-scale livestock and poultry farms, i.e., CAFOs, accounted for
most of the increased production capacity in China over the past dec-
ades. Fig. S2 and Tables S1–S6 of the Supplementary Data show the
shift in the production scales of swine, poultry, layer chicken, dairy
cattle, beef cattle, and sheep and goat in China between 2000 and 2014.
Overall, the production of swine, poultry, and dairy cattle has been
transitioning towards CAFOs quickly, while this occurred at much
slower rates in the production of beef cattle, and sheep and goat. As of
2012, CAFOs accounted for the production of about 80% of chicken,
60% of pigs, and 40% of dairy cattle in China (Z. Liu et al., 2013).
Among the food-producing animals, production of poultry is the most
industrialized, and the poultry sold on the market are predominantly
raised in CAFOs. Meanwhile, unlike the industrial model followed in
many developed countries, beef cattle and sheep/goat farming is still
based primarily on the “free range” and scattered model in China,
which occurs primarily in the western provinces with low population
densities and vast pasture lands.
Along with the rapid growth of industrial livestock and poultry
production, the pollutants released from the multiplying CAFOs have
received increasing concerns. Nonetheless, compared to the pollutant
discharges from industrial sources, environmental degradation caused
by agricultural sources has received relatively little attention in China,
partially because their pollutant emissions are much less conspicuous
and more difficult to supervise. Fig. 2 shows the contribution of various
pollution source categories to water pollution in China between 2011
and 2015. Agricultural activities, including farming, aquaculture, and
livestock and poultry farming, are already the largest source of che-
mical oxygen demand (COD) and the second largest source of ammo-
nium nitrogen (NH4+-N). It was estimated that livestock and poultry
farming released a total of 12.68 million tonnes of COD, 1.02 million -
tonnes of total nitrogen, 0.16 million tonnes of total phosphorus,
2397 tonnes of copper, and 4757 tonnes of zinc into aquatic
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Environment International 107 (2017) 111–130
Fig. 1. Growth in the supply of animal food
products in China between 1980 and 2015 (data
from National Bureau of Statistics, http://data.
stats.gov.cn/index).
environment in 2010 (MEP, 2010). That is, livestock and poultry
farming contributed to about 41.9, 21.7, and 37.9% of the COD, total
nitrogen, and total phosphorus discharged from all types of waste-
waters, respectively. It is obvious that livestock and poultry farming has
become a key source of environmental pollution in China.
A large number of studies have been conducted investigating var-
ious aspects of the environmental pollution and human health impacts
of CAFOs, but no review has attempted to systematically explore the
major pollutants emitted from CAFOs, their environmental impacts, and
the potential human health risks from exposures to them. While a
comprehensive review of all the environmental and public health
consequences of industrial livestock and poultry farming is not possible
here, it is important to identify the major impacts of CAFOs on the
environment and human health. We identified studies using the most
popular sources of scientific information, including PubMed, Scopus,
and Web of Science, and search terms such as CAFO, public health, and
environmental pollution, etc. to retrieve information on specific sub-
jects. With a special focus on the problem in China, several Chinese
papers were also identified using a major Chinese reference database,
CNKI (China National Knowledge Infrastructure). In addition, limited
information from conference proceedings, technical reports published
by several agencies and organizations, news from an authoritative
Chinese media source, statistical yearbooks, rules and technical
guidelines by Chinese government was included. Although the grey
literature referenced might contain biased viewpoints, the findings
were consolidated with those from the peer-reviewed publications to
ensure their validity as much as possible.
In this review, we summarize the major pollutants released from
industrial livestock and poultry farming operations, and pollution of
environmental media caused by them, focusing primarily on surface
water, soil, and groundwater. The potential health risks for animal
producers and neighboring communities from exposures to various
pollutants emitted from the CAFOs are then discussed. We also identify
key mitigation strategies to reduce the environmental pollution and
human health risks brought by the multiplying CAFOs in China. Finally,
we propose paradigm changes to improve the sustainability of China's
animal agriculture and promotion of healthy diets to slow down the
growth in consumption of animal-based foods to protect public health
and reduce environmental degradation brought by industrial animal
farming operations.
Y. Hu et al.
2. Pollutant emissions from CAFOs and their impacts on the
environment
Environmental pollution caused by industrial livestock and poultry
production has not been much publicized in China, nor has the control
of such pollution been heavily prioritized, probably because it occurs in
rural areas and its impacts are often considered local. The vast majority
of CAFOs, particularly the small- and middle-sized ones located rela-
tively far away from urban areas, barely have any dedicated pollution
control measures. A range of pollutants can be released into the en-
vironment from livestock and poultry CAFOs with the air emissions and
the disposal of large volumes of animal waste. These pollutants not only
negatively affect the quality of air, surface water, soil, and ground-
water, but also pose risks to public health, as illustrated on Fig. 3. The
environmental and human health consequences could become poten-
tially significant in the areas surrounding CAFOs if the problem remains
uncontrolled with the rapid expansion of industrial animal farming.
2.1. Gaseous pollutants and bioaerosols
A range of gaseous pollutants and bioaerosols are generated by the
animals raised in confinement facilities of CAFOs, while they are also
released during the handling, storage, and land application of manure.
Carbon dioxide, methane, ammonia, hydrogen sulfide, volatile acids,
mercaptans, and amines with low odor thresholds are the major com-
pounds released by the animals and from the decomposition of their
manure (Centner and Patel, 2010; Cole et al., 2000; Donham et al.,
2006; NRC, 2003; Reeve et al., 2013; Pohl et al., 2017). Particulate
matter and bioaerosols (bacteria, endotoxins, fungi, mycotoxins, β-
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Environment International 107 (2017) 111–130
Fig. 2. Discharges of wastewater from all major
sources, and the associated COD and NH4+-N in
China over the 2011–2015 period (data from
MEP, 2017).
glucans, and particles of plant and animal origin) come primarily from
the dust and particles of dried feces, as well as waste handling and
spreading activities that can aerosolize the material (Cole et al., 2000;
Greger and Koneswaran, 2010; Hoff et al., 2006; Schinasi et al., 2011;
Thorne et al., 2009). Reduction in the nitrogen content of animal waste
occurs in the storage lagoons with volatilization of ammonia and other
N-containing compounds resulting from degradation of the organic
matter (Aneja et al., 2000; Harper et al., 2004). Hydrogen sulfide,
which forms from anaerobic decomposition of animal waste, is another
gaseous by-product of significant concern (Greger and Koneswaran,
2010; Pavilonis et al., 2013). Spreading of the animal waste to farm-
lands, particularly in the cases of over-application, can also emit the
microbial agents and products contained in the animal waste, as well as
the gaseous products into the atmosphere (Greger and Koneswaran,
2010).
Animal farming contributes to more than one-third of the global
methane emissions, which results primarily from the enteric fermen-
tation in ruminants (dominated by beef and dairy cattle) and the de-
composition of animal wastes (Steinfeld et al., 2006). In 2015, enteric
fermentation and manure management accounted for 25.4 and 10.1%
of the total anthropogenic emissions of methane in the U.S. (USEPA,
2017). According to the inventory for non-CO2 greenhouse gas emis-
sions in China for the year of 2005, the methane emissions by enteric
fermentation of livestock amounted to 302.0 MT of CO2-equivalent, or
35.6% of the total emissions from all anthropogenic sources, while that
from manure management was 60.1 MT of CO2-equivalent (7.1% of
anthropogenic emissions) (B. Zhang et al., 2015). In term of N2O
emission, manure management produced 83.7 MT of CO2-equivalent, or
23.5% of the total N2O emissions in the country (B. Zhang et al., 2015).
Fig. 3. Schematic illustration on the transport of
pollutants released from CAFOs and the path-
ways these pollutants can pose risk to human
health in rural areas.
Y. Hu et al.
With the fast growth in the numbers of animals farmed for meat, egg,
and dairy products in China, greenhouse gas emissions from the animal
agriculture can become increasingly more important. Further details on
the animal agriculture sector's contributions to climate change and
mitigation strategies are beyond the scope of this review, and can be
found in some excellent review papers (Koneswaran and Nierenberg,
2008; Llonch et al., 2017; Knapp et al., 2014; Hristov et al., 2013a,
2013b; Montes et al., 2013; Place and Mitloehner, 2010).
A recent modeling study found that the concentrations of hydrogen
sulfide and ammonia could exceed background levels by more than an
order of magnitude within 1 km of poultry CAFOs, and they could
impact the air quality within a range of several kilometers (Pohl et al.,
2017). Besides impacting the local, and even regional air quality, the
gaseous pollutants and bioaerosols emitted from CAFOs can also con-
tribute to water and soil pollution. For example, significant portion of
the ammonia volatilized into the air from storage lagoons and land
applied animal waste ends up in local surface water bodies through dry
and wet deposition, which can cause eutrophication of surface water
(Aneja et al., 2000, 2003; Costanza et al., 2008). Further discussion on
the environmental impacts of the mixtures of air pollutants emitted
from CAFOs is not possible as the topic has received little attention,
particularly in China.
2.2. Organic matter and nutrients
With hundreds to tens of thousands of animals raised in a single
CAFO, the amount of animal waste generated daily can be very large,
posing significant storage and disposal challenges. Table 1 summarizes
the typical waste production rates of cattle, pigs, chicken, and duck
raised in CAFOs. Over their lifespans, each cattle or pig generates
hundreds to thousands of kilograms of manure and urine, while each
chicken or duck produces nearly 30 kg of manure. The manure is ty-
pically stored on site in surface lagoons, where it undergoes decom-
position to some extent prior to disposal. In contrast, the wastewater
generated in CAFOs is sometimes discharged without any kind of
treatment into local surface water bodies. It has been estimated that
only one-fifth of the livestock farms in China are equipped with the
simple treatment facilities of lagoons and sedimentation tanks (Liu
et al., 2012). Table 2 summarizes the means and ranges for the contents
of COD, NH4+-N, total nitrogen, and total phosphorus in the waste-
water from pig, beef cattle, dairy cattle, layer chicken, and duck farms.
Clearly, wastewater from CAFOs can be a significant source of en-
vironmental pollution if discharged directly into the environment. It
should be noted that the generation rates of pollutants can vary sig-
nificantly depending on the growth characteristics and the intake rates
of feed and nutrients of the animals, as exemplified by those of swine in
different feeding stages (Table 3).
With high contents of organic matter and macronutrients, animal
waste was traditionally incorporated into farmland soils to improve soil
fertility and crop yields in China (Shen et al., 1997; Yang et al., 2004).
Table 1
Typical waste production rates of different species of farmed animals in China (data from
MEP, 2009).
Animal species Cattle Pig Chicken Duck
Lifespan Days 365 199 210 210
Manure generationa kg per day 20 2 0.12 0.13
kg per life span 7300 398 25.2 27.3
Urine generationa kg per day 10 3.3 – –
kg per life span 3650 656.7 – –
Note:
a
It should be noted that the values listed here are the reference production rates used
for estimating the designed treatment capacity for animal waste when measurement data
or data from comparable livestock and poultry farms are not available (MEP, 2009). The
waste generation rates can vary largely, depending on the animal species, management
practices, climate, and season.
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Environment International 107 (2017) 111–130
Family-based and “free range” animal farms produce relatively small
amount of animal waste, which can be effectively used as an organic
fertilizer on local agricultural fields after composting. In contrast, be-
cause of the high content of water and high cost of transportation,
application of the manure generated in CAFOs to farmlands farther than
5–15 km away is economically unattractive (FAO, 2010), thus the
manure is spread, often repeatedly, on local farmlands. Fig. 4a shows
that the annual generation of animal waste and the associated COD,
total nitrogen, and total phosphorus by farmed animals in China had
been increasing quickly over the period of 1978 and 2011. Fig. 4b
depicts the average manure loadings of farmlands in different provinces
of mainland China estimated from the livestock and poultry production
and the cultivated land areas in 2011. Although no limit on manure
loading of farmland has been established in China, a threshold of
30 tonnes/hm2 was commonly adopted for assessing the risk of farm-
land pollution brought by land application of manure (Wang et al.,
2006; Zhu et al., 2014). The average manure loading of farmland in a
total of 6 provinces already exceeded this threshold, with Shandong
having the highest provincial average (105.3 tonnes/hm2), followed by
Beijing (55.4 tonnes/hm2). In comparison, the average manure loadings
of farmlands in Liaoning (33.1 tonnes/hm2), Fujian (31.5 tonnes/hm2),
Shanghai (30.9 tonnes/hm2), and Guangdong (30.7 tonnes/hm2) were
barely above the limit. It should be noted that the provincial average
values were calculated with the assumption that the animal waste was
uniformly applied on all the farmlands within the province, while the
lands surrounding CAFOs actually received animal waste at much
higher rates.
When animal waste is over-applied on farmlands, the excessive
amount of nutrients cannot be absorbed efficiently, and can run off
easily into the surface water or leach into the groundwater through
permeable soils (Burkholder et al., 2007; Steinfeld et al., 2006). In
addition, leakage from storage lagoons, and overflow of lagoons in
cases of heavy rainfall may also result in surface water contamination.
Spill of wastewater from CAFOs could cause development of very large
anoxic zones in surface water bodies (Burkholder et al., 1997; Mallin,
2000). In some areas of south China, swine manure was even dumped
directly into local ponds or waterways as the quantity produced far
exceeded what could be absorbed by the local farmlands, resulting in
direct releases of the nutrients and pollutants into surface water. The
excess nutrients, primarily phosphorous, can induce algal blooms and
cyanobacterial growth, while the associated hypoxia/anoxia conditions
developed in water column and high levels of ammonia can kill aquatic
animals.
2.3. Pathogens
Livestock and poultry, including swine, cattle, and chicken, can be
infected by numerous bacterial, viral, and parasitic enteric pathogens
that are also infectious to humans (Greger and Koneswaran, 2010).
Thus, the waste generated by livestock and poultry is a reservoir for a
wide range of pathogens. In CAFOs, particularly those raising swine,
animal waste is often removed from the production facilities by water
flushing, with the slurry collected and held in storage lagoons. Although
anaerobic digestion of the animal waste occurring in the storage la-
goons could kill or significantly reduce many pathogenic microbes, they
could still be present at substantial densities in waste spills and seepage
of lagoons, causing contamination of surface water bodies and
groundwater (Burkholder et al., 1997; Gentry-Shields et al., 2015;
Heaney et al., 2015; Mallin, 2000). Composting (at temperatures above
55 °C) can also drastically reduce the numbers of pathogens in manure,
but inconsistent pathogen reduction may occur if not managed properly
(Tiquia et al., 1998; Turner, 2002).
Overflow, spill, and seepage from manure storage lagoons can cause
pathogenic contamination of surface water and groundwater, while
land application of liquid and solid animal waste also transports the
pathogens in them to soils, surface water, and groundwater. Many of
Y. Hu et al. Environment International 107 (2017) 111–130

Table 2
Means and ranges (reported in parentheses) for the contents of major pollutants in the wastewater from livestock and poultry farms with different manure removal methods (data from
MEP, 2009).

Farmed animal Manure removal method CODcra, mg/L NH4+-Na, mg/L Total nitrogena, mg/L Total phosphorusa, mg/L pH

Pig Dry manure removal 2.64 × 103 (2.51–2.77 × 103) 261 (234–2880) 370 (317–423) 43.5 (34.7–52.4) 6.3–7.5
Manure cleaning by rinsing 2.16 × 104 (1.56–4.68 × 104) 590 (127–1780) 805 (141–1970) 127 (32.1–293)
Beef cattle Dry manure removal 887 22.1 41.1 5.33 7.1–7.5
Dairy cattle Dry manure removal 983 (918–1050) 51 (41.6–60.4) 67.8 (57.4–78.2) 18.6 (16.3–20.4) 7.1–7.5
Layer chicken Manure cleaning by rinsing 6.06 × 103 (2.74–10.5 × 103) 261 (70–601) 342 (97.5–748) 31.4 (13.2–59.4) 6.5–8.5
Duck Dry manure removal 27 1.85 4.7 0.139 7.4

Note:
a
It should be noted that pollutant concentrations in the wastewater can vary largely, depending on the animal species, management practices, climate, and season.

the pathogens in manure can survive in storage lagoons and soils after
land application for long periods of time (Burkholder et al., 2007;
McLaughlin et al., 2012; Nicholson et al., 2005). The survival of pa-
thogens following land application of the untreated or treated animal
waste depends on their interactions with indigenous microbial com-
munities, as well as the environmental factors, such as temperature, pH,
and moisture and nutrient contents of the soil (Avery et al., 2012). In
general, enteric pathogens could better survive in soils than in manures
or slurries, and cool temperatures favor their survival (Guan and
Holley, 2003). Bacterial pathogens, viruses, and protozoa could typi-
cally survive up to approximately two months, three months, and two
days in soils, respectively (Gerba and Smith, 2005). Depending on the
soil conditions and the organic wastes amended, survival times ranging
from days to over a year have been documented for bacterial pathogens
in soils (Avery et al., 2012). Manure-borne pathogens can also enter
rivers and lakes due to overflow of lagoons in cases of heavy rainfall
and runoff from manure-fertilized farmlands with rainwater and irri-
gation water, and leach into groundwater from the storage lagoons and
the farmlands as well. Significant increases in the concentrations of
pathogens in rivers adjacent to animal farms had long been documented
(Janzen et al., 1974; Walker and Grimes, 1985), while transport of
enteric microbes from manure-treated soils to surface water and
groundwater was also widely observed (Culley and Phillips, 1982;
Gagliardi and Karns, 2000; Mawdsley et al., 1996). Widespread fecal
pollution of surface waters impacted by animal farming operations has
been observed in China (Chen et al., 2011; Zhuang et al., 2017). The
occurrence of manure-borne pathogens at elevated levels adversely
affects the quality and safety of water resources. The disease-causing
pathogens, with well-known health effect on humans, can also poten-
tially impact aquatic organisms, which have not been well studied.
2.4. Antimicrobials, estrogens, and heavy metals
While the organic matter, nutrients, as well as dissolved solids and
salts are the normal components in animal waste, a range of veterinary
drugs and feed additives administered to the farmed animals via in-
jection, feed, and drinking water also end up in the animal waste.
Veterinary drugs, particularly antimicrobials, are used in food animal
production primarily for the purposes of disease control and growth
promotion, while trace elements are routinely supplemented in animal
feed to improve animal health and performance. As a result of their
large volumes used in food animal production, significant quantities of
these drugs and feed additives are discharged into the environment via
animal waste. In addition, steroid hormones produced naturally by
animals, along with those administered on them, are also excreted in
urine and feces. Table 4 summarizes the sources of antimicrobials, es-
trogens, heavy metals in animal waste, as well as their occurrence and
fate in environmental media, and potential impacts on the ecosystem.
Wastewater and liquefied animal waste loaded with these pollutants
can flow into local rivers and other waterways through spills, manure
runoff, and sometimes intentional releases. Although application of
animal waste (with and without treatment) can improve soil fertility
and soil property, the resulting accumulation of these pollutants, par-
ticularly the non-degradable heavy metals in soils, can cause significant
environmental concerns and pose potential risk to the ecosystem. An-
timicrobials, steroid hormones, and heavy metals can also be leached
out of the animal waste applied on agricultural fields by rainwater and
irrigation water, and subsequently cause contamination of surface
water and groundwater and impact the aquatic organisms. Overall,
while organic matter, nitrogen, phosphorus, and microorganisms are
traditionally the main problems associated with animal waste disposal,
antimicrobials, steroid hormones, and heavy metals contained in the
waste have emerged as important environmental concerns.
3. Human health risks of pollutants originated from CAFOs
The gaseous pollutants and bioaerosols emitted from CAFOs, and
the wide range of pollutants released into the air, surface water, soil,

Table 3
Growth characteristics, feed and nutrient intake rates, and pollutant generation rates of female pigs in different feeding stages observed in a swine CAFO in northern China (data from
Dong et al., 2011).

Feeding stage Nursing Fattening Breeding

Feed and nutrient intake Pollutant discharge Feed and nutrient intake Pollutant discharge Feed and nutrient intake Pollutant discharge

Average weight (kg) 31.3 ± 3.9 67.9 ± 6.7 203 ± 3.0

Weight gain (kg/d) 0.63 ± 0.18 0.69 ± 0.20 –
Feed intake (kg/d) 1.7 ± 0.27 2.5 ± 0.47 2.3 ± 0.18
Manure generation (kg/d) 0.91 ± 031 1.73 ± 0.60 1.63 ± 0.53
Urine generation (L/d) 1.66 ± 0.42 2.83 ± 0.42 4.68 ± 0.26
COD generation (g/d) 252.8 ± 70.1 479.6 ± 163.4 493.4 ± 147.4
Total nitrogen (g/d) 47.5 ± 9.5 20.4 ± 5.7 64.8 ± 17.2 33.2 ± 10.4 49.3 ± 3.8 43.7 ± 12.8
Total phosphorous (g/d) 10.7 ± 4.6 3.48 ± 1.28 10.9 ± 5.8 6.06 ± 1.78 14.2 ± 5.3 9.93 ± 1.44
Copper (mg/d) 267 ± 135 220.0 ± 48.0 188 ± 33 136.4 ± 51.0 52.6 ± 3.4 49.3 ± 6.1
Zinc (mg/d) 333 ± 88 285.3 ± 88.6 331 ± 69 281.7 ± 120.7 289 ± 25.1 279.0 ± 72.8

Note: All values are based on monitoring results for 5 female pigs conducted over all four seasons in a swine farm (with annual production of 10,000 heads) located in the rural area of
Beijing, China (Dong et al., 2011).

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Y. Hu et al.
and groundwater from animal waste can impact human health. The
noxious and unpleasant odors associated with animal waste generated
in CAFOs are well recognized as a public nuisance, while the selection
and spread of antimicrobial resistance (AMR) represents a potentially
significant public health risk, which is a concern globally. It should be
noted that the health risk of all pollutants associated with CAFOs is
higher for the vulnerable populations, including the young children, the
elderly, pregnant women, and the immunocompromised individuals
(Burkholder et al., 2007; Greger and Koneswaran, 2010).
3.1. Direct risks from pollutants in environmental media
Gases, vapors, fumes, and particulate matter emitted from the an-
imal confinement buildings and manure storage lagoons of CAFOs, as
well as land application of manure can affect not only the people
working in the CAFOs and on the farmlands, but also the neighboring
communities (Centner and Patel, 2010). Modeling results indicate that
the mixtures of chemical pollutants emanating from CAFOs had low
potential for adverse health effects on residents living near the CAFOs,
while the exposure to organic dust might have a significant impact
(Pohl et al., 2017). Nonetheless, exposure assessment using optimized
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Environment International 107 (2017) 111–130
Fig. 4. Waste generation from China's animal
agriculture and the average manure loading of
farmlands: (a) Annual generation of animal waste
(manure + urine) and the associated pollutants;
and (b) Estimated average manure loadings of
farmlands in different provinces in 2011. All data
are adapted from Zhu et al. (2014).
estimation technique suggests that ammonia emitted from CAFOs
contributed to burden of respiratory diseases among neighboring re-
sidents (Schulze et al., 2011). Occupational exposure to the air pollu-
tants at CAFOs has been well documented among the workers. The
airborne pathogens and endotoxins are known to cause adverse re-
spiratory effects, and workers in swine and poultry CAFOs, where air
emissions are concentrated in the confinement buildings, have elevated
occurrence of acute and chronic respiratory health problems, such as
sinusitis, bronchitis, mucus membrane inflammation, nose and throat
irritation, and decline of pulmonary functions (Cole et al., 2000;
Donham et al., 2007; Heederik et al., 2007). Buildup of hydrogen sul-
fide in manure pits could cause workers to lose consciousness or even
death (Greger and Koneswaran, 2010). Air emissions of CAFOs have
also been found to impact the health of neighboring residents in epi-
demiological studies. Neighbors of swine farms suffered more cases of
headache, runny nose, sore throat, coughing, diarrhea, and burning
eyes than comparable population living far away from CAFOs (Schinasi
et al., 2011; Thu, 2002; Wing and Wolf, 2000). The prevalence of
neurobehavioral and respiratory symptoms among children and adults,
who might have been exposed to the airborne pollutants from CAFOs,
was significantly increased compared to those without such exposure
 Table 4
Summary of the sources of antimicrobials, estrogens, and heavy metals released with animal waste from CAFOs and their impacts on the environment and ecosystem.
Pollutant Sources
Antimicrobials Besides treatment and prevention of animal diseases
caused by pathogens, antimicrobials are also used
routinely at sub-therapeutic levels to promote
animal growth and increase feed efficiency (Marshall
and Levy, 2011; Mathers et al., 2011; Mole, 2013;
Teuber, 2001).
The closely confined, stressful, and often unsanitary
conditions of CAFOs allow infectious diseases to
develop and spread easily, thus administration of
antimicrobials is often adopted as a convenient and
low cost solution to compensate for the poor
production practices (Hu and Cheng, 2015, 2016;
Mole, 2013; Marshall and Levy, 2011).
The fractions of drugs not absorbed or metabolized
in animal bodies, which are often significant
(e.g., < 20 to near 100% for common antimicrobials
in livestock and poultry), are excreted via urine and
feces (Kim et al., 2011; Sarmah et al., 2006).
Estrogens Some steroid hormones are naturally produced by
animals and constantly excreted in urine and feces,
while their types and excretion rates depend on a
117
range of factors, including the species, sex, age, and
reproductive cycle of the animal (Hanselman et al.,
2003; Shore and Shemesh, 2003).
It has been observed that the ratios of 17β-estradiol
to macronutrients in swine waste in the farrowing
stage were approximately two times higher than
those in the waste generated during the finishing
stage, and over four times higher compared to those
in the waste of lactating cows (Raman et al., 2004).
A similar trend was also observed for estrone, while
the highest 17α-estradiol to macronutrient ratios
was found in dairy cattle waste (Raman et al., 2004).
Steroid hormones can be excreted in the free form,
or as the biologically inactive conjugates with
glucuronide and/or sulfate groups, which can be bio-
transformed readily to the bio-active free form in the
environment (Arnon et al., 2008; Hanselman et al.,
2003; Hutchins et al., 2007; H. Zhang et al., 2014).
Besides the natural ones, synthetic estrogen
hormones are also used to promote the reproduction
and growth of farmed animals.
Use/occurrence in animal farming
Due to the ready availability of veterinary drugs at
low costs and poor oversights, their overuse and
misuse had been widespread in China (Ellis and
Turner, 2007; Hvistendahl, 2012; Larson, 2015),
resulting in a much greater average usage of
antimicrobials than those in the developed countries
(Hu and Cheng, 2015).
It has been reported that animal farming in China
consumed approximately 6000 and 97,000 tonnes of
antimicrobials in the year of 2001 and 2007,
respectively (Ellis and Turner, 2007; Hvistendahl,
2012).
A recent study estimated that a total of
84,240 tonnes of antimicrobials (all types) were used
in China's animal production in 2013 (Q. Zhang
et al., 2015).
Another study estimated that 38,500 tonnes of
antimicrobials were used in China's swine and
poultry production in 2012 (Krishnasamy et al.,
2015), although this number was based on the
recommended feed formulations in the U.S., instead
of the actual drug usages in China's animal farms.
It has been estimated that animal waste from CAFOs
accounts for approximately 90% of the total estrogen
load in the environment (Khanal et al., 2006).
A survey of livestock farms in north China found that
each dairy cattle excreted, primarily through feces
(> 90%), 956–1270 μg/day of total (free and
conjugated) estrogens, which are several times
higher than that (244–320 μg/day) of beef cattle (H.
Zhang et al., 2014). In comparison, each pig excreted
260–290 μg/day of total estrogens, almost
exclusively through urine (98–99%), while the
excretion rates were 21.6–28.7 and 4.6–5.4 μg/day
for sheep and broiler chicken, respectively (H. Zhang
et al., 2014).
It was estimated that swine and dairy cattle sources
released a total of 139 and 65.8 tonnes of steroids to
the environment annually in China, which are both
greater than that (60.7 tonnes/year) from human
source (Liu et al., 2012).
Synthetic hormones (e.g., 17α-ethinylestradiol)
excreted by the animals have also been detected in
the wastewater from CAFOs and rivers impacted by
discharges from CAFOs in south China (Liu et al.,
2012).
Occurrence and fate in the environment
It has been reported that veterinary use (pig: 52.2%,
chicken: 19.6%, and other animals: 12.5%) in China
accounted for 84.3% of the total consumption of 36
common antimicrobials (11 sulfonamides, 5
tetracyclines, 8 fluoroquinolones, 5 macrolides, 4 β-
lactams, 2 chloramphenicols, and 1 lincomycin with a
sum of 78,146 tonnes) in 2013, while up to
45,360 tonnes of them were excreted into the
environment by the animals (Q. Zhang et al., 2015).
The widespread use of veterinary antimicrobials,
along with the overall lack of treatment for
wastewaters discharged from animal farms, could
explain their frequently detection in the soils, surface
water, marine water, and sediments impacted by
discharges from CAFOs (Ben et al., 2013; Li et al.,
2011; Liu et al., 2016; Wei et al., 2011; Xiang et al.,
2016; Zhang et al., 2016; Zhou et al., 2011).
A study found that the 17β-estradiol equivalents of
four estrogens in cattle feces collected from 24 CAFOs
in northeast China ranged from 45.8 to 926 μg/kg
(Han et al., 2011). The average concentrations of 17α-
estradiol, 17β-estradiol, and estrone were 195, 104,
and 262 μg/kg in dairy cattle feces, respectively, while
their corresponding concentrations in beef cattle feces
were 104, 67.7, and 216 μg/kg, respectively (Han
et al., 2011).
Natural estrogens excreted by animals in CAFOs can
enter the environment with land spreading of manure
and leakage or spills of manure lagoons.
Animal waste in slurry form is held in manure lagoons,
where the estrogens could biodegrade under both
aerobic and anaerobic conditions (Zhao et al., 2010;
Zheng et al., 2013).
Solid/dry manure is often composted in windrows or
stacked piles prior to land application, where the
natural estrogens can biodegrade relatively fast under
aerobic conditions (Kolok and Sellin, 2008).
It has been found that 18.7, 34.1, 50.9, and 59.6% of
the total estrogens were removed by composting from
the feces of chicken, beef cattle, cow, and sheep,
respectively, and the concentrations of total estrogens
in the composted manures were between 13.0 and
74.0 ng/g (H. Zhang et al., 2014).
With animal manure applied for land fertilization over
long periods, the manure-borne estrogens can
accumulate in the farmland soils, and thus become a
potential source of these compounds. Runoff from
farm soils and infiltration through the soils can result
in elevated levels of manure-borne estrogens in
Y. Hu et al.
Impacts on ecosystem
The concentrations of antimicrobials found in animal
manure and lagoon effluent are generally not high
enough to cause adverse effects on organisms.
Antimicrobials can impact the microbial communities
by altering phylogenetic structure, causing resistance
expansion, and disturbing ecological function in the
micro-ecosystem (Ding and He, 2010).
Even the antimicrobials bound to soil particles are still
bioactive and exhibit antibacterial activities (Chander
et al., 2005; Peng et al., 2014).
The presence of antimicrobials has been reported to
influence biomass production, and biotransformation
of elements (e.g., nitrogen and sulfur) and organic
pollutants (e.g., pyrene) in soils and aquatic
environment (Cordova-Kreylos and Scow, 2007;
Hansen et al., 1992; Klaver and Matthews, 1994;
Kotzerke et al., 2008; Naslund et al., 2008; Thiele-
Bruhn and Beck, 2005).
Many antimicrobials have also been proven to affect
plant's developmental and physiological processes
(Bartikova et al., 2016).
Steroid hormones in surface water have the potential
to disrupt endocrine function, activate the estrogen
receptors, and change secondary sex characteristics of
sensitive aquatic species even at low ng/L
concentrations (Hanselman et al., 2003).
The presence of natural estrogens, such as 17α-
estradiol, 17β-estradiol, and estrone, at
environmentally relevant concentrations (down to a
few ng/L), has been shown to adversely impact the
development of a range of aquatic species, such as
turtles, trout, and minnows (Irwin et al., 2001; Panter
et al., 1998; Thorpe et al., 2003).
It has been found that the substrate utilization and
enzymatic activities of microbial communities in a
lake sediment contaminated with trenbolone were
significantly suppressed (Radl et al., 2005).
A recent study reported that soil microbial activity
and bacterial diversity were enhanced by the presence
of degraded estrone and 17β-estradiol, which
probably served as nutrient sources to the soil
microorganism, although such positive effects could
be suppressed by the presence of sulfamethoxazole as
a co-pollutant (X. Zhang et al., 2014).
Many hormones are also known to have phytotoxicity
by impacting plant developmental and physiological
processes (Bartikova et al., 2016).
(continued on next page)
Environment International 107 (2017) 111–130
 Table 4 (continued)
Pollutant Sources
118
Heavy metals Trace elements, including copper and zinc, and to a
lesser extent, nickel and selenium, which are
essential for many physiological processes in
animals, are supplemented extensively in
commercial feed in the forms of oxides or sulfate
salts to improve animal health and performance
(Richards et al., 2010).
Only small fractions (10–20%) of the ingested trace
elements are absorbed by the animal bodies, while
the rest are excreted into the environment via urine
and feces.
Unlike other metals, arsenic is widely used in the
form of phenylarsenicals (primarily roxarsone and p-
arsanilic acid) in swine and poultry farming to
improve weight gain, enhance feed efficiency, and
control intestinal parasites (X. Liu et al., 2013;
Mangalgiri et al., 2015).
Use/occurrence in animal farming
With most of the trace elements (e.g., Cu, Se, Zn, and
As) supplemented to commercial feed excreted by
the animals, manure often contains elevated levels of
Cu (up to ~ 1000 mg/kg) and Zn (up to 1500 mg/kg)
(Shi et al., 2011, Y. Zhang et al., 2014).
Due to the toxicity of their degradation products
(arsenite and arsentate), the use of phenylarsenicals
as animal feed additives has been banned in the
European countries and in the U.S., but they are still
legally and widely used in China, along with many
other countries around the world (X. Liu et al. 2013).
Occurrence and fate in the environment Impacts on ecosystem
Y. Hu et al.
surface water, sediments, and groundwater.
In a typical intensive vegetable cultivation area with a
long history of heavy manure application in north
China, the concentrations of seven steroids (estrone,
17α-estradiol, 17β-estradiol, estriol, testosterone,
androstendione, and progesterone) in the soils from
vegetable greenhouses ranged from non-detectable to
110 μg/kg (F. Zhang et al., 2015). Their
concentrations in the water from the adjacent
drainage ditch and the groundwater were up to 14 and
2.4 ng/L, respectively, while their concentrations in
the sediments of drainage ditch were up to 3.0 μg/kg
(F. Zhang et al., 2015).
In the sediments of storage lagoon and the effluent
drainage drench of a dairy CAFO in north China, 17α-
estradiol, 17β-estradiol, and estrone were found to
occur at concentrations ranging from below the
detection limit to 6.6 μg/kg, while they were detected
in the range of 3.2–31.6 ng/L in local groundwater (Li
et al., 2012).
Even though natural estrogens derived from animal
manure can biodegrade rapidly in farm soils and
sediments, and some of them (e.g., 17β-estradiol) can
also undergo abiotic degradation (Khanal et al., 2006;
Kolok and Sellin, 2008), they occur at measurable
concentrations in the farmlands fertilized by animal
manure and the surface water impacted by runoff from
these fields as a result of repeated manure application.
Unlike organic pollutants, heavy metals do not The elevated concentrations of metals (e.g., Cu and
undergo degradation, storage of animal waste in Zn) could negatively affect soil quality and soil
lagoons and its land application can lead to microbial community, and reduce the yield and
contamination of surface water and soils (Duan et al., quality of crops (Athar and Ahmad, 2002; Baker et al.,
2012; Fan et al., 2013). 2011; Cheng et al., 2007; Nagajyoti et al., 2010; Zhou
It has been reported that the concentrations of Cu and et al., 2005).
Zn increased by around 17 and 19 times, respectively, While phenylarsenicals have relatively low toxicity,
in farmland soils after repeated application of pig they can degrade into more toxic and mobile
manure for 17 years (Wu et al., 2012). inorganic arsenic species (arsenate and arsenite) in
Heavy metals accumulated in the soils can leach into the environment (Mangalgiri et al., 2015).
groundwater or run-off into surface water with
irrigation water or rainwater, while spills from the
animal waste lagoons can result in their direct
discharge into surface water.
Phenylarsenicals can undergo degradation to produce
inorganic arsenic during manure composting
(Garbarino et al., 2003), in surface water under
sunlight irradiation (Xie et al., 2016), and in surface
soils through oxidation mediated by metal oxides
(e.g., δ-MnO2) (Wang and Cheng, 2015).
Studies showed that phenylarsenic compounds can
transform both abiotically and biotically under
anaerobic conditions, but barely undergo
biodegradation under aerobic conditions (Cortinas
et al., 2006; Stolz et al., 2007).
Repeated application of animal waste containing
phenylarsenicals could elevate the arsenic levels in the
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Y. Hu et al. Environment International 107 (2017) 111–130

(Greger and Koneswaran, 2010; Merchant et al., 2005; Mirabelli et al.,

2006; Radon et al., 2007; Von Essen and Auvermann, 2005), and the
health risks were particularly high for pregnant women and children
(Merchant et al., 2005; Mirabelli et al., 2006). It has been estimated
that infant mortality increased by 2.8% in the counties with increases in
animal units in the U.S. between 1982 and 1997, and that infant
mortality could increase by 7.4% with the doubling of CAFOs
(Sneeringer, 2009).
Overall, cross-sectional and longitudinal studies conducted in North
Impacts on ecosystem

America consistently showed that exposure to air pollutants near swine

CAFOs was associated with increased upper respiratory symptoms and
nose and eye irritation (Merchant et al., 2005; Schinasi et al., 2011;
Villeneuve et al., 2009; Wing and Wolf, 2000). Although no systematic
evaluation on the human health impact of CAFOs has been conducted in
China, similar risk is expected for the country's CAFOs due to the very
similar, and probably poorer, animal farming practices. It should be
The levels of total arsenic in the surface soils from an

contribution of animal manure to soil arsenic pollution

119.0 mg/kg) in the manures from 8 swine farms in

CAFOs in Guangdong of south China were elevated,

concentrations, which is indicative of the important

Arsenic was detected at appreciable levels (0.42 to

noted that most of the published epidemiological studies were based on

Beijing, with the manures from 2 farms containing
arsenic at concentrations exceeding 75 mg/kg of

agricultural zone with densely distributed swine

and p-arsanilic acid was detected at appreciable

personal health interviews or self-administered questionnaires, while

the prevalence of self-reported symptoms could be quite different from
Occurrence and fate in the environment

that derived from doctors' diagnosis (Harlow and Linet, 1989;

Kriegsman et al., 1996; Mohangoo et al., 2006; Smith et al., 2008). It
has long been known that the occurrence rates of respiratory condi-
in such areas (Liu et al., 2015).

tions, including asthma, sinusitis, and chronic bronchitis, reported by

arsenic (Li and Chen, 2005).

the patients were higher than those diagnosed by their general practi-
tioners (Harlow and Linet, 1989). The prevalence rates of asthma or
chronic obstructive pulmonary disease (COPD) in the general popula-
farmland soils.

tion of the Netherlands diagnosed by doctors were only approximately a

quarter of the estimates from health interview surveys (Mohangoo
et al., 2006). On the other hand, a recent study found that among the
residents living in the vicinity of livestock farms in southern Nether-
lands, a substantial number of people with spirometry-based COPD
were not identified by self-reported questionnaires or medical records
(Borlee et al., 2017a). A cross-sectional study based on the medical
records from general practitioners revealed positive association be-
tween pneumonia and unspecified infectious diseases diagnosed by
doctors and the number of goat CAFOs near homes of the neighboring
Use/occurrence in animal farming

residents, but no association was found between the occurrence of re-

spiratory, allergic or gastrointestinal conditions and the presence of
swine, cattle, and poultry CAFOs in a region with high CAFO density in
the Netherlands (Hooiveld et al., 2016). Another cross-sectional study
based on pulmonary function test found an association between lung
function reduction and air pollutant emissions from livestock farms
among non-farming, rural residents in the Netherlands (Borlee et al.,
2017b).
The crowded conditions in CAFOs increase the chance of trans-
mission of disease-causing pathogens among animals raised in them
(Gilchrist et al., 2007). In particular, the large populations of animals
raised in close confinement provide an environment that facilitates the
evolution of new infectious diseases (Coman et al., 2013; Hollenbeck,
2016). On the other hand, farm-to-farm transmission of diseases can be
limited by the significant separation between CAFOs. The chance for
transmission of the pathogens to the general population is also low due
to the lack of direct and indirect contacts, although such pathogens
have much greater chance of infecting the CAFO workers. Livestock and
poultry manure contains a range of enteric pathogens, which can affect
the sanitary quality of water and sediments and pose potential public
health risks. Recreational body-contact or consumption of the water
contaminated by these pathogens can result in illness and diseases, such
Sources

as diarrhea, typhoid fever, and cholera (Burkholder et al., 2007).

Human infections can also result from consumption of the water and
Table 4 (continued)

vegetable crops contaminated by animal waste, as well as the meat

contaminated by fecal matter during animal slaughtering (Barza, 2002).
The chemical pollutants in animal waste, including nutrients, ve-
Pollutant

terinary antimicrobials, estrogens, and heavy metals, can also pose

human health hazards through consumption and/or recreational con-
tact of contaminated water (Burkholder et al., 2007; Kolok and Sellin,

119
Y. Hu et al.
2008; Nachman et al., 2005). The presence of nutrients, particularly
phosphorous, at elevated levels in surface water causes algal blooms
and growth of cyanobacteria, leading to the production of algal toxins
(e.g., microcystins) and bioactive compounds that can cause acute and
chronic illnesses in humans (Carmichael et al., 2001; Rao et al., 2002).
Elevated levels of nitrate in drinking water can cause serious illness for
young infants (< 6 months), while nitrate in drinking water can also
bring a range of other health effects, including cancer, adverse re-
productive outcomes, diabetes, and thyroid conditions (Ward et al.,
2005; Yang and Cheng, 2007). Although exposure to antimicrobials and
residues of other drugs in drinking water at low levels does not re-
present a major health risk (Webb et al., 2003), the health consequence
of unintentional long-term exposures to multiple drugs can be of con-
cern (Burkholder et al., 2007). Similarly, estrogens can exhibit biolo-
gical hormonal activity at very low levels, while the potential effect of
their occurrence in drinking water on human health is not clear
(Burkholder et al., 2007). As the rural communities in China typically
do not have any water treatment or disinfection utilities, contamination
of local groundwater and surface water sources is of particular concern.
Some organic pollutants and heavy metals accumulated in soils from
amendment of animal manure can be absorbed by agricultural crops
and vegetables, thus pose potential health risks to humans by entering
the food chain. For example, antimicrobials, including sulfonamides,
tetracyclines, and quinolones, have been detected at concentrations up
to several hundred μg/kg in vegetables grown in soils fertilized by
animal manure (Hu et al., 2010; Li et al., 2014; Wu et al., 2014; Zhang
and Cheng, 2017). In general, the occurrence levels of antimicrobials in
plants are far below the limits considered safe for animal or human
consumptions (Dolliver et al., 2007; Kumar et al., 2005). Heavy metals,
such as Cd and Pb, are well known to accumulate in the grains of cereal
plants, including maize, wheat, and rice (Athar and Ahmad, 2002;
Cheng et al., 2007; Hu et al., 2016). The intensive industrial develop-
ment and poor environmental protection were primarily responsible for
the widespread pollution of soils by heavy metals in China (Hu et al.,
2016). Nonetheless, repeated application of animal waste on farmlands
can lead to enrichment of heavy metals in surface soils in the rural
regions with little industrial activities, while the subsequent uptake and
accumulation of these metals in vegetables and cereal grains can pose
direct health risks to the consumers. In addition, with frequent use of
antimicrobials and other veterinary drugs in food animal production,
drug residues can occur at varying levels in foods of animal origin,
including meat, milk, and eggs, which bring food safety concerns (Table
S7).
3.2. Potential public health risk from AMR
Antimicrobials are typically present at very low levels in animal
products and food crops impacted by manure from CAFOs, and their
direct toxic effect on humans is negligible. On the other hand, the
emergence and spread of AMR in CAFOs due to the overuse and misuse
of antimicrobials represents a potential public health risk. The wide use
of antimicrobials at sub-therapeutic doses in CAFOs over long periods
of time naturally and unavoidably leads to the selection of bacteria
resistant to the antimicrobials (Mathers et al., 2011; McKinney et al.,
2010; Pruden et al., 2006). All major classes of antimicrobials except
vancomycins have been used in swine farms for disease treatment and
growth promotion in China (Zhu et al., 2013). The crowded conditions
in CAFOs favor selection of antimicrobial resistant bacteria, and once
emerged, the antimicrobial resistance genes (ARGs) can spread readily
among microorganisms of the same or different species (Chapin et al.,
2005; Marshall and Levy, 2011; Saenz et al., 2006).
AMR developed in CAFOs can be transferred easily from the farmed
animals to the workers at CAFOs and the neighboring communities by
the airborne bacteria (Barrett, 2005; Chapin et al., 2005). The risk is
particularly high for the workers in CAFOs, who are routinely exposed
to the air emissions from CAFOs and are in direct contacts with
120
Environment International 107 (2017) 111–130
hundreds to thousands of farmed animals and their waste (Barza,
2002). Resistant bacteria have been found at levels that could cause
human health hazard within the animal confinement facilities and
downwind of the CAFOs (Gibbs et al., 2004), while methicillin-resistant
Staphylococcus aureus (MRSA) were widely detected among swine and
swine workers in the U.S. (Khanna et al., 2008; Smith et al., 2009).
AMR developed in animal farms can also spread to humans through
direct contact and consumption of food products of animal origin,
particularly meat products. Recent studies showed that the abundance
of AMR carried by food-borne bacteria was relatively high in animal
products and AMR exhibited a generally increasing trend in food-pro-
ducing animals in China's major livestock production provinces (Jiang
and Shi, 2013; Lai et al., 2014). A metagenomics analysis found a total
of 70 resistance gene types in more than half of the human gut mi-
crobiota samples of Chinese individuals, much higher than those de-
tected in the people from Spain (49 types) and Denmark (45 types) (Hu
et al., 2013). The ARGs in human gut came probably both from the
adaption of bacteria strains after antimicrobial exposure in the gastro-
intestinal tract and from the antimicrobial-resistant bacteria and ARGs
spread from animals to humans. It has been observed that the abun-
dance of ARGs for antimicrobials used frequently in food animal pro-
duction was significantly elevated in human gut microbiome, particular
for those that had been used for longer times (Forslund et al., 2013). In
addition, pathogens carrying AMR can also contaminate surface water,
soil, and groundwater with spills and land application of animal waste
(Brooks et al., 2014; He et al., 2016). Consequently, human infections
might result from consumption of the water and vegetable crops con-
taminated by animal waste, as well as the meat contaminated by fecal
matter during slaughtering (Barza, 2002; Hu and Cheng, 2016).
As most of the antimicrobials used in livestock production, such as
tetracyclines, macrolides, sulfonamides, and quinolones, are also
widely used in human health care or are closely related to the medically
important ones for human use, AMR poses a significant public health
challenge by compromising the usefulness of human medicines
(Marshall and Levy, 2011; Martínez, 2008). Nonetheless, it is worth
noting that the relationship between antimicrobial use on food-produ-
cing animals and AMR in humans is complex and poorly quantified, and
even considered controversial (Jensen et al., 2004; Phillips et al., 2004;
Smith et al., 2005; van Bunnik and Woolhouse, 2017). While the high
use of antimicrobials in human healthcare is well accepted to be a key
driver of AMR in humans (Holmes et al., 2016), the specific contribu-
tion of the indirect routes of AMR transmission from animal farms to
the general population can be very difficult to quantify. Furthermore,
with the large variations in antimicrobial drugs, bacteria strains, animal
species in animal farms, as well as the significant differences in
healthcare systems and animal agricultural systems among countries,
quantitative evaluation likely yields vastly different results (van Bunnik
and Woolhouse, 2017). Mathematical models have been used as a
quantitative tool to understand the underlying epidemiological pro-
cesses of AMR spread (Lipsitch et al., 2002; Smith et al., 2005; van
Bunnik and Woolhouse, 2017). Smith et al. (2005) showed that the
development and transmission of AMR resulting from antimicrobial use
in agriculture could even have a greater impact on human health than
that of hospital use under certain model assumptions. On the other
hand, van Bunnik and Woolhouse (2017) found that reducing anti-
microbial use in animal farms alone had little impact on AMR in hu-
mans under many scenarios.
Although the contribution of antimicrobial use in animal farming
relative to that of human use to AMR development in the general po-
pulation of China is difficult to evaluate, the high antimicrobial use in
CAFOs has been well observed to contribute to the abundance and di-
versity of ARGs in the environment. Resistant bacteria and ARGs con-
tained in animal waste can be spread directly to the environment during
the handling and disposal of the waste discharged from CAFOs (He
et al., 2016). In addition, the releases of antimicrobials associated with
such activities also contribute to the development of AMR in the
Y. Hu et al.
impacted environmental compartments and its maintenance in bac-
terial populations, as emergence and enrichment of AMR in natural
environment can occur at very low concentrations of antimicrobials
(Gullberg et al., 2011; Martínez, 2008; Mole, 2013). Resistance to a
range of antimicrobials were found in the Escherichia coli isolates in the
surface water of the Min River drainage basin, a major intensive live-
stock and poultry production area in southeast China (Chen et al.,
2011). Furthermore, the occurrence rates of ARGs were comparable to
or even higher than those detected in fecal, wastewater, and clinical
isolates in China, North America, and Europe (Chen et al., 2011). Re-
sidues of tetracyclines and their degradation products in the range of
5.4 to 377.8 μg/kg (dry wt.) were found in the farmland soils near nine
swine farms in Beijing, Tianjing, and Zhejiang province, and the
abundance of tetracycline resistance genes was strongly correlated with
the contents of tetracycline residues in these soils (Wu et al., 2010). A
total of 149 unique ARGs had been detected in the manure from 3 swine
CAFOs located in north, east, and southeast China and in the soils
fertilized by the manure (Zhu et al., 2013). The concentrations of the
top 63 ARGs were 192 (median) and up to 28,000 times higher than
those in the antimicrobial-free manure and soils, while the abundance
of ARGs decreased in the order of fresh manure, composted manure,
and soils (Zhu et al., 2013). ARGs were also found to be prevalent in the
manure/litter, soil, sediment, and water samples of broiler chicken
farms located in Guangdong province of south China, with chlor-
amphenicol and sulfonamide ARGs having much greater abundance
than tetracycline ARGs, and the development of ARGs was apparently
contributed by the antimicrobials and metals (e.g., Cu, Zn, and As) (He
et al., 2014).
Overall, although the public health risk of antimicrobial use in
CAFOs remains uncertain due to the problem's biological complexity
(Smith et al., 2005), the spread of AMR from animal farms to the en-
vironment and human population can occur. Thus, restriction of anti-
microbial use in animal farming is necessary for the protection of public
health based on the precautionary principle.
4. Measures on mitigation of the environmental and public health
risks
4.1. Treatment of waste and wastewater
Proper treatment of the large volumes of wastewater and manure
generated in CAFOs can help mitigate their environmental impacts and
recycle some of the nutrients and even energy. Technical guidelines
have been established for the treatment of wastewater and manure
discharged from livestock and poultry CAFOs by the Ministry of
Environmental Protection (MEP) in China (MEP, 2009). Depending on
the number of animals raised, manure removal method (dry or wet),
and the environmental setting of the animal farms, different treatment
schemes for wastewater and manure from animal farms are required
(Fig. 5). Overall, the primary technologies used are anaerobic digestion
for liquid waste and composting for manure and digester sludge, which
are generally of low cost and robust.
Besides increasing the contents of nutrients and organic matter,
application of manure and composted manure can improve the struc-
ture, water-holding capacity, and drainage property of the soils, and
promote the growth of beneficial soil organisms (e.g., earthworms)
(Cheng et al., 2007). However, fresh manure may also have high con-
tents of soluble salts, viable weed seeds, and various pathogenic mi-
croorganisms. Composting is often adopted in the management of an-
imal manures to reduce their volume (~ 50 to 65%), and kill the
pathogens and weed seeds. The significant reduction in the volume and
mass of manure lowers the cost of transportation. Composting also re-
duces the soluble forms of nitrogen in manure and stabilizes the ni-
trogen in humus-like compounds, which mineralize slowly to provide
plant-available nitrogen (Flavel and Murphy, 2006). After proper
composting, manure can serve as an economic resource and greatly
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Environment International 107 (2017) 111–130
reduce the dependence of farmlands on chemical fertilizers. Com-
posting typically works only with dry manure handling systems, as
anaerobic conditions can develop in compost piles with too high con-
tents of water (> 60%), while solids separated from liquid manure
handling systems can also be composted.
For wastewater and liquefied manure, anaerobic digestion, which
converts the animal manure into a less toxic residue while generating a
combustible gas mixture (biogas), is the most frequently used treat-
ment. Besides treating the liquid waste from animal farms, biogas di-
gesters contribute to rural sustainability by reducing the dependence of
local households on biomass (straw and firewood) and coal for cooking
and heating (Hu and Cheng, 2013a). Biogas facilities have been actively
promoted for treating animal manure in China since 2000, and up to
50% of the cost for some biogas projects were subsidized by the central
and local governments (Min et al., 2013). The central government in-
vested 35 billion Yuan on promoting rural biogas during the 10th Five-
year plan period (2001–2005), and around 2200 large-scale biogas fa-
cilities capable of treating over 60 million tonnes of animal manure
were developed (Li, 2006). By the end of 2010, a total of 4700 biogas
facilities had been constructed, treating the manure from 39% of the
large- and medium-scale CAFOs (Min et al., 2013). Currently, installa-
tion of biogas digesters is mandatory for CAFOs with over 1000 cows,
10,000 pigs, or 100,000 chickens. Some environmentally progressive
local governments even require animal farms with as few as 50 pigs to
install biogas digesters.
Biogas digester is a promising way for disposing of the large mass of
animal waste plaguing the CAFOs while producing a safe and odorless
fertilizer and recovering energy from the animal waste. The biogas
production potential of the animal waste from large- and medium-scale
CAFOs in China was estimated to be 2.4 × 1010 m3, or the equivalent of
1.35 × 1010 m3 of natural gas in 2009 (Zhang et al., 2012). Despite of
the strong policy and financial supports from the central and local
governments, biogas digesters cannot be a panacea for solving the
manure disposal problem of CAFOs, as their performance is depended
on the climatic conditions. Nonetheless, to efficiently treat the manure
from CAFOs, the extra costs from adopting the necessary technologies
(e.g., with solar energy heating) to maintain microbial activity and
biogas production in the cold climates can be justified. Rich in nutrients
and minerals, the bio-slurry from biogas digesters is also an excellent
organic fertilizer, although large areas of farmlands are still required to
fully assimilate the nutrients in the bio-slurry. Meanwhile, the heavy
metals and some feed additives, such as un-degraded antimicrobials,
present in animal manure are also concentrated in the bio-slurry, and
their accumulation in farm soils should be monitored and avoided.
4.2. Environmentally sound sitting of CAFOs
The livestock and poultry industry in China has been expanding
rapidly over the past several decades, with little government guidance
and planning on the sitting of CAFOs. Due to the large amount of
manure and liquid waste discharged, the carrying capacity of local
environment can be far exceeded in the areas crowded with CAFOs. To
be close to the consumers, CAFOs are typically developed in the rural
areas not quite far away from the large urban centers. Unfortunately,
their locations are often chosen based on “conveniences” and “com-
promises” (i.e., near villages with road access, but not too close to bring
the nuisances of odors or insects to the neighborhoods) rather than
environmental considerations (Ellis and Turner, 2007). A national
survey in 2003 found over 90% of the CAFOs in China had been con-
structed without conducting environmental impact assessment (EIA)
(Wang, 2003), while the situation has not been improved much since
then. Appropriate zoning plan should be developed for CAFOs based on
the need of environmental protection and the long-term development of
animal agriculture. They should be prohibited in drinking water source
protection areas, while mandatory distances between CAFOs and water
bodies, as well as the dense residential population should be required
Y. Hu et al.
even in the permitted zones. In addition, CAFOs should not be allowed
in the areas prone to flooding or those with shallow groundwater tables
to avoid contamination of surface water and groundwater. The en-
vironmental impacts of CAFOs should also be closely monitored, and
animal farming should be restricted when significant deterioration in
environmental quality occurs. These measures can help ensure that the
environmental impacts of CAFOs are well contained, and the long-term
operation of CAFOs does not cause significant environmental de-
gradation.
Besides compliance with the EIA requirements, CAFOs should be
developed with full considerations of the potential market demand,
feed supply, transportation, and availability of manure disposal options.
In particular, it is important to site CAFOs near rural mass transporta-
tion routes to ensure sufficient areas of farmlands are within reach to
assimilate the large volumes of animal waste generated. Reducing the
distance of transportation can lower the disposal cost and facilitate the
recycling of nutrients in animal waste. Meanwhile, the proper rate of
land application is critical for effective use of manure and compost and
protection of the environment. Guidelines on the application rate of
animal waste should be established based on the geographical setting of
farmlands, the crops cultivated, and the animal species, which can help
ensure effective assimilation of the nutrients in the animal waste.
Overall, government regulations and coordination are needed to guide
the healthy growth of industrial livestock and poultry production by
limiting the number and scale of CAFOs, as well as their geographical
distributions, in accordance with the market demand, environmental
carrying capacity, and resource supply.
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Environment International 107 (2017) 111–130
Fig. 5. Basic treatment processes for wastewater
and manure from CAFOs according to the
Technical Specifications for Pollution Treatment
Projects of Livestock and Poultry Farms (MEP,
2009). Animal waste from farms with over 2000
feeder pigs or equivalent numbers of other ani-
mals should be treated with Scheme I or II, while
Scheme III should be adopted for farms with over
10,000 feeder pigs or equivalent numbers of
other animals. Schemes I and II can be adopted
only when the animal farms are not located in
environmentally sensitive areas, the environ-
mental capacity is large, far away from urban
centers with demand for energy, and sufficient
lands are available to assimilate the digester
sludge and liquid. Scheme I is not suitable for
animal farms with dry manure removal, in which
case the dry manure should be treated by aerobic
composting.
4.3. Strengthening waste discharge oversight and enforcement
With emissions of air pollutants, and discharges of liquid and solid
animal waste, CAFOs are important point source polluters in rural
areas. The Chinese government has developed a series of regulations
and technical guidelines targeting the animal agriculture, including the
Livestock and Poultry Industry Pollution Control Regulations (SEPA,
2001) and the Discharge Standard of Pollutants for Livestock and
Poultry Breeding (MEP, 2003). CAFOs are also required to obtain per-
mits for discharges in the areas where pollution caps have been set. The
Regulation on Prevention and Control of Pollution from Large Scale
Raising of Livestock and Poultry (SC, 2013) issued in 2013 further re-
quired all CAFOs to construct storage and treatment facilities for their
wastewater and manure.
Despite the existence of regulations, significant fractions of CAFOs,
particularly the mid- and small-scale ones, still do not have any pol-
lution control measures beyond storage lagoons and composts. Laws
and regulations on environmental protection are often poorly im-
plemented and enforced at the local level in China due to a range of
factors, such as lack of political will, insufficient authority, corruption,
as well as difficulty in compliance monitoring (Cheng and Hu, 2010,
2012; Hu and Cheng, 2013b). Therefore, besides enhanced monitoring
on pollutant discharges and manure-handling practices of CAFOs, im-
proved government oversight and enforcement on the local level are
necessary to curb the pollution caused by wastewater and waste from
CAFOs (Centner, 2006). Furthermore, efforts should be made to im-
prove the transparency and accountability of regulation enforcement,
Y. Hu et al.
while proper financial instrument can facilitate the adoption of treat-
ment technologies by the CAFOs. In addition, to minimize the en-
vironmental impacts of spills during manure handling and disposal,
overflow and runoff from storage lagoons or flooding events, CAFOs
should also be required to develop and follow incident response plans.
4.4. Developing integrated farming systems
CAFOs depend on commercial feed and generate large volumes of
manure that cannot be effectively absorbed by the surrounding farm-
lands. In contrast, family farming is essentially a livestock-crop system,
in which crop and/or crop residues grown on farmlands are used to feed
the livestock and the animal manure is recycled to fertilize the lands. In
such integrated farming systems, the outputs (typically by-products) of
one production sub-system are used as inputs by another one. However,
the increased separation of crop and livestock production with specia-
lized farms, together with the increased availability of chemical ferti-
lizers at relatively low costs, has caused declines in the use of animal
manure, and even dumping of animal manure due to the associated
high transportation costs (Yang et al., 2004). It is necessary to renew
the development of integrated farming systems to improve the sus-
tainability of animal agriculture, particularly in south China, where
dense river networks are available for developing fish ponds. Livestock-
fish integration provides a less land-demanding alternative to direct
land application of manure. Due to their higher microbial activity, pond
ecosystems have much greater assimilating capacity than farmlands,
particularly in the tropical and subtropical climate zones. The nutrient-
rich manure is decomposed by microorganisms and ultimately con-
verted to digestible, protein-rich, live food for the fish in the ponds,
while the spilled and partially digested feed can also be directly con-
sumed by the fish (Fig. S3). In livestock-fish integration, polyculture of
fish species at different trophic levels is key to efficient organic matter
recycling (Csavas, 1992). In such treatment systems, fresh manure can
be discharged directly into the fish ponds next to CAFOs, which elim-
inates the need for additional processing and transportation, while the
bio-slurry from biogas digesters can also be applied. By using the pond
silt as a fertilizer in the production of fodder crops, livestock produc-
tion, fish farming, and crop cultivation can be integrated. As a result,
materials, and energy to a less extent, can be recycled efficiently in
well-managed integrated livestock-fish-crop systems.
It should be noted that the main feature of integrated farming sys-
tems is disposal of animal manure, instead of efficient nutrient re-
cycling. The fish yield could only recover around 15% of the nitrogen
input in manure-loaded ponds, while over 80% of the nitrogen could be
immobilized in the sediment or lost to air (e.g., as N2) through bacterial
nitrification and denitrification (Csavas, 1992). Except the supplement
feed derived from the crops grown on farmlands fertilized by the pond
silt, the livestock do not benefit much from being around the fish ponds.
Safe processing of manure from pigs, poultry, and ruminants in fish
ponds has been demonstrated in many countries, mostly in Asia
(Csavas, 1992; NACA, 1989). The constant output of manure from C-
AFOs can be managed by fish ponds of proper sizes with fish species
efficient at food harvesting. Meanwhile, attention should be paid to
ensure the quality and safety of the fish raised to safeguard consumers'
health. This entails restricting the inputs of antimicrobials and heavy
metals with the manure, which ultimately relies on minimizing their
uses in livestock and poultry production, as discussed in the subsequent
section.
4.5. Controlling the use of veterinary drugs and feed additives
To better understand the environmental impacts and public health
risks of veterinary drugs and feed additives used in animal farming, the
fate and transport of these compounds and their metabolites in soils,
surface water, and groundwater need to be studied, while the effect of
their interactions on the ecosystem and public health should also be
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Environment International 107 (2017) 111–130
systematically investigated. One of the main causes for the develop-
ment of AMR in CAFOs is the indiscriminate use of antimicrobials to
compensate for the poor production practices and to promote animal
growth. Phasing out the use of antimicrobials as animal growth pro-
moters can effectively reduce the environmental load of ARGs, as has
been observed in the European countries (e.g., Sweden and Denmark)
(Clark et al., 2012; Marshall and Levy, 2011). Following the ban on the
use of antimicrobials for growth promotion adopted in European
countries, China phased out the non-therapeutic use of 150 anti-
microbial products in food animal production and made the veterinary
use of a total of 227 drugs only available by prescription in March 2014
(MOA, 2013a, 2013b). This is an important step in the country's efforts
on improving the safety of animal food products and curbing the
emergence of AMR in animal husbandry (Hu and Cheng, 2014, 2015).
Instead of the routine use of antimicrobials, proper vaccination can help
prevent the occurrence of common infectious diseases, while probiotics
can strengthen the immune system of farmed animals (Clark et al.,
2012). In addition, improving the sanitary conditions and reducing
animal over-crowding, along with good nutrition, can significantly re-
duce the occurrence and spread of infectious diseases in CAFOs (Hu and
Cheng, 2016; Jordan, 2013). With the health and well-being of farmed
animals maintained by good health management practices, anti-
microbials would only be necessary to treat acute infections occasion-
ally, significantly lowering the consumption of antimicrobials in animal
husbandry.
In addition to antimicrobials, synthetic growth hormones are also
widely used in CAFOs to promote growth of farmed animals, particular
beef cattle and sheep. These steroid hormone drugs are effective at
increasing the growth rates and feed efficiency of food-producing ani-
mals. Nonetheless, controversies have arisen from the use of these
compounds, as they can cause endocrine-disrupting effect on aquatic
organisms once released into the environment, while their residues in
animal food products can bring potentially adverse effects on human
health. The use of hormonal growth promoters was approved in the U.S.
in the 1950s, and the U.S. government has insisted that their residues in
meat and meat products pose no threat to human health (Johnson,
2015). On the other hand, the European Union (EU) has banned the use
of synthetic hormones and restricted natural hormones to therapeutic
use only in livestock production, out of concerns on the potential effects
to public health from these compounds and their metabolites, since
1981 (EC, 1999; Stephany, 2001). Although there are insufficient long-
term epidemiological data on exposure to hormone residues in animal
food products, the environmental risk of hormonal growth promoters
has been relatively well understood. In China's recent ban on non-
therapeutic use of veterinary drugs, a total of 9 growth hormone pro-
ducts were made only available for use on animals by veterinarian
prescription, along with the antimicrobials (MOA, 2013a, 2013b). It is
worth noting that the banned list does not include all the major hor-
monal growth promoters used in animal farming. To better protect
public health and the environment, efforts on controlling the use of
hormonal growth promoters in animal farming should be stepped up.
Deemed essential for many physiological processes in animals, trace
metals are often supplemented in animal feed, while most parts of them
are excreted by the animals. Because of their non-degradability and
toxicity, long-term disposal of manure can result in elevated levels of
heavy metals in surface soils. It is important to reduce the contents of
trace elements in the feed to levels just sufficient to maintain animal
health, which can be achieved by strict regulations and close super-
vision on feed products. The use of phenylarsenicals as feed additives in
swine and poultry production has been banned in many developing
countries, while they are still legally and widely used in China (X. Liu
et al., 2013). Degradation of these compounds in the environment re-
leases inorganic arsenic (Mangalgiri et al., 2015; Wang and Cheng,
2015; Xie et al., 2016), while their use as feed additives also increases
the levels of residual arsenic species in chicken tissues, which pose
cancer risk to the consumers (Hu et al., 2017; Nachman et al., 2013).
Y. Hu et al. Environment International 107 (2017) 111–130

Table 5
Comparison of the general performance of CAFOs with that of family farms and “free range” farms in livestock and poultry production.

Category CAFOs Family farms and “free range” farms

Productivity and economic
efficiency
Demand on land resource
Disease prevention and
epidemic control
Animal welfare
Supervision
Food safety
Environmental impact
Large numbers of animals, almost always a single species, are confined
in specialized buildings or open-air pens, which increases the efficiency
of meat and dairy production.
The overall economic efficiency of CAFOs is higher than most of the
smaller, non-confinement operations.
CAFOs are easier to manage with consistency in efficiency.
Compared to the traditional family-based and “free range” farming
operations, CAFOs have lower production cost and higher business
profits with less resources consumption.
Large quantities of harvested feed is required for the large numbers of
animals raised in CAFOs, and substantial areas of land are needed to
grow the feed;
Due to the high quality of the feed, less feed is required for meat
production compared to grazing on per animal basis.
The crowded, and often unsanitary, conditions in CAFOs increase the
chance of transmission of pathogens among animals, thus antimicrobials
are used routinely to prevent disease (and for growth promotion as
well).
Farm-to-farm transmission of diseases is limited for CAFOs as the
animals are kept in enclosed systems and the CAFOs are separated from
each other over relatively long distances.
Vaccination and culling of diseased animals can be carried out
efficiently in cases of epidemic outbreaks.
Thousands of or more animals are raised in extremely crowded facilities
with limited movement, often with little access to sunlight and fresh air,
and they have high levels of stress.
Farmed animals are sometimes subjected to inhumane treatment by
CAFO workers.
It is easier to supervise the management of animals and the production
of animal food products in CAFOs.
The use of veterinary drugs and feed additives can be monitored
efficiently in CAFOs.
Animal loss resulting from diseases can be easily tracked in CAFOs,
which can help ensure the sanitary disposal of livestock and poultry
carcasses.
Formulated animal feed and feed additives are used to feed animals in
CAFOs, and antimicrobials and hormones are routinely administered to
them, which may result in animal food products with residues of various
drugs and feed additives.
The animal food products are expected to be safe because the use of
veterinary drugs and feed additives is standardized, and drug
withdrawal periods are closely followed.
Large volumes of water are typically required for cleaning of animal
waste in CAFOs.
CAFOs produce air emissions, and large volumes of wastewater and
manure, which can pollute surface water, soils, and groundwater.
The large volumes of animal waste generated cannot be efficiently
assimilated by local farmlands, while it is economically unattractive to
transport the manure produced from CAFOs to distant farmlands.
Having a few large CAFOs instead of many smaller farms can provide
Such farms often do not adopt the advanced technologies and thus lack
economic advantages.
Even though well managed small farms can be cost-effective and may
produce animals at costs lower than CAFOs, their economic efficiency
varies significantly.
Large areas of pasture lands are required for “free range” animal
production;
There is not enough land available for raising all animals in “free range”
farms.
Animals are raised in less crowded facilities with healthier conditions or
on pasture, and they have lower chance of transmitting diseases
compared to those raised in CAFOs.
The exposure to soil, water, vegetation, as well as other animal species,
which can potentially be disease carriers, and their waste, could
increase the rates of animal infections by virus (e.g., avian influenza),
bacteria (e.g., Salmonella), and parasites (e.g., Trichinella) in family and
“free range” farms.
Most parasites need to infect different host species at different stages of
development, and have greater chance of completing their life cycle in
the natural environment. Thus, the prevalence of parasites is higher in
“free range” animals compared to those raised in CAFOs.
Lack of rotational grazing practices or insufficient attention paid to
disease control measures in family and “free range” farms, where it is
more difficult to carry out pathogen eradication compared to CAFOs,
can increase the risk of parasite or pathogen buildup.
Compared to the animals farmed in CAFOs, which are confined indoors
and are medicated to prevent diseases, livestock and poultry raised in
family and “free range” settings without administration of preventive
antimicrobials can have higher rates of pathogen infections.
Animals raised in numerous family farms and “free range” farms can be
challenging for disease prevention and monitoring, and pose challenges
in vaccination and culling.
Farm-to-farm transmission of diseases can be a problem because of the
greater chances of direct and indirect contacts between animals from
different farms in family-based and “free range” farming.
Animals are typically raised with freedom of movement and access to
sunlight and fresh air, which is beneficial for their stress levels.
Nonetheless, measures (e.g., access to overhead cover for chicken) are
necessary for protection against the presence of predators in the
surroundings and reduction of regular fear reactions.
Animals are typically treated humanely and are allowed to behave
naturally.
Violation of animal welfare regulations may occur due to the lack of
supervision on such small farms.
Disease prevalence can be higher in the animals raised in family farms
and “free range” farms due to insufficient attention paid to animal
health by the owners.
The practices in numerous family farms and “free range” farms are
difficult to supervise.
Animal mortality and disposal of diseased animals are also difficult to
monitor, which could potentially allow occurrence of illegal animal
carcass disposal.
Animals are generally raised without the use of antimicrobials, growth
hormones, and other additives in these farms.
Due to lack of oversight, some producers may misuse and overuse
veterinary drugs, and ignore the requirement of drug withdrawal
periods, resulting in excessive residues in the animal food products.
“Free range” animals require less water for cleaning.
The relatively small amount of animal waste produced can be effectively
used as a soil fertilizer and absorbed by local farmlands.
Over-grazing by “free range” animals can cause decline in land quality.
Although the pollution brought by individual family farms and “free
range” farms is low, the collective impacts from many of them can be
considerable.
Manure disposal can still be a problem if too many family farms and
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Table 5 (continued)

Category CAFOs Family farms and “free range” farms

opportunities for environmentally sound sitting of these farms.
Pollution control Wastewater and manure generated from CAFOs can be managed
efficiently and effectively when suitable measures are taken.
CAFOs can afford installation of pollution control technologies, which
are also more cost-effective for them compared to smaller farms.
Pollutant discharges and pollution control in CAFOs are easy to monitor
and supervise.
Impacts on rural Feed is typically purchased and shipped to CAFOs, and the products are
communities marketed primarily to urban residents.
CAFOs hire as few workers as possible.
CAFOs can drive family farms out of business.
CAFOs may cause significant damage to local environment.
Human health Close contact with the large number of animals in CAFOs and their
waste cause health problems to the workers.
Animals raised in CAFOs generally have no direct contact with the
general population, except the CAFO workers, thus the chance for
transmission of diseases to the general population is low.
Air emissions from CAFOs contain volatile pollutants and bioaerosols,
which can lead to higher rates of respiratory and other diseases in the
neighboring communities.
The routine use of antimicrobials in CAFOs leads to development of
AMR, which can potentially spread to humans.
Sustainability CAFOs are resource-intensive and unsustainable.
Animal diet is primarily derived from corn and soy produced elsewhere,
and the operation is not integrated with crop production.
“free range” farms are densely distributed, while the sitting for some of
these farms is unlikely to be environmentally sound, which can result in
easy occurrence of environmental pollution.
Due to their low profit margins, family farms and “free range” farms are
reluctant to invest in pollution control measures and implementation of
pollution control technologies may not be cost-effective.
Monitoring of pollutant discharges from large number of such small
farms is difficult.
Family farms support local economies through purchasing raw materials
and marketing their products locally.
Family-based and “free range” farming are important ways of
alleviating rural poverty and provide employment opportunities.
Owners of family farms and “free range” farms are part of the rural
communities, and these farms contribute to rural resilience.
Farmers are subjected to less health hazards in family farms and “free
range” farms compared CAFOs due to the much smaller number of
animals raised.
Transmission of diseases to the general population can be a problem
because of the greater chances of direct and indirect contacts between
animals and humans.
Due to the much smaller number of animals raised, air emissions and
animal waste released from such farms pose lower health risk compared
to those from CAFOs.
Animals are produced under ecologically more sustainable and non-
intensive conditions.
Food animal production can be effectively integrated with crop
production by feeding animals with feed grown on neighboring farms
and returning the nutrients contained in the animal manure to the fields
where the feed is gown.

Thus, China should also develop an action plan to gradually phase out waste (Hu and Cheng, 2014; Pruden et al., 2013).
the use of phenylarsenicals in the swine and poultry production.
Overall, controlling the uses of veterinary drugs and feed additives
in CAFOs is expected to significantly reduce the potentials for the de- 4.7. Sanitary disposal of animal carcasses
velopment of AMR in animal husbandry, and lower the residues of
drugs and heavy metals in animal food products and the associated food Loss of farmed animals is almost unavoidable in livestock and
safety risk. Furthermore, the animal waste will be much more benign poultry CAFOs, and management of on-farm animal mortalities is an
for fertilizing farmlands with or without treatment, and thus facilitate important issue. Improper disposal of the carcasses of dead animals,
recycling of the nutrients. particularly those died of infectious diseases, can create a nuisance,
adversely impact the quality of surface water and groundwater, and
spread disease. In March 2013, over 16000 dead pigs were found
4.6. Disinfection of animal waste
drifting in the Huangpu River of Shanghai, which is a major source for
drinking water supply of the city (Liu and Jiang, 2013). Animal pro-
Depending on the treatment conditions and duration, significant
ducers are required to cremate (for those died from anthrax) or properly
fractions of antimicrobials in animal waste could be degraded during
bury the animal carcasses in disposal sites, according to the Animal
storage in surface lagoons, composting (primarily during the thermo-
Epidemic Prevention Law of China (NPCSC, 1997). They could receive a
philic phase), or fermentation in anaerobic digesters (Mohring et al.,
subsidy of 80 Yuan RMB for each dead pig disposed of, which is typi-
2009; Pei et al., 2007; Wang et al., 2012; Wu et al., 2010). Meanwhile,
cally below the actual disposal cost (Wei et al., 2015). As a result, the
the antimicrobials not amenable to biodegradation could persist, fos-
producers often chose to sell the diseased animals to meat traders,
tering development of AMR (Larson, 2015). Meanwhile, survival of
which was illegal but did not receive enough government scrutiny until
many bacteria and persistence of ARGs in the animal waste during
recently. Due to the crack-down on such illegal activities in the up-
storage (in surface lagoons) and biological treatment (composting and
stream Zhejiang province, the operators of swine CAFOs discarded their
anaerobic digestion) have been well documented (e.g., Johnsen et al.,
dead pigs directly into adjacent waterways, which ultimately drifted to
2011; McKinney et al., 2010; Sharma et al., 2009; Storteboom et al.,
the Huangpu River in Shanghai. This scandal brought significant public
2007; Wang et al., 2012). Once released into the environment with the
attention on the potential impact of industrial animal farming on public
animal waste, these bacteria and ARGs could also survive in natural
health and welfare, and highlighted the need for effective supervision
aquatic systems and soils for long periods of time (Levy and Marshall,
and enforcement of laws and regulations for public health and animal
2004; Martínez, 2008; Mole, 2013). Thus, preventing the resistant
health on the local level in China (Liu and Jiang, 2013). Overall,
bacteria and ARGs in animal waste from spreading to the environ-
prompt disposal of routine animal mortalities can minimize the threats
mental compartments is important for containing their risks to public
to the environment and public health, while timely reporting of animal
health. Limited research has been conducted on disinfection of resistant
death of unexplained causes or catastrophic mortalities to local animal
bacteria and the ARGs in animal waste generated from CAFOs
health authorities is necessary to prevent spreading of infectious dis-
(Macauley et al., 2006; McKinney and Pruden, 2012; Wang et al.,
eases.
2012). It is imperative to develop and implement cost-effective disin-
fection technologies, such as chlorination, ozonation, and UV irradia-
tion, to sterilize the resistant bacteria and destruct the ARGs in animal

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5. Towards sustainable animal farming in China
As a result of the increasing awareness of the environmental and
public health challenges of industrial livestock and poultry production,
its benefits and risks have been under debate in recent years. In general,
family farms and “free range” farms are associated with less food safety
and environmental concerns compared to CAFOs, although this might
partially result from the lack of insight on the activities and practices of
these farms and their relatively small and localized impacts. On the
other hand, such farms are generally inefficient, and they cannot meet
the steadily growing demands for meat and dairy products (Table 5).
Furthermore, the collective environmental impacts of numerous small
farms can still be significant, although they would be more difficult to
be assessed compared to those of a few CAFOs. China does not have
enough land resources to develop numerous small-scale animal farms to
meet the growing demands for animal food products, while it can be
very challenging to monitor and supervise them with respect to disease
prevention, animal welfare, and pollution control (Table 5). As a result,
the central and local governments have actively promoted the devel-
opment of industrial-scale animal farms with high-value breeds.
Animal farming is a pillar industry of the rural economy and con-
sistently accounts for over 30% of the agricultural output in China
(MEP and MOA, 2012). The demand for animal food products is ex-
pected to keep rising with the continued strong economic growth and
the ongoing urbanization. Meanwhile, productivity improvement has
become increasingly more important for livestock producers under the
constraints of land availability and rising feed costs. With high eco-
nomic efficiency and relatively low resources consumption, industrial
animal farming provides a solution to meet the growing demand for
animal food products. Nonetheless, CAFOs are not the only way of
producing animal products at reasonable costs, as many medium-sized
animal feeding operations can be as cost effective as the average large
CAFOs (Gurian-Sherman, 2008). On the other hand, despite of the
challenges of animal waste disposal and the releases of pollutants that
may exceed the carrying capacity of local environment, having a few
large CAFOs instead of many smaller ones can provide opportunities for
environmentally sound sitting of these farms, while the increased se-
paration between CAFOs also reduces the transmission of infectious
diseases. It is not possible to conclude unambiguously that collectively,
the risks from many small-scale farms raising equivalent numbers of
livestock and poultry would be less than a few large CAFOs. In fact,
family farms, “free range” farms, small- and mid-sized farms, and large
CAFOs all have their own strengths, weaknesses, opportunities, and
challenges, and each of these farming systems has its market potential
given an environment and a set of resources. There are significant
spatial variations in population density and economy development
across China. For example, the 11 coastal provinces, which cover 15%
of the country's land area, host about 40% of the total population and
produce roughly 2/3 of the gross domestic product (Cheng et al., 2009).
CAFOs appear to be a logical option to meet the large and growing
demand for animal food products in these regions with increasingly
restrained land resource. For the rest parts of the country, the sizes of
animal farms should be determined based on local supply of feed crop,
market demand, and agricultural production, and priority should be
given to the farms that can achieve efficient assimilation of the animal
waste and recycling of the nutrients.
With potentially significant environmental and public health im-
pacts, authorities should ensure that all animal farms are maintained
and operated properly, and that their emissions and discharges cause
little harm to the local environment and the surrounding communities
(Hribar, 2010). Furthermore, measures should be taken to contain and
actively mitigate the impacts of CAFOs, or even smaller animal farms,
on the environment and public health. China can benefit from the ex-
periences of the developed countries on dealing with some of the
pressing environmental and public health issues caused by the multi-
plying CAFOs. For example, U.S. has well established best management
126
Environment International 107 (2017) 111–130
practices for the production areas and the land application areas of C-
AFOs, which minimizes their negative impacts on the environment. EU
countries have been proactive on controlling the use of veterinary an-
timicrobials and hormones in livestock production, which can help
China on developing guidelines for veterinary drug use while protecting
public and animal health and welfare.
A new, sustainable paradigm of livestock and poultry production,
which is not only economically viable, but also ecologically sound and
socially responsible, should be developed in China. When possible, food
animal production should be effectively integrated with crop produc-
tion by feeding animals with the feed grown on neighboring farms. The
wastewater and solid waste should be effectively treated, while the
nutrients contained in the manure should be returned to the soil to
recycle them back into the crops. Animals should be raised under hy-
gienic conditions, following good health management practices. Such
conditions eliminate the need of routine antimicrobial use, even though
antimicrobials are still necessary to treat acute infections. Trace ele-
ments are supplemented at just the necessary levels, while no anti-
microbial or hormonal growth promoters are used. As the meat and
dairy products produced in such farms are free from the antimicrobial
and hormone concerns, they can be more profitable than those from the
traditional CAFOs. Such livestock and poultry production practices are
crucial for the food security and safety in China, while bringing few
environmental issues and public health concerns.
Globally, consumption of animal-based foods has significantly ex-
ceeded that of other groups of foods since the 1960s (FAO, 2009), and
such transition towards a meat-heavy diet has noteworthy public health
implications (Popkin and Du, 2003; Walker et al., 2005). It has been
well documented that animal-based foods increase the risk of cancer
while plant-based ones have the opposite effect (Chang-Claude et al.,
1992; Thorogood et al., 1994), and increased consumption of animal-
based foods results in significant rises of chronic diseases, including
cardiovascular diseases and diabetes (Popkin and Du, 2003; Walker
et al., 2005). The more affluent population subgroups in China are
adopting energy-dense diets high in animal protein and fat similar to
those in the developed countries. A survey by the Chinese Center for
Disease Control and Prevention showed that nearly 30% of Chinese
population consumed over 100 g of meat products daily, which is much
higher than the recommended daily consumption guidelines of 75 and
50 g for men and women, respectively (Shan, 2014). This already
brought obvious public health consequences in the country: > 30% of
the adult population were overweight and approximately 260 million
people were suffering some chronic diseases, including hypertension
and diabetes, by 2010 (Shan, 2014). As China is in the course of nu-
trition transition towards animal-based foods, promoting healthy food
consumption to increase public awareness of nutrition and avoid over-
consumption of meat is important for public health authority in China.
Ultimately, healthy diets, which are based predominantly on plant
source foods, will not only improve public health through lowering the
risk of diseases associated with excessive consumption of animal-based
foods (Akhtar et al., 2009; Ornish et al., 1998), but also significantly
reduce the need for industrial animal farming, and correspondingly, the
associated environmental and public health risks.
Acknowledgement
The authors thank the anonymous reviewers for their valuable in-
sights and advice, as well as helpful suggestions for improvement on an
earlier version of this manuscript. This work was supported in parts by
the Natural Science Foundation of China (Grant Nos. 41673089 and
41472324), the National Key Research and Development Program of
China (2016YFD0800302), and the National Program for Support of
Top-notch Young Professionals.
Y. Hu et al. Environment International 107 (2017) 111–130

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