C 2015 Poultry Science Association, Inc.

Antibiotic-free poultry production: Is it sustainable?

Hector M. Cervantes1

Phibro Animal Health Corporation, Glenpointe Centre East, 3rd Fl, 300 Frank W. Burr
Blvd., Ste. 21, Teaneck, NJ 07666-6712

Primary Audience: Veterinarians, Nutritionists, Live Production Managers, Producers

SUMMARY
There is growing acknowledgement that use of antibiotics in people is the primary driver of
antibiotic-resistant infections in humans [1, 7–9], however, antibiotic-free production of poultry
has become increasingly popular. Consumer perception is that antibiotic-free produced poultry
is superior to conventionally raised poultry in spite of a lack of supporting scientific data [2]. A
widely accepted definition of antibiotic-free poultry in the United States is that there is “no use
of antibiotics (including ionophore anticoccidials) at the farm.” That means that coccidiosis and
necrotic enteritis prevention must rely on synthetic or “chemical” anticoccidials, or on live coc-
cidiosis vaccines, or on rotations between drugs and vaccines. The problem with this approach is
that chemical anticoccidials (with the exception of nicarbazin) build coccidial resistance much
quicker than ionophores and must be rested for a prolonged period of time. Further, there are
limited numbers of anticoccidials of this class on the market. Moreover, unlike the ionophores,
the chemicals do not have an antibiotic effect that aids in the prevention of necrotic enteritis and
typically nicarbazin is only used during the cool months. Additionally, live coccidiosis vaccines
induce immunity by invading, replicating, and cycling through the intestines. The coccidial
infection, therefore, damages the intestinal epithelium and predisposes the birds to necrotic
enteritis [3]. These intestinal health problems lead to bird welfare issues that must be addressed
in the antibiotic-free production system. Likewise, it is generally acknowledged that production
efficiency (weight gain, feed conversion ratio, mortality and yield) is adversely impacted in the
antibiotic-free production system [4]. Thus, antibiotic-free production results in a greater car-
bon footprint and is less efficient [5, 6]. Companies considering raising antibiotic-free poultry
must be aware of the expected adverse effects on bird health, production efficiency, and cost.

Key words: Antibiotics, Antibiotic-Free, ABF, Poultry Production

2015 J. Appl. Poult. Res. 24:91–97
http://dx.doi.org/10.3382/japr/pfv006

INTRODUCTION Trade Association, sales of antibiotic-free (ABF)

There is little convincing scientific evidence
that the use of antibiotics in food-producing
animals is contributing to the antibiotic resis-
tance issues that are relevant to human medicine
[1, 7–9]. However, public perception in first-
world countries suggests that consumers believe
this to be true. According to the U.S. Organic
1
Corresponding author: Hector.Cervantes@pahc.com
organic foods have grown at a rate of 20% per
year since 1990. This is in spite of wider recogni-
tion that antibiotic resistance in humans is caused
by antibiotic use in humans and not in food-
producing animals. In a recent document entitled
“UK Five Year Antimicrobial Resistance Strat-
egy 2013 to 2018” [1], the report states “Increas-
ing scientific evidence suggests that the clinical
issues with antimicrobial resistance that we face
in human medicine are primarily the result of
92
antibiotic use in people, rather than the use of
antibiotics in animals.” This recent admission
is in agreement with previous manuscripts that
have shown that antibiotic resistance in a com-
munity closely matches antibiotic use in people
from the same community [10]. Another study
showed that antibiotic use in food-producing an-
imals in a worst case scenario contributes less
than 1% to the overall antibiotic resistance prob-
lem confronted by the medical profession [11].
Trends in consumer preference like buying
ABF products are based largely on perception
rather than scientific facts [12]. For example,
most consumers do not realize that all chicken
meat is ABF or contain levels below tolerances
considered safe for humans. Regulatory agen-
cies like the USDA-FSIS for decades have rou-
tinely monitored drug residues by sampling and
testing tissues to ensure that no drug residues
(including antibiotics) are found to be above the
tolerance or maximum residue limit (MRL) es-
tablished for each drug [13, 14]. The poultry
industry in particular has an outstanding record
of compliance with drug withdrawal periods and
residue tolerances [13, 14]. A recent report en-
titled “The Organic Marketing Report” written
by Academics Review, an independent interna-
tional organization founded by professors from
the University of Illinois and the University of
Melbourne, states that the 25 years of fast growth
by the organic food industry has been achieved
through fear and deception [15]. Specifically,
the report also indicates that more transparency
is needed as the USDA organic seal says nothing
about food safety, yet many consumers mistak-
enly associate it with “healthier”, “safer,” and
“more nutritious” food [15].
An important aspect of ABF production is
the definition used or the requirements of the
food store or fast food chain being supplied by a
producer. For example, the definition of “no an-
tibiotics chicken” by the USDA-FSIS is “these
chickens have never been given antibiotics, in-
cluding in the egg.” In contrast, the USDA-FSIS
definition of organic chicken allows for antibi-
otic use in the egg and during the first day of
life of the chicks, the drug-free rule kicks in
the day after hatching. According to the USDA-
FSIS the label claim “raised without antibiotics”
(RWA) means “no antibiotics in their feed, wa-
ter, or injection including no ionophores” during
JAPR: Review Article
the birds’ life. This strict definition of ABF can
certainly make the growing of chickens and the
prevention and control of diseases much more
inefficient, expensive, and challenging.
CHALLENGES OF RAISING ABF
BIRDS
There are numerous challenges faced by com-
panies attempting to produce ABF birds [4, 16,
17], these typically involve one or more of the
following:
1) Production challenges (raising ABF, RWA,
organic, split birds or 100% ABF, separate
processing plants, etc.)
2) Management challenges (reducing stocking
density, increasing down-time, cleaning-out
more frequently, maintaining ideal temper-
ature, keeping strict biosecurity, reducing
stress, breed selection, etc.)
3) Health challenges (increased enteric and
systemic diseases)
4) Animal welfare challenges (establish when
and how to treat, option to divert to conven-
tional program, etc.)
For the purpose of this manuscript, we will
concentrate on the main health challenges that
are likely to result from a company making the
decision to grow a percentage of their birds as
ABF.
HEALTH CHALLENGES
While some alternative compounds have spe-
cific physiological, immunological, and/or bac-
teriostatic effects in the intestine, none (to date)
convey the range and extent of the effects of
the antibiotics [18]. Other researchers have sug-
gested that the unique and highly reproducible
effects of the in-feed antibiotics may be due to the
prevention of immunologic stress [19] or their
anti-inflammatory effect [20] rather than their
antimicrobial effect, and this should be consid-
ered when searching for new compounds to be
used as replacements. A producer raising ABF
birds should be prepared to deal with a variety
of health challenges that for simplification pur-
poses can be divided into two main groups:
CERVANTES: SUSTAINABILITY OF ABF POULTRY PRODUCTION
1) Enteric disease challenges.
2) Systemic disease challenges.
ENTERIC DISEASE CHALLENGES
The main challenges faced by producers of
ABF chickens or turkeys are undoubtedly re-
lated to intestinal health, and more specifically
to the prevention and control of coccidiosis and
necrotic enteritis (NE). The prevention of these
two diseases is intimately linked as intestinal le-
sions induced by coccidiosis (especially E. max-
ima), whether due to field challenge or live coc-
cidiosis vaccine are a well-known predisposing
factor for clinical outbreaks of NE [3].
Removing ionophore anticoccidials and an-
tibiotic feed additives is certain to cause prob-
lems in controlling coccidial parasites and
bacterial organisms, in particular, Clostridium
perfringens, the causative agent of NE in chick-
ens and turkeys. Interestingly, both coccidiosis
and NE in their subclinical forms, are widely
recognized as the most prevalent and costly dis-
eases of broiler chickens and turkeys [21–23].
Without use of ionophores in a coccidial pre-
vention program, control of coccidiosis will have
to be achieved exclusively with synthetic “chem-
ical” anticoccidials or live coccidiosis vaccines
or, more than likely, rotations between the two.
The problem of coccidiosis prevention
through the use of chemical anticoccidials, is
that with the exception of nicarbazin, a synthetic
anticoccidial that has been successfully used to
prevent coccidiosis in chickens since 1955 [24],
the remaining anticoccidials are only highly ef-
fective for a limited period of time. They tend to
suppress coccidiosis almost completely and for
that reason they are more likely to select for a re-
sistant mutant population of parasites. Once the
parasites have developed resistance to the antic-
occidial, they are likely to remain resistant for a
long period, as there are not enough chemical an-
ticoccidials available to allow extended periods
without use of individual chemical products. In
addition, a well-known adverse interaction with
high environmental temperature [25] restricts the
use of nicarbazin to primarily the cooler months
of the year.
Live coccidiosis vaccines have been used in
rotations with chemical anticoccidials to seed the
93
chicken houses with vaccine strains of Eimeria
oocysts that are fully susceptible to all anticoc-
cidials [26]. However, the problem with the live
coccidiosis vaccines is that they induce immu-
nity by replicating and cycling a number of times
through the intestines. Along with the replica-
tion and cycling required to induce active im-
munity, the parasites also cause damage to the
epithelium of the intestinal tract and this predis-
poses the birds to outbreaks of NE caused by C.
perfringens type A, a bacteria normally present
in the hind gut of chickens. This is the main
reason for which live coccidiosis vaccines work
more effectively when an antibiotic feed additive
with good anticlostridial activity can be added to
the feed. Field experiences from integrators have
shown that Virginiamycin at 22 mg/kg has pro-
duced excellent results in preventing cases of
NE when live coccidiosis vaccines have been
used to prevent coccidiosis in chickens. This
may be related to Virginiamycin’s potent activ-
ity against C. perfringens as demonstrated by
having the lowest mean inhibitory concentra-
tion (MIC) among other antibiotic feed addi-
tives [27]. This could also be related to Virgini-
amycin’s unique structure, which as with other
streptogramins, is composed of two antibiotic
molecules that work synergistically and are less
likely to result in the development of resistance
[28, 29]. Unfortunately, the in-feed use of antibi-
otics like Virginiamycin is not an option avail-
able to producers of ABF chickens. Therefore
producers of ABF chickens have to rely on a
combination of strategies designed to minimize
the adverse effects on performance and intestinal
health resulting from the removal of antibiotic
feed additives and ionophore anticoccidials.
A variety of strategies have been used by pro-
ducers of ABF poultry to minimize the effects on
flock performance of removing antibiotics and
ionophores from the feed [16]. Table 1 presents
a summary of those strategies including the tar-
get or actions to be taken for each. Even when
all of these strategies are implemented, cases of
NE are still likely to occur at least in some cases.
If a flock breaks out with NE or coccidiosis,
it should be treated with an effective antibiotic
or anticoccidial, respectively, in order to reduce
mortality, morbidity, and unnecessary bird suf-
fering. Treatment should not be withheld or de-
layed even if it means the loss of ABF status
94
Table 1. Strategies used by producers of ABF poultry (adapted from P. Woodward, 2005).
STRATEGY:
Processing of feed to decrease bacterial load
Conversion to a vegetarian diet
Maintenance of dry litter
Sanitation of drinking water
Frequent disposition of mortality
Use of probiotics early in life
Coarser grinding of grain
Supplementation with whole grain or grit
Supplementation with essential oil extracts
Minimize non-protein nitrogen by formulating diets
based on digestible AAs
Use ingredients with more soluble fiber
Use highly digestible fats and starches
Minimize inclusion of ingredients like wheat, barley
and oats
Maintain proper electrolyte balance
Limit feed changes
Add exogenous enzymes
Maintain good management practices
Follow good biosecurity practices
and the corresponding economic consequences
associated with the change. Companies that pro-
duce both conventional and ABF birds and have
separate processing plants for each type of pro-
duction system, are in a better position to react
appropriately to disease outbreaks and channel
the treated flocks to the corresponding plant.
Although in some cases the use of alterna-
tives to in-feed antibiotics has helped in reducing
the problems associated with producing chick-
ens without antibiotics, the performance of these
flocks when raised at similar stocking densities
is usually below that of flocks raised conven-
tionally resulting in a higher cost of produc-
tion [4]. On average, this cost is approximately
20% higher than that of chickens raised con-
ventionally. In a paper from a symposium on
alternatives to raising broiler chickens without
antibiotics, a well respected poultry veterinar-
ian with many years of experience in producing
ABF chickens in the United States concluded
that although ABF and drug-free production is
feasible, it comes at a hefty cost to the producer
and the health of the birds [17]. After a large
number of alternatives to antibiotic feed addi-
tives ranging from prebiotics and probiotics to
live E. coli vaccines, oregano and organic acids
JAPR: Review Article
TARGET OR ACTIONS TO BE TAKEN:
<10 CFU after pelleting or <103 CFU at the farm
Minimize potential for clostridial contamination
Decrease stocking density, increase rate of
ventilation, increase depth of shavings, etc.
Minimize bacterial contamination
Prevent cannibalism and bacterial contamination
Establish a healthy intestinal microflora
Improve function of gizzard and digestion
Improve function of gizzard and digestion
Keep bacteria in check and improve gut health
Prevent bacterial proliferation
Prevent accumulation of insoluble fiber in the hind
gut
Favor good digestion, prevent NSPs from reaching
the hind gut
Reduce gut damage and subsequent necrotic
enteritis
Minimize flushing and feed passage
Minimize disturbances of gut microflora
Maximize extraction and digestion of nutrients,
minimize viscosity of digesta
Minimization of stress
Reduce the possibility of disease
were field tested, the author concluded that none
of them worked like an antibiotic feed additive
or were not cost effective [17].
SYSTEMIC DISEASE CHALLENGES
In both chickens and turkeys, septicemic bac-
terial infections are nearly always caused by
strains of Escherichia coli (E. coli), a bacteria
normally present in the intestinal tract of both
species [30]. In many cases E. coli is not a pri-
mary pathogen but rather an opportunistic one.
If the birds are stressed for any reason or their
immune system compromised, the E. coli bac-
teria can multiply and cause a systemic infec-
tion that typically results in mortality and gross
lesions characterized by the accumulation of a
fibrino-purulent exudate. In other cases the trig-
gering agent can be a viral respiratory disease
like Newcastle disease or infectious bronchitis
or a viral immunosuppressive disease like infec-
tious bursal disease, infectious anemia, Marek’s
disease of chickens, and hemorrhagic enteritis
of turkeys [30]. In many countries, mycoplasma
infections like those caused by M. gallisepticum
CERVANTES: SUSTAINABILITY OF ABF POULTRY PRODUCTION
or M. synoviae are the most common triggering
factors [30].
If birds experiencing an outbreak of colisep-
ticemia are left untreated, morbidity and mortal-
ity will increase, and these can be severe enough
to cause catastrophic losses to the producer. Re-
gardless of the cause, birds diagnosed with sys-
temic E. coli infection must be treated with
antibiotics to mitigate the disease and prevent
unnecessary bird suffering. Even when the dis-
ease is not as severe and the losses are mild,
untreated flocks carry a higher load of bacte-
ria into the processing plant, have lighter body
weights and generate more processing errors at
the processing plant resulting in higher levels of
bacterial contamination of the carcasses [31].
OTHER IMPORTANT
CONSIDERATIONS
Veterinarians may have a philosophical dis-
agreement with a policy of no use of antibiotics
to prevent or treat disease and relieve bird suffer-
ing. They will probably not endorse such policy
unless steps are taken to ensure that treatment is
not withheld from flocks that need it regardless
of the economic consequences for the company
involved in the production of the birds. Addi-
tionally, another philosophical problem is likely
to emerge when a professional is asked to sup-
port a system that is less efficient over benefits
that cannot be scientifically documented and are
only perceived as such by consumers that have
been influenced at times by misleading adver-
tisements [2, 15]. Therefore, the overall impact
of ABF production should be carefully consid-
ered before making a decision. The following is
a list of well-known and documented negative
aspects of production without antibiotics:
1) It is generally understood that there will be
a loss in performance [average daily gain,
feed conversion ratio (FCR), mortality and
yield] in flocks raised ABF [4]. In an effort
to minimize the loss of performance, many
companies will increase the floor space al-
lowance per bird placed, for example a
company growing conventional chickens at
0.23 m2 /bird (0.75 ft2 /bird) may increase it
to 0.27 m2 /bird (0.9 ft2 /bird). Therefore, in
95
order for a company to maintain the same
live weight output, it would have to feed
more tons of feed, build more farms and
poultry houses, keep the birds in the field
longer (reducing the number of placements
per year for the contract growers) or a com-
bination of these.
2) By feeding more tons of feed, the company
has to purchase or produce more ingredi-
ents, mix more tons of feed at the feed mill,
deliver more tons of feed to the farms, use
more drinking water for the flocks, and dis-
pose of more excreta and nutrients into the
environment [5, 6].
3) Because ABF production is less efficient,
the cost of producing a kg or lb of chicken
or turkey is higher and consequently con-
sumers have to pay more for chicken and
turkey meat. A 1999 study by the National
Academy of Sciences [32] estimated that
the cost of not using antibiotics would result
in an increased cost per person for poul-
try of between $1.36 to $2.76 per person,
when adjusted for inflation, and for today’s
United States population this would be an
additional cost of $604 to $1,224 million for
poultry alone. Moreover, low-income con-
sumers would be impacted disproportion-
ately by the higher cost of poultry and a
larger percentage of their disposable income
would have to be spent on food.
4) With the global trade and economy that ex-
ists today, food preference trends in one
country, like the United States or other
first-world nations may have adverse, unin-
tended consequences impacting the world’s
population in other countries. For example,
by making production of poultry less ef-
ficient, more cropland (a very scarce and
non-renewable resource) must be dedicated
to the production of additional feed ingre-
dients to make up for the loss in efficiency.
Taking more cropland and natural resources
(including water) from the environment to
maintain the same meat output is not a de-
sirable position in a world that is expected
to add 64 million people each year from
2015 to 2020 [33]. Producing more animal
waste to maintain the same meat output gen-
erates more pollution of the environment
and a larger carbon foot-print, so contrary to
96
consumer perception, consuming ABF meat
has a greater environmental impact than
consuming conventionally-produced meat
[5, 6]. Finally, and more importantly, by
making the production of poultry less ef-
ficient and requiring additional feed ingre-
dient resources for the manufacturing of
feed, ABF production could create addi-
tional demand for feed ingredients and, con-
sequently, a rise in feed ingredient prices
that impact both ABF and conventional pro-
duction. Therefore, ABF production could
make animal protein less accessible to those
who need it most, the undernourished and
hungry of the world [34].
CONCLUSION AND APPLICATIONS
1. ABF production is likely to result in signifi-
cant health challenges and its corresponding
adverse consequences on bird welfare.
2. In terms of residues in edible tissues,
all poultry production is ABF or at least
meets FDA established tolerances, which
are deemed safe for consumers. Random
sampling of poultry tissues from conven-
tionally raised poultry by the USDA-FSIS
shows compliance with tolerances estab-
lished by the United States FDA.
3. In terms of food safety, there are no scien-
tifically documented benefits derived from
producing ABF birds when compared to
conventionally raised poultry [2]. When
properly cooked and handled, poultry meat
contains no viable bacteria and dead bacte-
ria cannot transmit antibiotic resistance to
people.
4. ABF production is less efficient than con-
ventional production with antibiotics, and;
therefore, its higher consumption of feed,
water, and production of animal waste re-
sults in a larger carbon foot-print making it
less sustainable [4–6].
5. If in spite of the negatives aspects of ABF
production, a company decides to produce
ABF poultry numerous changes to its feed-
ing, management, and health programs will
have to be made in order to succeed, but
even successful companies will face higher
JAPR: Review Article
costs of production, some of which may be
passed along to the consumers.
REFERENCES AND NOTES
1. UK Five Year Antimicrobial Resistance Strategy
2013 to 2018, First Published: September, 2013, Department
of Health, Richmond House, 79 Whitehall, London SW1A
2NS. This publication is available at: www.gov.uk/dh
2. Smith-Spangler, C., M. L. Brandeau, G. E. Hunter,
C. Bavinger, M. Pearson, P. J. Eschbach, V. Sundaram, H.
Liu, P. Schirmer, C. Stave, I. Olkin, and D. M. Bravata.
2012. Are organic foods safer or healthier than conventional
alternatives? Ann. Intern. Med. 157:348-W102.
3. Al-Sheikhly, F., and A. Al-Saieg. 1980. Role of coc-
cidia in the occurrence of necrotic enteritis of chickens. Avian
Dis. 24:324–333.
4. Rosen, G. D. 2004. Optimizing the replacement of
pronutrient antibiotics in poultry nutrition. pp. 93–101 in
Proc. of Alltech’s 20th Annual International Symposium.
Alltech, Lexington, Kentucky, U.S.A.
5. Leinonen, I., A. G. Williams, J. Wiseman, J. Guy, and
I. Kyriazakis. 2012. Predicting the environmental impacts of
chicken systems in the United Kingdom through a life cycle
assessment: egg production systems. Poult. Sci. 91:26–40.
6. Smith, R. 2008. Research looks at foot-
print. Feedstuffs Food Link, article available at
http://fdsmagissues.feedstuffs.com/fds/pastissues/fds8002/
fds09_8002.pdf
7. Cox, L. A. Jr., D. A. Popken, and R. Carnevale. 2007.
Quantifying Human Health Risks from Animal Antimicro-
bials. Interfaces 37(1):22–38.
8. Phillips, I., M. Casewell, T. Cox, B. De Groot,
C. Friis, R. Jones, C. Nightingle, R. Preston, and J. Waddell.
2004. Does the use of antibiotics in food animals pose a
risk to human health? A critical review of published data. J.
Antimicrob. Chemother. 53:28–52.
9. Phillips, I. 2007. Withdrawal of growth-promoting
antibiotics in Europe and its effects in relation to human
health. Int. J. Antimicrob. Ag. 30(2):101–107.
10. Magee, J. T., E. L. Pritchard, K. A. Fitzgerald, F. D.
J. Dunstan, and A. J. Howard. 1999. Antibiotic prescribing
and antibiotic resistance in community practice: retrospec-
tive study, 1996–8. Brit. Med. J. 319:1239–1240
11. Bywater, R. J., and M. W. Casewell. 2000. An as-
sessment of the impact of antibiotic resistance in different
bacterial species and of contribution of animal sources to
resistance in human infections. J. Antimicrob. Chemother.
46:1052.
12. Brewer, M. S., and M. Rojas. 2008. Consumer atti-
tudes towards issues in food safety. J. Food Safety 28:1–22.
13. United States Department of Agriculture, Food
Safety and Inspection Service, Office of Public Health Sci-
ence. 2010. National residue program for meat, poultry and
egg products, 2010 residue sample results.
14. Donoghue, D. J. 2003. Antibiotic residues in poul-
try tissues and eggs: Human health concerns? Poult. Sci.
82:618–621.
15. Schroeder, J., B. Chassy, D. Tribe, G. Brookes,
and D. Kershen. 2014. Organic Marketing Report, Aca-
demics Review. Accessible at Academics Review website:
http://academicsreview.org/wp-content/uploads/2014/04/
Academics-Review_Organic-Marketing-Report1.pdf.
CERVANTES: SUSTAINABILITY OF ABF POULTRY PRODUCTION
16. Woodward, P. 2005. Impact of a ban on animal
byproducts and antibiotic growth promoters. Proc. 32nd Car-
olina Poultry Nutrition Conference, Oct. 26–27, Sheraton
Imperial Hotel and Convention Center, Research Triangle
Park, North Carolina.
17. Smith, J. A. 2011. Experiences with drug-free broiler
production. Poult. Sci. 90:2670–2678.
18. Applegate, T. J., V. Klose, T. Steiner, A. Ganner, and
G. Schatzmayr. 2010. Probiotics and phytogenics for poultry:
Myth or reality? J. Appl. Poult. Res. 19:194–210.
19. Roura, E., J. Homedes, and K. C. Klasing. 1992.
Prevention of immunologic stress contributes to the growth-
permitting ability of dietary antibiotics in chicks. J. Nutr.
122:2383–2390.
20. Niewold, T. A. 2007. The nonantibiotic anti-
inflammatory effect of antimicrobial growth promoters,
the real mode of action? A hypothesis. Poult. Sci. 86:
605–609.
21. Cervantes, H. 2002. Incidence of pathological con-
ditions in clinically normal broilers from different regions
of the USA. 51st Western Poultry Disease Conference,
May 1–4, Casa Magna Marriott Resort, Puerto Vallarta,
Jalisco, Mexico, pp. 220–223.
22. Kaldhusdal, M., and M. Hofshagen. 1992. Barley
inclusion and avoparcin supplementation in broiler diets. 2.
Clinical, pathological and bacteriological findings in a mild
form of necrotic enteritis. Poult. Sci. 71:1145–1153.
23. Van der Sluis, W. 2000. Clostridial enteritis is an
often underestimated problem. World’s Poult. Sci. J. 16:
42–43.
24. Cuckler, A. C., C. M. Malanga, and W. H. Ott. 1955.
The antiparasitic activity of nicarbazin. Poult. Sci. 34:98–
109.
97
25. Keshavarz, K., and L. R. McDougald. 1981. Influ-
ence of anticoccidial drugs on losses of broiler chickens
from heat stress and coccidiosis. Poult. Sci. 60:2423–2428.
26. Mathis, G. F., and C. Broussard. 2006. Increased level
of Eimeria sensitivity to diclazuril after using a live coccidial
vaccine. Avian Dis. 50:321–324.
27. Stutz, M., and G. Lawton. 1984. Effects of diet and
antimicrobials on growth, feed efficiency, intestinal Clostrid-
ium perfringens and ileal weight of broiler chicks. Poult. Sci.
63:2036–2042.
28. De Somer, P., and P. Van Dijck. 1955. A preliminary
report on antibiotic number 899. Antib. Chemo. 5:632–639.
29. Ruiz, Jaime, H. Cervantes, S. Christenberry, and
K. Bafundo. 2013. In-vitro antimicrobial susceptibility of
Clostridium perfringens isolates from broiler origin. Proc.
International Poultry Scientific Forum, January 31, World
Congress Center, Atlanta, Georgia.
30. Barnes, H. J., L. K. Nolan, and J.-P. Valliancourt.
2008. Colibacillosis, in: Diseases of Poultry, 12th Ed., Black-
well Publishing Professional, Ames, Iowa, USA. pp. 691–
737.
31. Russell, S. M. 2003. The effect of airsacculitis on bird
weights, uniformity, fecal contamination, processing errors
and populations of Campylobacter spp. and E. coli. Poult.
Sci. 82:1326–1331.
32. National Academy of Sciences. 1999. The use of
drugs in food animals: Benefits and risks. Natl. Acad. Press,
Washington, DC.
33. United Nations Population Division, United Nations
Food and Agriculture Organization.
34. United Nations Food and Agriculture Organization,
Rome, Italy. Number of hungry people rises to 963 million.
Accessed 3/14/2014.