Antibiotic-free poultry production: Is it sustainable?

Antibiotic-free poultry production: Is it sustainable?

 C 2015 Poultry Science Association, Inc. Antibiotic-free poultry production: Is it sustainable? Hector M. Cervantes1 Phibro Animal Health Corporati...

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 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

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 There is little convincing scientific evidence that the use of antibiotics in food-producing animals is contributing to the antibiotic resistance issues that are relevant to human medicine [1, 7–9]. However, public perception in firstworld countries suggests that consumers believe this to be true. According to the U.S. Organic 1

Corresponding author: [email protected]

Trade Association, sales of antibiotic-free (ABF) organic foods have grown at a rate of 20% per year since 1990. This is in spite of wider recognition that antibiotic resistance in humans is caused by antibiotic use in humans and not in foodproducing animals. In a recent document entitled “UK Five Year Antimicrobial Resistance Strategy 2013 to 2018” [1], the report states “Increasing scientific evidence suggests that the clinical issues with antimicrobial resistance that we face in human medicine are primarily the result of

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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 coccidiosis 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 carbon 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.

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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 companies 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 temperature, 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 conventional 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 specific physiological, immunological, and/or bacteriostatic effects in the intestine, none (to date) convey the range and extent of the effects of the antibiotics [18]. Other researchers have suggested 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 considered 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 purposes can be divided into two main groups:

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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 community closely matches antibiotic use in people from the same community [10]. Another study showed that antibiotic use in food-producing animals in a worst case scenario contributes less than 1% to the overall antibiotic resistance problem 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 agencies like the USDA-FSIS for decades have routinely 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) established 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 entitled “The Organic Marketing Report” written by Academics Review, an independent international 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 mistakenly 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 antibiotics chicken” by the USDA-FSIS is “these chickens have never been given antibiotics, including in the egg.” In contrast, the USDA-FSIS definition of organic chicken allows for antibiotic 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 USDAFSIS the label claim “raised without antibiotics” (RWA) means “no antibiotics in their feed, water, or injection including no ionophores” during

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CERVANTES: SUSTAINABILITY OF ABF POULTRY PRODUCTION 1) Enteric disease challenges. 2) Systemic disease challenges.

ENTERIC DISEASE CHALLENGES

chicken houses with vaccine strains of Eimeria oocysts that are fully susceptible to all anticoccidials [26]. However, the problem with the live coccidiosis vaccines is that they induce immunity by replicating and cycling a number of times through the intestines. Along with the replication and cycling required to induce active immunity, the parasites also cause damage to the epithelium of the intestinal tract and this predisposes 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 produced 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 activity against C. perfringens as demonstrated by having the lowest mean inhibitory concentration (MIC) among other antibiotic feed additives [27]. This could also be related to Virginiamycin’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 antibiotics like Virginiamycin is not an option available 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 producers 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 target 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 suffering. Treatment should not be withheld or delayed even if it means the loss of ABF status

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The main challenges faced by producers of ABF chickens or turkeys are undoubtedly related 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 lesions induced by coccidiosis (especially E. maxima), whether due to field challenge or live coccidiosis vaccine are a well-known predisposing factor for clinical outbreaks of NE [3]. Removing ionophore anticoccidials and antibiotic feed additives is certain to cause problems in controlling coccidial parasites and bacterial organisms, in particular, Clostridium perfringens, the causative agent of NE in chickens and turkeys. Interestingly, both coccidiosis and NE in their subclinical forms, are widely recognized as the most prevalent and costly diseases of broiler chickens and turkeys [21–23]. Without use of ionophores in a coccidial prevention program, control of coccidiosis will have to be achieved exclusively with synthetic “chemical” 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 effective 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 resistant mutant population of parasites. Once the parasites have developed resistance to the anticoccidial, they are likely to remain resistant for a long period, as there are not enough chemical anticoccidials 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

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Table 1. Strategies used by producers of ABF poultry (adapted from P. Woodward, 2005). STRATEGY:

TARGET OR ACTIONS TO BE TAKEN:

Processing of feed to decrease bacterial load Conversion to a vegetarian diet Maintenance of dry litter

<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

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

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 produce both conventional and ABF birds and have separate processing plants for each type of production 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 alternatives to in-feed antibiotics has helped in reducing the problems associated with producing chickens without antibiotics, the performance of these flocks when raised at similar stocking densities is usually below that of flocks raised conventionally resulting in a higher cost of production [4]. On average, this cost is approximately 20% higher than that of chickens raised conventionally. In a paper from a symposium on alternatives to raising broiler chickens without antibiotics, a well respected poultry veterinarian 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 additives ranging from prebiotics and probiotics to live E. coli vaccines, oregano and organic acids

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 bacterial 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 primary pathogen but rather an opportunistic one. If the birds are stressed for any reason or their immune system compromised, the E. coli bacteria can multiply and cause a systemic infection that typically results in mortality and gross lesions characterized by the accumulation of a fibrino-purulent exudate. In other cases the triggering agent can be a viral respiratory disease like Newcastle disease or infectious bronchitis or a viral immunosuppressive disease like infectious 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

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Use highly digestible fats and starches

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

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OTHER IMPORTANT CONSIDERATIONS Veterinarians may have a philosophical disagreement with a policy of no use of antibiotics to prevent or treat disease and relieve bird suffering. 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. Additionally, another philosophical problem is likely to emerge when a professional is asked to support 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 advertisements [2, 15]. Therefore, the overall impact of ABF production should be carefully considered 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 allowance 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

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 combination of these. 2) By feeding more tons of feed, the company has to purchase or produce more ingredients, 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 dispose 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 consumers 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 poultry 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 consumers would be impacted disproportionately 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 exists today, food preference trends in one country, like the United States or other first-world nations may have adverse, unintended consequences impacting the world’s population in other countries. For example, by making production of poultry less efficient, more cropland (a very scarce and non-renewable resource) must be dedicated to the production of additional feed ingredients 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 desirable 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 generates more pollution of the environment and a larger carbon foot-print, so contrary to

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or M. synoviae are the most common triggering factors [30]. If birds experiencing an outbreak of colisepticemia are left untreated, morbidity and mortality will increase, and these can be severe enough to cause catastrophic losses to the producer. Regardless of the cause, birds diagnosed with systemic E. coli infection must be treated with antibiotics to mitigate the disease and prevent unnecessary bird suffering. Even when the disease is not as severe and the losses are mild, untreated flocks carry a higher load of bacteria 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].

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CONCLUSION AND APPLICATIONS 1. ABF production is likely to result in significant 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 conventionally raised poultry by the USDA-FSIS shows compliance with tolerances established by the United States FDA. 3. In terms of food safety, there are no scientifically 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 bacteria cannot transmit antibiotic resistance to people. 4. ABF production is less efficient than conventional production with antibiotics, and; therefore, its higher consumption of feed, water, and production of animal waste results 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 feeding, management, and health programs will have to be made in order to succeed, but even successful companies will face higher

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 coccidia 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 footprint. 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 Antimicrobials. 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: retrospective study, 1996–8. Brit. Med. J. 319:1239–1240 11. Bywater, R. J., and M. W. Casewell. 2000. An assessment 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 attitudes 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 Science. 2010. National residue program for meat, poultry and egg products, 2010 residue sample results. 14. Donoghue, D. J. 2003. Antibiotic residues in poultry 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, Academics Review. Accessible at Academics Review website: http://academicsreview.org/wp-content/uploads/2014/04/ Academics-Review_Organic-Marketing-Report1.pdf.

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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 efficient and requiring additional feed ingredient resources for the manufacturing of feed, ABF production could create additional demand for feed ingredients and, consequently, a rise in feed ingredient prices that impact both ABF and conventional production. Therefore, ABF production could make animal protein less accessible to those who need it most, the undernourished and hungry of the world [34].

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25. Keshavarz, K., and L. R. McDougald. 1981. Influence 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 Clostridium 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., Blackwell 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.

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16. Woodward, P. 2005. Impact of a ban on animal byproducts and antibiotic growth promoters. Proc. 32nd Carolina 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 growthpermitting ability of dietary antibiotics in chicks. J. Nutr. 122:2383–2390. 20. Niewold, T. A. 2007. The nonantibiotic antiinflammatory effect of antimicrobial growth promoters, the real mode of action? A hypothesis. Poult. Sci. 86: 605–609. 21. Cervantes, H. 2002. Incidence of pathological conditions 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.

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