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/lp/springer-journals/lysozyme-as-an-alternative-to-growth-promoting-antibiotics-in-swine-KSpNnQKisS
- Publisher
- Springer Journals
- Copyright
- Copyright © 2015 by Oliver and Wells.
- Subject
- Life Sciences; Agriculture; Biotechnology; Food Science; Animal Genetics and Genomics; Animal Physiology
- eISSN
- 2049-1891
- DOI
- 10.1186/s40104-015-0034-z
- pmid
- 26273432
- Publisher site
- See Article on Publisher Site
Abstract
Lysozyme is a naturally occurring enzyme found in bodily secretions such as tears, saliva, and milk. It functions as an antimicrobial agent by cleaving the peptidoglycan component of bacterial cell walls, which leads to cell death. Antibiotics are also antimicrobials and have been fed at subtherapeutic levels to swine as growth promoters. These compounds benefit swine producers by minimizing production losses by increasing feed efficiency and decreasing susceptibility to bacterial infection and disease. This manuscript reviews the knowledge of the effects of lysozyme, as compared to traditional subtherapeutic antibiotics in swine feed, on pig performance and health. It is clear from decades of studies that antibiotic use in feeds increases pig performance, particularly in the nursery. Similarly, lysozyme, as a feed additive, increases growth and feed efficiency. While the mechanism by which antibiotics and lysozyme improve performance is not clearly understood, both of these feed additives improve gastrointestinal health, improve the metabolic profile, and alter the gastrointestinal bacteria ecology of swine. Therefore, lysozyme is a suitable alternative to growth-promoting subtherapeutic antibiotic use in swine feed. Keywords: Antibiotics, Gastrointestinal, Lysozyme, Microbiota, Review, Swine Introduction Lysozyme is a 1,4-β-N-acetylmuramidase that enzy- Antimicrobials have been fed at subtherapeutic levels to matically cleaves a glycosidic linkage in the peptidogly- swine as growth promoters for more than 60 years, and can component of bacterial cell walls, which results in the majority of pigs produced in the U.S. receive antimi- the loss of cellular membrane integrity and cell death crobials in their feed at some point in their production [4]. In addition, hydrolysis products are capable of enhan- cycle. These compounds benefit swine producers by cing immunoglobulin A (IgA) secretion, macrophage acti- minimizing production losses by increasing feed effi- vation, and rapid clearance of bacterial pathogens [5, 6]. ciency and decreasing susceptibility to bacterial infection Thesedataindicatethatlysozyme may be aviablealterna- and disease [1]. Wells et al. [2] observed 62 % prevalence tive to antibiotics in diets fed to swine. for Salmonella in swine prior to the growing phase of Until recently, the literature pertaining to lysozyme as production, and this number decreased to less than 15 % a feed additive was limited to studies using transgenic after 8 weeks on diets containing chlortetracycline, a vectors to deliver lysozyme. These studies have shown broad based antimicrobial. In addition, increased Cam- changes in metabolite profiles [7], intestinal microbiota pylobacter shedding is associated with reduced perform- [8], and intestinal morphology [9] in pigs fed milk from ance in growing pigs [3]. Therefore, a reduction in transgenic goats expressing human lysozyme in their pathogen shedding due to antibiotic use appears to be mammary gland. In addition, Humphrey et al. [10], re- associated with increased animal performance. However, ported that diets supplemented with transgenic rice ex- in recent years, foreign and domestic markets have been pressing lysozyme had antibiotic-like properties when pressuring swine producers to reduce or remove antimi- fed to chicks. While these reports are encouraging, the crobials from their diets. delivery of lysozyme from transgenic goats’ milk or transgenic rice is problematic in a swine production set- ting. However, recent research with egg-white lysozyme showed a performance benefit when fed to young pigs * Correspondence: William.Oliver@ars.usda.gov USDA, ARS, U.S. Meat Animal Research Center, P. O. Box 166, Clay Center, NE [11–13]. 68933-0166, USA © 2015 Oliver and Wells. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. Oliver and Wells Journal of Animal Science and Biotechnology (2015) 6:35 Page 2 of 7 Lysozyme sources and current use Lysozyme as a feed additive Before discovering penicillin, Alexander Fleming discov- Performance ered the enzyme lysozyme based on the ability of nasal The use of antibiotics in livestock feed is well established secretions to prohibit bacterial growth [14]. Lysozyme is and can improve growth rates in several species, includ- a naturally occurring enzyme found in bodily secretions ing swine [28–30]. The most important phenotypes for such as tears, saliva, and milk. It functions as an anti- any antimicrobial feed additives are weight gain and feed microbial by enzymatically cleaving a glycosidic linkage efficiency. Studies using human lysozyme from trans- of bacterial cell walls peptidoglycan, which leads to cell genic goats’ milk did not show an improvement in death [4]. Lysozyme is found in many biological organ- growth of pigs consuming human lysozyme [8, 9]. This isms from bacteria and fungi to animal bodily secretions was likely due to the experimental design in these exper- and tissues [15, 16]. Lysozyme is an important defense iments as they were not conducted to evaluate the effect mechanism and is considered a part of the innate immune of lysozyme on pig performance. In these experiments, system in most mammals [17], and is also an important growth improvement due to lysozyme was likely masked component of human breast milk [18]. However, due to due to the presence of antibiotics in both the control its very low concentration in sow milk (<0.065 μg/mL), and the experimental diet [9]. Presumably, Maga et al. lysozyme is not believed to play a major role in the pre- [8] fed diets that included antibiotics also. In addition, vention of infection in suckling pigs. both Brudige et al. [9] and Maga et al. [8] fed dry, In vitro, lysozyme is generally considered effective pelleted nursery diets in addition to the lysozyme- against some Gram-positive bacteria, but ineffective containing goats’ milk. Thus, it is unclear how much against Gram-negative bacteria [19]. However, lysozyme, lysozyme was consumed by pigs in relation to the dry di- perhaps indirectly, can affect Gram-negative bacteria ets in these studies. Due to the changes in intestinal in vivo [11, 20]. Due to these antimicrobial properties, morphology and microflora, the pigs consumed a signifi- lysozyme has been used effectively in the food industry cant amount of lysozyme, but this amount may not have [21]. For example, it has been used in the cheese indus- been sufficient to impact growth rate. Humphrey et al. try to prevent late blowing [22, 23]. Lysozyme has also [10] fed 152 mg human lysozyme (produced from trans- been used as a preservative for other fresh foods [19], in- genic rice) per kg feed, but did not improve the growth cluding controlling meat spoilage [24]. rate of chicks. However, the chicks had significantly im- Lysozyme is not currently used extensively as a feed proved feed efficiency over those reared on a diet con- additive in the animal industry. However, its effective- taining neither the transgenic protein nor antibiotics. ness on pigs has been evaluated in different models. Lysozyme sourced from chicken eggs improves growth Until recently, the literature pertaining to lysozyme as performance comparable to neomycin/oxytetracycline a feed additive was limited to studies using milk from (milk diets; [11]), carbadox/copper sulfate (nursery diets; transgenic organisms or transgenic rice to produce [12]) or chlortetracycline/tiamulin hydrogen fumarate and deliver the enzyme. Human lysozyme has been (nursery diets; [13]) compared with pigs consuming a expressed in the milk of pigs [25], mice [26], and goats nonmedicated diet (Fig. 1). Due to the study design, [8] as models for human medicine. Subsequent studies feeding group-housed pigs a milk diet, May et al. [11] using transgenic goats’ milk suggested that lysozyme did not have the statistical power to detect changes in could be used as a feed antimicrobial. These studies have feed efficiency. However, Oliver and Wells [12] and shown changes in metabolite profiles [7], intestinal Oliver et al. [13] were the first examples of lysozyme im- microbiota [8], and intestinal morphology [9] in pigs fed proving feed efficiency in swine, where pigs consuming milk from transgenic goats expressing human lysozyme lysozyme had an improved feed efficiency of about 8 % in the mammary gland. Diets supplemented with trans- compared with pigs consuming the untreated diet, which genic rice expressing human lysozyme also improved the was similar to pigs consuming the antibiotic-treated performance of chicks [10]. These experiments were not feeds (Fig. 1). designed to evaluate lysozyme as a feed additive. How- ever, results from recent experiments have shown that Gastrointestinal tract lysozyme sourced from chicken eggs (Neova Technolo- Improved villus height and crypt depth in the small in- gies; Abbotsford, Canada) improved growth rate and testine generally indicates improved intestinal health intestinal morphology and reduced Campylobacter [31–33]. However, due to the already rapidly changing shedding in both 10-day-old pigs consuming a milk diet gross morphology in nursery pigs due to weaning, ob- [11] as well as nursery pigs [12, 13, 20]. In addition, served changes in intestinal morphology due to dietary Nyachoti et al. [27] reported the same source of lyso- subtherapeutic antibiotic are variable. Studies have shown zyme alleviated the piglet response to an oral challenge that some antibiotics improve morphology [12, 34] of Escherichia coli K88. whereas others do not [30, 35]. Previous work with human Oliver and Wells Journal of Animal Science and Biotechnology (2015) 6:35 Page 3 of 7 Fig. 1 Average daily gain and feed efficiency of nursery pigs consuming control (non-mediated), control + antibiotics, or control + lysozyme diets for 28 days. Nursery pigs consuming lysozyme or antibiotics gained weight approximately 8 % faster. In addition, pigs consuming either lysozyme or antibiotics had improved feed efficiency of approximately 7 %. These data were adapted from Oliver and Wells [12] and Oliver et al. [13]. *Mean differs from control (P < 0.05) lysozyme from transgenic goats’ milk or transgenic rice did not show improvements in intestinal morphology in the jejunum or ileum [9, 10, 36]. Cooper et al. [36] did show a tendency for lysozyme to increase duodenal villi height and observed a decrease in lamina propria thick- ness. Similar to the lack of improvement in growth per- formance in these studies, the lack of morphology response is likely due to the concomitant presence of anti- biotics in the feed, or simply a lower consumption of lysozyme. May et al. [11] and Oliver and Wells (Fig. 2; [12]) both observed increased villus heights and crypt depths, indi- cating improved intestinal health. However, the major morphological responses in pigs consuming lysozyme or antibiotics in liquid diets was observed in the ileum [11] compared with responses seen exclusively in the je- junum by Oliver and Wells [12]. Presumably, this is due to the different physical forms of the diets consumed. Major changes occur in the gastrointestinal tract in re- sponse to the transition from a liquid to dry diet [37], in particular to ion transport [38]. Presumably the changes in structure and function of the small intestine allowed lysozyme and antibiotics to have a greater effect on the jejunum. Oliver and Wells et al. [12] observed de- Fig. 2 Villi height/crypt depth ratio of nursery pigs fed either a control creased crypt depth in pigs consuming lysozyme or an- (non-medicated), control + antibiotics, or control + lysozyme diet for tibiotics (Fig. 2), whereas they were increased in pigs 28 days. Villi height increased and crypt depth decreased exclusively in the jejunum of pigs consuming antibiotics or lysozyme, resulting in an consuming lysozyme in liquid diets [11]. This is likely increase of approximately 70 % in villi height to crypt depth ratio. due to the fact that cellular proliferation is very high in These data were adapted from Oliver and Wells [12]. *Mean differs the crypts in the younger animal, while villi enterocytes from control (P <0.05) are longer-lived in suckling animals compared with Oliver and Wells Journal of Animal Science and Biotechnology (2015) 6:35 Page 4 of 7 weaned animals [39]. Nyachoti et al. [27] observed in- For example, poultry and swine reared in germ-free envi- creased villi height in the ileum of pigs weaned at ronments grow at a faster rate than animals reared in con- 17 days and fed an egg white source of lysozyme, but je- ventional production environments [43, 44]. In addition, junum morphology was not measured. Changes in ileal utilizing a clean vs. a dirty environment to stimulate a morphology were likely due to the effect of the Escherichia chronic immune response decreases animal performance coli K88 challenge on the small intestine [27]. Taken to- [45–47]. In pigs, an immune response does not generally gether, these data indicate that this source of lysozyme result in decreased feed conversion [48–50]. However, improves small intestinal morphology [11, 12, 27]. Im- both lysozyme [12] and antibiotics [1] improve feed effi- provements in small intestinal morphology may lead to a ciency in nursery swine. In addition, Nyachoti et al. [27] greater absorptive capacity and be a mechanism by which reported that lysozyme alleviated the piglet response to an lysozyme and antibiotics improve growth rates. oral challenge of Escherichia coli K88, similar to trad- itional antibiotics. Metabolites While cytokines primarily regulate the immune re- Nutritional regime, health status, age, level of produc- sponse, they have an equal effect on nutrient metabol- tion, and gastrointestinal microflora are a few examples ism. During an immune response, pro-inflammatory of the many factors that contribute to the metabolite cytokines redirect nutrients away from growth and to- profile of an animal. It is clear that both lysozyme and ward the immune response [51, 52]. Although not the antibiotics alter many of these factors including growth only mode of action, cytokines increased both muscle rate, microbiota (or at least individual organisms), and protein degradation and acute phase protein production gastrointestinal health. Circulating urea N is a reliable [53]. Cytokines and acute phase proteins were measured indirect measurement to show the oxidation of dietary in a study designed to elicit a low level immune re- amino acids in young pigs [40, 41]. Blood urea N (BUN) sponse, to both confirm the chronic immune stimulation is lower in pigs consuming either lysozyme or antibiotics and to determine the effect of antibiotics and lysozyme under a chronic immune challenge compared with con- on the immune response [13]. Interleukin-6 and pig trol pigs [13]. This contradicts earlier work in non- major acute phase protein were unaffected by immune challenged pigs [12]. However, considering that pigs status. In contrast, circulating levels of the cytokine consuming lysozyme or antibiotics accrued more protein tumor necrosis factor-α (TNF-α) and the acute phase and consumed similar amounts of feed compared with proteins haptoglobin and C-reactive protein (CRP) were control pigs [13], the greater BUN was expected. There- higher in chronically immune stimulated pigs compared fore, presumably, pigs that consumed lysozyme or anti- with pigs reared in a clean nursery. These changes in cy- biotics utilized more of their dietary amino acids for tokines and acute phase proteins, as well as the perform- protein deposition than control pigs. Oliver and Wells ance changes observed, indicate that an acceptable level [12] likely had too few of animals to detect a response in of immune response was generated in pigs reared in the BUN. dirty nursery to make inferences into the effect of antibi- The most efficient way to measure metabolites is otics and lysozyme on chronically immune stimulated through metabolomic experiments. Brundige et al. [7] pigs. Pigs consuming antibiotics or lysozyme had lower found 18 known serum metabolites that were changed TNF-α, haptoglobin, and CRP, compared with control by the consumption of lysozyme. Of these 18, most pigs, regardless of whether pigs were under chronic im- changed in a direction that was decidedly “positive” for mune stimulation or reared in a clean nursery. Similarly, pig health and(or) growth. Four of these (methionine, Lee et al. [54] observed lower haptoglobin levels in threonine, hydroxyproline, and urea) indicate a propen- antibiotic-fed pigs compared with non-medicated con- sity for increased growth in pigs consuming lysozyme. trols. In addition, Nyachoti et al. [27] observed lower cir- Methionine, threonine, and hydroxyproline increased in culating TNF-α levels post-challenge in pigs consuming serum indicating potential increases in protein synthesis lysozyme. While these later studies used a different and skeletal growth, while serum urea decreased. These model (acute Escherichia coli challenges), antibiotics and findings support Oliver et al. [13], in that lysozyme con- lysozyme fed to pigs reduced the immune response sumption increased growth rate and decreased circulat- when exposed to pathogens. In addition to these studies, ing urea, in addition to an increase in protein accretion Cooper et al. [36] determined that RNA for transforming compared with pigs consuming a non-medicated diet. growth factor-β1 was increased in unchallenged pigs consuming lysozyme from transgenic goats’ milk. Cytokines and Immune Response Immune system activation, including pro-inflammatory Microbial ecology cytokine and acute phase protein production, prevents an- It is clear that the microbiota are important to pig health imals from reaching their genetic growth potential [42]. and growth [26, 55]. However, Holman and Chenier [56] Oliver and Wells Journal of Animal Science and Biotechnology (2015) 6:35 Page 5 of 7 observed relatively minor changes to the pig’s microbiota associated with gastrointestinal health (Bifidobacteria- in pigs consuming either tylosin or chlortetracycline. ceae and Lactobacillaceae). These data support May Unno et al. [57] showed that the use of antibiotics in et al. [11] and Wells et al. (Fig. 3, [20]), who observed a swine feed inhibited potential pathogens. However, the 50 % reduction of Campylobacter spp. in pigs consum- use of chlortetracycline, sulfathiazole, and penicillin did ing lysozyme compared with non-medicated pigs. While not elicit a growth response making it impossible to de- carbadox/copper sulfate is effective against Campylobac- termine if the change in microbiota was associated with ter spp. [3], Wells et al. [20] observed that chlortetracyc- improved performance. Clearly, more work in this area line/tiamulin hydrogen fumarate did not change the is warranted. Campylobacter spp. in the feces similar to lysozyme. It is now well documented that lysozyme has anti- microbial qualities and improves pig performance and Conclusions gastrointestinal health. It is likely that lysozyme alters It is clear that feeding subtherapeutic levels of antibiotics the gastrointestinal bacterial population, either through improves performance and overall health and is used ex- direct bacterial elimination (Gram-positive bacteria) or tensively throughout the swine industry. However, it is changes to the ecology that favor one group of bacteria also clear that swine producers are under pressure to re- over another. However, little work has been done look- duce or eliminate the use of antibiotics due to concerns ing at the effect of lysozyme on pig gastrointestinal mi- over antibiotic resistance. Research into possible alterna- crobial populations. In a small, proof of concept tives is essential and will allow swine producers to keep experiment, Maga et al. [8] observed that lysozyme was the animal well-being and monetary advantages of antibi- capable of modulating the bacterial populations in the otics without the perceived negative effects of their use. duodenum and ileum of both kid goats and piglets. In Lysozyme is a natural antimicrobial already used in other pigs, lysozyme from transgenic goats’ milk reduced both facets of the food industry. In nursery pigs, lysozyme total coliforms and E. coli in the duodenum, while only added to feed improves gastrointestinal health, reduces total coliforms were reduced in the ileum. This small potential pathogen shedding, and improves growth and study clearly shows that lysozyme has the ability to alter feed efficiency. Therefore, lysozyme is a viable alterna- microbial populations in vivo. Lysozyme was also shown tive to traditional subtherapeutic antibiotic use in swine to reduce enterotoxigenic E. coli (ETEC) in challenged production. piglets [27]. However, the observed effect of lysozyme on E. coli species seems to be variable. The prevalence of Shiga-toxigenic E. coli (STEC) is generally low in nursery pigs [20] and was not altered by lysozyme or antibiotics. The eae gene, which is an indicator gene for entero- pathogenic and enterohemorrhagic E. coli (EPEC and EHEC, respectively) is observed in nursery pigs [20]. However, this gene increases over the course of the nur- sery phase, neither lysozyme or antibiotics seem to alter its abundance [20]. The different observations due to feeding lysozyme on E. coli may be due to the different sources of lysozyme, different species of E. coli (ETEC vs. STEC, EPEC, and EHEC), or the presence of a direct E. coli K88 challenge [27]. Maga et al. [58] studied the microbiome of pigs con- suming lysozyme expressed in transgenic goats’ milk. Lysozyme decreased the levels of Firmicutes and in- creased the levels of Bacteroidetes in pig feces. High levels of Bacteroidetes are associated with decreased nu- trient absorption [59], but the level of change in piglets consuming lysozyme is unlikely to cause decreased ab- sorption, especially considering the changes in gut Fig. 3 Campylobacter spp. shedding of nursery pigs fed either a morphology and performance observed when feeding control (non-medicated), control + antibiotics, or control + lysozyme diet for 28 days. Lysozyme, but not chlortetracyline/tiamulin in nursery lysozyme [12, 13]. At the taxonomic Family or Order swine feed prevented the normal increase in campylobacter shedding level, lysozyme decreased the abundance of bacteria as- in the feces of nursery pigs. These data were adapted from Wells et al. sociated with disease (Mycobacteriaceae, Streptococca- [20]. *Within day, mean differs from lysozyme (P < 0.05) ceae, and Campylobacterales) and increased bacteria Oliver and Wells Journal of Animal Science and Biotechnology (2015) 6:35 Page 6 of 7 Abbreviations 17. Varahan S, Iyer VS, Moore WT, Hancock LE. Eep confers lysozyme resistance BUN: Blood urea nitrogen; CRP: C-reactive protein; TNF-α: Tumor necrosis to enterococcus faecalis via the activation of the extracytoplasmic function factor- α; ETEC: Enterotoxigenic E. coli; STEC: Shiga-toxigenic E. coli; sigma factor SigV. J Bacteriol. 2013;195:3125–34. EPEC: Enteropathogenic E. coli; EHEC: Enterohemorrhagic E. coli. 18. Lonnerdal B. Nutritional and physiologic significance of human milk proteins. Am J Clin Nutr. 2003;77:1537S–43. 19. Cunningham FE, Proctor VA, Goetsch SJ. Egg-white lysozyme as a food Competing interests preservative: An overview. World's Poult Sci J. 1991;47:141–63. The authors declare that they have no competing interests. 20. Wells JE, Berry ED, Kalchayanand N, Rempel LA, Kim M, Oliver WT. Effect of lysozyme or antibiotics on faecal zoonotic pathogens in nursery pigs. J Appl Microbiol. 2015;118:1489–97. Authors’ contributions 21. Proctor VA, Cunningham FE. The chemistry of lysozyme and its use as a WO and JW contributed to the writing of this review paper. Both authors food preservative and a pharmaceutical. Crit Rev Food Sci Nutr. read and approved the final manuscript. 1988;26:359–95. 22. Scharfen EC, Mills DA, Maga EA. Use of human lysozyme transgenic goat Acknowledgments milk in cheese making: effects on lactic acid bacteria performance. J Dairy Support for the work described in Oliver et al. (2014) was provided by the Sci. 2007;90:4084–91. National Pork Board (#12-148, WO). Mention of trade names, proprietary 23. Bottazzi V, Battistotti B, Rebecchi A, Bertuzzi S. Germination of Clostridium products, or specified equipment does not constitute a guarantee or spores and the action of lysozyme in Grana cheese. Latte. 1996;11:80. warranty by the USDA and does not imply approval to the exclusion of 24. Nattress FM, Yost CK, Baker LP. Evaluation of the ability of lysozyme and other products that may be suitable. The USDA is an equal opportunity nisin to control meat spoilage bacteria. Int J Food Microbiol. 2001;70:111–9. provider and employer. 25. Tong J, Wei H, Liu X, Hu W, Bi M, Wang Y, et al. Production of recombinant human lysozyme in the milk of transgenic pigs. Transgenic Res. Received: 23 December 2014 Accepted: 15 July 2015 2011;20:417–9. 26. Maga EA, Anderson GB, Murray JD. The effect of mammary gland expression of human lysozyme on the properties of milk from transgenic mice. J Dairy Sci. 1995;78:2645–52. References 27. Nyachoti CM, Kiarie E, Bhandari SK, Zhang G, Krause DO. Weaned pig 1. Verstegen MW, Williams BA. Alternatives to the use of antibiotics as growth responses to Escherichia coli K88 (ETEC) oral challenge when receiving a promoters for monogastric animals. Anim Biotechnol. 2002;13:113–27. lysozyme-supplement. J Anim Sci. 2012;90:252–60. 2. Wells JE, Yen JT, Miller DN. Impact of dried skim milk in production diets on 28. Schwarz S, Kehrenberg C, Walsh TR. Use of antimicrobial agents in Lactobacillus and pathogenic bacterial shedding in growing-finishing swine. veterinary medicine and food animal production. Int J Antimicrob Agents. J Appl Microbiol. 2005;99:400–7. 2001;17:431–7. 3. Wells JE, Oliver WT, Yen JT. The effects of dietary additives on faecal levels 29. Cromwell GL. Why and how antibiotics are used in swine production. Anim of Lactobacillus spp., coliforms, and Escherichia coli, and faecal prevalence of Biotechnol. 2002;13:7–27. Salmonella spp. and Campylobacter spp. in U.S. production nursery swine. 30. Thymann T, Sorensen KU, Hedemann MS, Elnif J, Jensen BB, Banga-Mboko J Appl Microbiol. 2010;108:306–14. H, et al. Antimicrobial treatment reduces intestinal microflora and improves 4. Ellison III RT, Giehl TJ. Killing of gram-negative bacteria by lactoferrin and protein digestive capacity without changes in villous structure in weanling lysozyme. J Clin Invest. 1991;88:1080–91. pigs. Br J Nutr. 2007;97:1128–37. 5. Kawano M, Namba Y, Hanaoka M. Regulatory factors of lymphocyte- 31. Argenzio RA, Liacos JA, Levy ML, Meuten DJ, Lecce JG, Powell DW. Villous lymphocyte interaction. I. Con A-induced mitogenic factor acts on the late atrophy, crypt hyperplasia, cellular infiltration, and impaired glucose-Na G1 stage of T-cell proliferation. Microbiol Immunol. 1981;25:505–15. absorption in enteric cryptosporidiosis of pigs. Gastroenterology. 6. Clarke TB, Davis KM, Lysenko ES, Zhou AY, Yu Y, Weiser JN. Recognition of 1990;98:1129–40. peptidoglycan from the microbiota by Nod1 enhances systemic innate 32. Zijlstra RT, Whang KY, Easter RA, Odle J. Effect of feeding a milk replacer to immunity. Nat Med. 2010;16:228–31. early-weaned pigs on growth, body composition, and small intestinal 7. Brundige DR, Maga EA, Klasing KC, Murray JD. Consumption of pasteurized morphology, compared with suckled littermates. J Anim Sci. 1996;74:2948–59. human lysozyme transgenic goats' milk alters serum metabolite profile in 33. Oliver WT, Mathews SA, Phillips O, Jones EE, Odle J, Harrell RJ. Efficacy of young pigs. Transgenic Res. 2010;19:563–74. partially hydrolyzed corn syrup solids as a replacement for lactose in 8. Maga EA, Walker RL, Anderson GB, Murray JD. Consumption of milk from manufactured liquid diets for neonatal pigs. J Anim Sci. 2002;80:143–53. transgenic goats expressing human lysozyme in the mammary gland results 34. Piva A, Grilli E, Fabbri L, Pizzamiglio V, Gatta PP, Galvano F, et al. Intestinal in the modulation of intestinal microflora. Transgenic Res. 2006;15:515–9. metabolism of weaned piglets fed a typical United States or European diet 9. Brundige DR, Maga EA, Klasing KC, Murray JD. Lysozyme transgenic goats' with or without supplementation of tributyrin and lactitol. J Anim Sci. milk influences gastrointestinal morphology in young pigs. J Nutr. 2008;86:2952–61. 2008;138:921–6. 35. Shen YB, Piao XS, Kim SW, Wang L, Liu P, Yoon I, et al. Effects of yeast 10. Humphrey BD, Huang N, Klasing KC. Rice expressing lactoferrin and culture supplementation on growth performance, intestinal health, and lysozyme has antibiotic-like properties when fed to chicks. J Nutr. immune response of nursery pigs. J Anim Sci. 2009;87:2614–24. 2002;132:1214–8. 36. Cooper CA, Brundige DR, Reh WA, Maga EA, Murray JD. Lysozyme 11. May KD, Wells JE, Maxwell CV, Oliver WT. Granulated lysozyme as an transgenic goats' milk positively impacts intestinal cytokine expression and alternative to antibiotics improves growth performance and small intestinal morphology. Transgenic Res. 2011;20:1235–43. morphology of 10-day-old pigs. J Anim Sci. 2012;90:1118–25. 37. Koldovsky O, Dobiasova M, Hahn P, Kolinska J, Kraml J, Pacha J. 12. Oliver WT, Wells JE. Lysozyme as an alternative to antibiotics improves Development of gastrointestinal functions. Physiol Res. 1995;44:341–8. growth performance and small intestinal morphology in nursery pigs. 38. Pacha J. Ontogeny of Na + transport in rat colon. Comp Biochem Physiol A J Anim Sci. 2013;91:3129–36. Physiol. 1997;118:209–10. 13. Oliver WT, Wells JE, Maxwell CV. Lysozyme as an alternative to antibiotics 39. Smith MW. Postnatal development of transport function in the pig intestine. improves performance in nursery pigs during an indirect immune Comp Biochem Physiol A Comp Physiol. 1988;90:577–82. challenge. J Anim Sci. 2014;92:4927–34. 40. Oliver WT, Touchette KJ, Coalson JA, Whisnant CS, Brown JA, Oliver SA, et al. 14. Fleming A. On a remarkable bacteriolytic element found in tissues and Pigs weaned from the sow at 10 days of age respond to dietary energy secretions. Proc R Soc. 1922;93:306–17. source of manufactured liquid diets and exogenous porcine somatotropin. 15. Tenovuo J, Lumikari M, Soukka T. Salivary lysozyme, lactoferrin and J Anim Sci. 2005;83:1002–9. peroxidases: Antibacterial effects on cariogenic bacteria and clinical applications in preventive dentistry. Proc Finn Dent Soc. 1991;87:197–208. 41. Oliver WT, Miles JR. A low-fat liquid diet increases protein accretion and 16. Jolles P, Jolles J. What's new in lysozyme research? Always a model system, alters cellular signaling for protein synthesis in 10-day-old pigs. J Anim Sci. today as yesterday. Mol Cell Biochem. 1984;63:165–89. 2010;88:2576–84. Oliver and Wells Journal of Animal Science and Biotechnology (2015) 6:35 Page 7 of 7 42. Cook ME. Triennial Growth Symposium: A review of science leading to host- targeted antibody strategies for preventing growth depression due to microbial colonization. J Anim Sci. 2011;89:1981–90. 43. Drew MD, Van Kessel AG, Maenz DD. Absorption of methionine and 2- hydroxy-4-methylthiobutoanic acid in conventional and germ-free chickens. Poult Sci. 2003;82:1149–53. 44. Loynachan AT, Pettigrew JE, Wiseman BS, Kunkle RA, Harris DL. Evaluation of a diet free of animal protein in germfree swine. Xenotransplantation. 2005;12:149–55. 45. Roura E, Homedes J, Klasing KC. Prevention of immunologic stress contributes to the growth-permitting ability of dietary antibiotics in chicks. J Nutr. 1992;122:2383–90. 46. Bassaganya-Riera J, Hontecillas-Magarzo R, Bregendahl K, Wannemuehler MJ, Zimmerman DR. Effects of dietary conjugated linoleic acid in nursery pigs of dirty and clean environments on growth, empty body composition, and immune competence. J Anim Sci. 2001;79:714–21. 47. Renaudeau D, Gourdine JL, St-Pierre NR. A meta-analysis of the effects of high ambient temperature on growth performance of growing-finishing pigs. J Anim Sci. 2011;89:2220–30. 48. Williams NH, Stahly TS, Zimmerman DR. Effect of level of chronic immune system activation on the growth and dietary lysine needs of pigs fed from 6 to 112 kg. J Anim Sci. 1997;75:2481–96. 49. Williams NH, Stahly TS, Zimmerman DR. Effect of chronic immune system activation on body nitrogen retention, partial efficiency of lysine utilization, and lysine needs of pigs. J Anim Sci. 1997;75:2472–80. 50. Renaudeau D. Effect of housing conditions (clean vs. dirty) on growth performance and feeding behavior in growing pigs in a tropical climate. Trop Anim Health Prod. 2009;41:559–63. 51. Johnson RW. Inhibition of growth by pro-inflammatory cytokines: An integrated view. J Anim Sci. 1997;75:1244–55. 52. Spurlock ME. Regulation of metabolism and growth during immune challenge: An overview of cytokine function. J Anim Sci. 1997;75:1773–83. 53. Elsasser TH, Caperna TJ, Li CJ, Kahl S, Sartin JL. Critical control points in the impact of the proinflammatory immune response on growth and metabolism. J Anim Sci. 2008;86:E105–25. 54. Lee JS, Awji EG, Lee SJ, Tassew DD, Park YB, Park KS, et al. Effect of Lactobacillus plantarum CJLP243 on the growth performance and cytokine response of weaning pigs challenged with enterotoxigenic Escherichia coli. J Anim Sci. 2012;90:3709–17. 55. Rist VT, Weiss E, Eklund M, Mosenthin R. Impact of dietary protein on microbiota composition and activity in the gastrointestinal tract of piglets in relation to gut health: A review. Animal. 2013;7:1067–78. 56. Holman DB, Chenier MR. Temporal changes and the effect of subtherapeutic concentrations of antibiotics in the gut microbiota of swine. Microb Ecol. 2014;90:599–608. 57. Unno T, Kim J, Guevarra RB, Nguyen SG. Effects of antibiotic growth promoter and characterization of ecological succession in swine gut microbiota. J Microbiol Biotechnol. 2015;25(4):431–8. 58. Maga EA, Desai PT, Weimer BC, Dao N, Kultz D, Murray JD. Consumption of lysozyme-rich milk can alter microbial fecal populations. Appl Environ Microbiol. 2012;78:6153–60. 59. Jumpertz R, Le DS, Turnbaugh PJ, Trinidad C, Bogardus C, Gordon JI, et al. Energy-balance studies reveal associations between gut microbes, caloric load, and nutrient absorption in humans. Am J Clin Nutr. 2011;94:58–65. Submit your next manuscript to BioMed Central and take full advantage of: • Convenient online submission • Thorough peer review • No space constraints or color figure charges • Immediate publication on acceptance • Inclusion in PubMed, CAS, Scopus and Google Scholar • Research which is freely available for redistribution Submit your manuscript at www.biomedcentral.com/submit
Journal
Journal of Animal Science and Biotechnology – Springer Journals
Published: Aug 13, 2015