Hostname: page-component-cd9895bd7-mkpzs Total loading time: 0 Render date: 2024-12-29T19:50:30.020Z Has data issue: false hasContentIssue false
  • English
  • Français

Modulation of intestinal mucin composition and mucosal morphology by dietary phytogenic inclusion level in broilers

Published online by Cambridge University Press:  10 January 2012

P. Tsirtsikos ,
K. Fegeros ,
A. Kominakis ,
C. Balaskas  and
K. C. Mountzouris
P. Tsirtsikos
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
K. Fegeros
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
A. Kominakis
Affiliation:
Department of Animal Breeding and Husbandry, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
C. Balaskas
Affiliation:
Department of Anatomy and Physiology of Farm Animals, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
K. C. Mountzouris*
Affiliation:
Department of Nutritional Physiology and Feeding, Agricultural University of Athens, Iera Odos 75, 118 55 Athens, Greece
*
†E-mail: [email protected]
Get access

Abstract

The effect of a dietary phytogenic feed additive (PFA) inclusion level in mucin monosaccharide composition, mucosal morphometry and mucus histochemistry along the broiler intestinal tract was studied. Cobb male broilers (n = 525) were allocated into five experimental treatments that, depending on the type of addition in the basal diet (BD), were labeled as follows: C (BD based on maize–soybean meal with no other additions), E1 (80 mg PFA/kg BD), E2 (125 mg PFA/kg BD), E3 (250 mg PFA/kg of BD) and A (2.5 mg avilamycin/kg BD). Samples from duodenum, ileum and cecum of 14- and 42-day-old broilers were collected and analyzed. In 14-day-old broilers, treatments E2 and E3 had higher (P < 0.01) duodenal mannose than treatments C, E1 and A. Ileal mannose was lower (P < 0.05) in treatment C compared with PFA treatments, and ileal galactose (Gal) was higher (P < 0.01) in treatments E2 and E3 compared with C and A. Polynomial contrast analysis with respect to PFA inclusion level showed that in 14-day-old broilers there was a linear increase (P = 0.001) in duodenal mannose and a quadratic effect (P = 0.038) in duodenal N-acetyl-galactosamine with increasing PFA level. Ileal Gal and mannose increased linearly (P = 0.002 and P = 0.012, respectively) with PFA inclusion level. There were no significant differences between treatments in mucin monosaccharide molar ratios of 42-day-old broilers. However, increasing PFA inclusion level resulted in a linear decrease of ileal fucose (P = 0.021) and cecal N-acetylgalactosamine (P = 0.036). Experimental treatments did not differ (P > 0.05) regarding duodenal villus height (Vh), crypt depth (Cd) and Vh/Cd ratio, irrespective of broiler age and the intestinal segment examined. However, increasing dietary PFA inclusion level showed a pattern of linear increase of duodenal Vh/Cd ratio in 14-day-old broilers and ileal Vh in 42-day-old broilers (P = 0.039 and P = 0.039, respectively). Alcian Blue–Periodic Acid-Schiff (pH 2.5) staining of neutral and acidic mucins showed that the staining intensity of mucus layer in villi was fragment (i.e. tip, midsection and base) dependent, whereas in crypts it was dependent both on intestinal segment (i.e. duodenum, ileum and cecum) and fragment. Finally, mucus layer thickness did not differ (P > 0.05) between treatments, yet a pattern of linear increase (P < 0.05) with PFA inclusion level was observed in the duodenum of 42-day-old broilers. In conclusion, the dietary inclusion level of PFA modulated broiler intestinal mucin composition and morphology. Further studies are required to elucidate the physiological implications of such changes in host–microflora interactions.

Keywords

phytogenic feed additiveessential oilsbroilermucinintestinal morphology
Type
Full Paper
Information
animal , Volume 6 , Issue 7 , 28 May 2012 , pp. 1049 - 1057
Copyright
Copyright © The Animal Consortium 2012

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Anumula, K 1994. Quantitative determination of monosaccharides in glycoproteins by high-performance liquid chromatography with highly sensitive fluorescence detection. Analytical Biochemistry 220, 275–283.CrossRefGoogle ScholarPubMed
Anumula, K 1995. Rapid quantitative determination of sialic acids in glycoproteins by high-performance liquid chromatography with a sensitive fluorescence detection. Analytical Biochemistry 230, 24–30.CrossRefGoogle ScholarPubMed
Applegate, TJ, Klose, V, Steiner, T, Ganner, A, Schatzmayr, G 2010. Probiotics and phytogenics for poulty: myth or reality. Journal of Applied Poultry Research 19, 194–210.CrossRefGoogle Scholar
Batal, AB, Parsons, CM 2002. Effects of age on nutrient digestibility in chicks fed different diets. Poultry Science 81, 400–407.CrossRefGoogle ScholarPubMed
Brenes, A, Roura, E 2010. Essential oils in poultry nutrition: main effects and modes of action. Animal Feed Science and Technology 158, 1–14.CrossRefGoogle Scholar
Bry, L, Falk, PG, Midtvedt, T, Gordon, JI 1996. A model of host–microbial interactions in an open mammalian ecosystem. Science 273, 1380–1383.CrossRefGoogle Scholar
Cairnie, AB, Lamerton, LF, Steel, GG 1965. Cell proliferation studies in the intestinal epithelium of the rats. Experimental Cell Research 39, 528–538.CrossRefGoogle Scholar
Carlstedt-Duke, B, Høverstad, T, Lingaas, E, Norin, KE, Saxerholt, H, Steinbakk, M, Midtvent, T 1986. Influence of antibiotics on intestinal mucin in healthy subjects. European Journal of Clinical Microbiology 5, 634–638.CrossRefGoogle ScholarPubMed
Chee, SH, Iji, PA, Choct, M, Mikkelsen, LL, Kocher, A 2010a. Characterisation and response of intestinal microflora and mucins to manno-oligosaccharides and antibiotic supplementation in broiler chickens. British Poultry Science 51, 368–380.CrossRefGoogle Scholar
Chee, SH, Iji, PA, Choct, M, Mikkelsen, LL, Kocher, A 2010b. Functional interactions of manno-oligosaccharides with dietary threonine in chicken gastrointestinal tract. I. Growth performance and mucin dynamics. British Poultry Science 51, 658–666.CrossRefGoogle ScholarPubMed
Fernandez, F, Sharma, R, Hinton, M, Bedford, M 2000. Diet influences the colonisation of Campylobacter jejuni and distribution of mucin carbohydrates in the chick intestinal tract. Cellular and Molecular Life Sciences 57, 1793–1801.CrossRefGoogle ScholarPubMed
Forstner, JF, Forstner, GG 1994. Gastrointestinal mucus. In Physiology of the gastrointestinal tract (ed. LR Johnson), pp. 1255–1284. Raven Press, New York, USA.Google Scholar
Freitas, M, Axelsson, LG, Cayuela, C, Midtvedt, T, Trugnan, G 2005. Indigenous microbes and their soluble factors differentially modulate intestinal glycosylation steps in vivo. Histochemistry and Cell Biology 124, 423–433.CrossRefGoogle ScholarPubMed
García, V, Catalá-Gregori, P, Hernández, F, Megías, MD, Madrid, J 2007. Effect of formic acid and plant extracts on growth, nutrient digestibility, intestine mucosa morphology and meat yield of broilers. Journal of Applied Poultry Research 16, 555–562.CrossRefGoogle Scholar
Gheri Bryk, S, Sgambati, E, Gheri, G 1999. Lectin histochemistry of goblet cell sugar residues in the gut of the chick embryo and of the newborn. Tissue and Cell 31, 170–175.CrossRefGoogle Scholar
Giannenas, I, Florou Paneri, P, Papazahariadou, M, Christaki, E, Botsoglou, NA, Spais, AB 2003. Effect of dietary supplementation with oregano essential oil on performance of broilers after experimental infection with Eimeria tenella. Archives of Animal Nutrition 57, 99–106.CrossRefGoogle ScholarPubMed
Gusils, C, Oppezzo, O, Pizarro, R, González, S 2003. Adhesion of probiotic lactobacilli to chick intestinal mucus. Canandian Journal of Microbiology 49, 472–478.CrossRefGoogle ScholarPubMed
Hoskins, LC, Agustines, M, McKee, WB, Boulding, ET, Kriaris, M, Niedermeyer, G 1986. Mucin degradation in human colon ecosystems. Isolation and properties of fecal strains that degrade ABH blood group antigens and oligosaccharides from mucin glycoproteins. Journal of Clinical Investigation 75, 944–953.CrossRefGoogle Scholar
Jamroz, D, Wertelecki, T, Houszka, M, Kamel, C 2006. Influence of diet type on the inclusion of plant origin active substances on morphological and histochemical characteristics of the stomach and jejunum walls in chicken. Journal of Animal Physiology and Animal Nutrition 90, 255–268.CrossRefGoogle ScholarPubMed
Kirjavainen, P, Ouwehand, A, Isolauri, E, Salminen, S 1998. The ability of probiotic bacteria to bind to human intestinal mucus. FEMS Microbiology Letters 167, 185–189.CrossRefGoogle ScholarPubMed
Libao-Mercado, A, De Lange, C 2007. Refined methodology to purify mucins from pig colonic mucosa. Livestock Science 109, 141–144.CrossRefGoogle Scholar
Mack, DR, Michail, S, Wie, S, McDougall, L, Hollingsworth, MA 1999. Probiotics inhibit enteropathogenic E. coli adherence in vitro by inducing intestinal mucin gene expression. American Journal of Physiology-Gastrointestinal and Liver Physiology 276, 941–950.CrossRefGoogle ScholarPubMed
Mack, DR, Ahrne, S, Hyde, L, Wei, S, Hollingsworth, MA 2003. Extracellular MUC3 mucin secretion follows adherence of Lactobacillus strains to intestinal epithelial cells in vitro. Gut 52, 827–833.CrossRefGoogle ScholarPubMed
Montagne, L, Toullec, R, Lallès, P 2000. Calf intestinal mucin: isolation, partial characterization and measurment in ileal digesta with an enzyme-linked immunosorbent assay. Journal of Dairy Science 83, 507–517.CrossRefGoogle ScholarPubMed
Montagne, L, Pluske, JR, Hampson, DJ 2003. A review of interactions between dietary fibre and the intestinal mucosa, and their consequences on digestive health in young non-ruminant animals. Animal Feed Science and Technology 108, 95–117.CrossRefGoogle Scholar
Mountzouris, KC, Paraskevas, V, Tsirtsikos, P, Palamidi, I, Steiner, T, Schatzmayr, G, Fegeros, K 2011. Assessment of a phytogenic feed additive effect on broiler growth performance, nutrient digestibility and caecal microflora composition. Animal Feed Science and Technology 168, 223–231.CrossRefGoogle Scholar
Ouwehand, A, Kirjavainen, P, Grunlund, M, Isolauri, E, Salminen, S 1999. Adhesion of probiotic micro-organisms to intestinal mucus. International Dairy Journal 9, 623–630.CrossRefGoogle Scholar
Perić, L, Milošević, N, Žikić, D, Bjedov, S, Cvetković, D, Markov, S, Mohnl, M, Steiner, T 2010. Effects of probiotic and phytogenic products on performance, gut morphology and cecal microflora of broiler chickens. Archives of Animal Breeding 53, 350–359.CrossRefGoogle Scholar
Ruas-Madiedo, P, Gueimonde, M, Fernandez-Garcia, M, de los Reyes-Gavilan, CG, Margolles, A 2008. Mucin degradation by Bifidobacterium strains from the human intestinal microbiota. Applied and Environmental Microbiology 74, 1936–1940.CrossRefGoogle ScholarPubMed
Salyers, AA 1979. Energy sources of major intestinal fermentative anaerobes. American Journal of Clinical Nutrition 32, 158–163.CrossRefGoogle ScholarPubMed
Scwad, C, Gänzle, M 2011. Lactic acid bacteria fermentation of human milk oligosaccharide components, human milk oligosaccharides and galactooligosaccharides. FEMS Microbiology Letters 315, 141–148.Google Scholar
Sharma, R, Fernandez, F, Hinton, M, Schumacher, U 1997. The influence of diet on the mucin carbohydrates in the chick intestinal tract. Cellular and Molecular Life Sciences 53, 935–942.CrossRefGoogle ScholarPubMed
Shub, M, Pang, K, Swann, D, Walker, W 1983. Age-related changes in chemical composition and physical properties of mucus glycoproteins from rat small intestine. Biochemistry Journal 215, 405–411.CrossRefGoogle ScholarPubMed
Smirnov, A, Tako, E, Ferket, PR, Uni, Z 2006. Mucin gene expression and mucin content in the chicken intestinal goblet cells are affected by in ovo feeding of carbohydrates. Poultry Science 85, 669–673.CrossRefGoogle ScholarPubMed
Smirnov, A, Perez, R, Amit-Romach, E, Sklan, D, Uni, Z 2005. Mucin dynamics and microbial populations in chicken small intestine are changed by dietary probiotic and antibiotic growth promoter supplementation. Journal of Nutrition 135, 187–192.CrossRefGoogle ScholarPubMed
Stahl, M, Friis, LM, Nothaft, H, Liu, X, Li, J, Szymanski, CM, Stinzi, A 2011. l-Fucose utilization provides Campylobacter jejuni with a competitive advantage. The Proceedings of the National Academy of Sciences 108, 7194–7199.CrossRefGoogle ScholarPubMed
Strous, GJ, Dekker, J 1992. Mucin-type glycoproteins. Critical Reviews in Biochemistry and Molecular Biology 27, 57–92.CrossRefGoogle ScholarPubMed
Tekeli, A, Kutlu, HR, Celik, L, Doran, F 2010. Determination of the effects of Z. Officinale and propolis extracts on intestinal microbiology and histological characteristics in broilers. International Journal of Poultry Science 9, 898–906.CrossRefGoogle Scholar
Turck, D, Feste, A, Lifschitz, C 1993. Age and diet affect the composition of porcine colonic mucins. Pediatric Research 33, 564–567.CrossRefGoogle ScholarPubMed
Uni, Z, Platin, R, Sklan, D 1998. Cell proliferation in chicken intestinal epithelium occurs both in the crypts and along the villus. Journal of Comparative Physiology B 168, 241–247.CrossRefGoogle ScholarPubMed