Influence of the type of autonomic tone on the volume of the mucous membrane of the small intestine of laying hens

Keywords: small intestine of chickens; sympathicotonic chickens; sympathico-normotonic chickens; volume of villi; volume of connective tissue fibers.


The connection between the separate structural parts of the mucous membrane of the small intestine of laying hens and the typological features of the autonomic tone were investigated. The studies were conducted on adult chickens of the cross-breed "Isa-Brown", which were divided into two groups: sympathicotonic chickens and sympathico-normotonic chickens, by the methods of electrocardiography and variation-pulsometry research. In the small intestine of the poultry of each group, the linear dimensions were determined first, and then the volume of the entire mucous membrane and its separate parts (villi, crypt, muscular plate), as well as the volume of connective tissue fibers in the crypt region. Research has shown that the villi account for ¾ of the volume of the entire mucous membrane. The volume of villi in the entire small intestine is more important in sympathico-normotonic chickens. This same poultry group has an advantage in the indicators of the volume of the muscular plate, but only in the duodenum and jejunum. In indicators of crypt volume, it turned out to be quite the opposite of the relationship with the typology of autonomous influences. In all studied intestines, the higher values of this indicator belong to the sympathotonic chickens. However, in terms of the volume of the entire mucous membrane, larger values still correspond to sympathico-normotonic chickens. Sympathicotonic chickens are inferior to them in the duodenum – at 1,005 mm3, in the jejunum – at 2,699 mm3 and in the ileum – only 78 mm3. Investigating the structure of the villi, we established that the volume of their epithelium in all three sections of the small intestine has higher values in the sympathico-normotonic chickens, and the larger volume of the lamina propria of the villi in the sympathicotonic chickens. At the same time, the connection with the type of autonomic tone is reflected in the ratio between the two layers of villi. In all three sections of the small intestine of sympathicotonic chickens, the ratio between the epithelium and the lamina propria was, on average, 65%/35%, or 2/1. In sympathico-normotonic chickens, this ratio varied and, on average, equalled 75%/25%, or 3/1. The increase in the tone of sympathetic centers contributes to the growth of volume both as the total amount of fibers of connective tissue, and also as separate elastic fibers in the area of crypt. According to the data,indicators of the sympathico-normotonic chickens are inferior to those of sympathicotonic chickens in all of the small intestine. It was also found that in both groups of poultry the volume of elastic fibers was approximately half the volume of all fibers of the connective tissue of the duodenum. In other sections of the small intestine, this figure was reduced to about ⅓. Consequently, the typological features of the autonomic tone, providing various trophic-regulatory effects on the mucous membrane of the small intestine, cause the formation of differences in its volume.


Ali, H. A., & McLelland, J. (1978). Avian enteric nerve plexuses. A histochemical study. Cell and Tissue Research, 189, 537–548.

Aubert, A. E., Beckers, F., Ramaekers, D., Verheyden, B., Leribaux, C., Aerts, J.-M., & Berckmans, D. (2004). Heart rate and heart rate variability in chicken embryos at the end of incubation. Experimental Physiology, 89(2), 199–208.

Baevskij, R. M., Kirilov, O. I., & Kleckin, S. Z. (1984). Matematicheskij analiz serdechnogo ritma pri stresse [Mathematical analysis of cardiac rhythm in stress]. Nauka, Moscow (in Russian).

Bahr, J. M. (2008). The chicken as a model organism. Sourcebook of Models for Biomedical Research, 161–167.

Bedecarrats, G. Y., Baxter, M., & Sparling, B. (2016). An updated model to describe the neuroendocrine control of reproduction in chickens. General and Comparative Endocrinology, 227, 58–63.

Borda-Molina, D., Seifert, J., & Camarinha-Silva, A. (2018). Current perspectives of the chicken gastrointestinal tract and its microbiome. Computational and Structural Biotechnology Journal, 16, 131–139.

Borell, E., Langbein, J., Despres, G., Hansen, S., Leterrier, C., Marchant-Forde, J., Marchant-Forde, R., Minero, M., Mohr, E., Prunier, A., Valance, D., & Veissier, I. (2007). Heart rate variability as a measure of autonomic regulation of cardiac activity for assessing stress and welfare in farm animals – A review. Physiology and Behavior, 92, 293–316.

Casteleyn, C., Doom, M., Lambrechts, E., Van den Broeck, W., Simoens, P., & Cornillie, P. (2010). Locations of gut-associated lymphoid tissue in the 3-month-old chicken: A review. Avian Pathology, 39(3), 143–150.

Cheled-Shoval, S. L., Withana Gamage, N. S., Amit-Romach, E., Forder, R., Marshal, J., Van Kessel, A., & Uni, Z. (2014). Differences in intestinal mucin dynamics between germ-free and conventionally reared chickens after mannan-oligosaccharide supplementation. Poultry Science, 93, 636–644.

Chevalier, N. R., Fleury, V., Dufour, S., Proux-Gillardeaux, V., & Asnacios, A. (2017). Emergence and development of gut motility in the chicken embryo. PLoS One, 12(2), e0172511.

China, A. M., Hill, D. R., Aurorac, M., & Spencea, J. R. (2017). Morphogenesis and maturation of the embryonic and postnatal intestine. Seminars in Cell and Developmental Biology, 66, 81–93.

Crossley, D., & Altimiras, J. (2000). Ontogeny of cholinergic and adrenergic cardiovascular regulation in the domestic chicken (Gallus gallus). American Journal of Physiology. Regulatory, Integrative and Comparative Physiology, 279, 1091–1098.

Dennis, R. L. (2016). Adrenergic and noradrenergic regulation of poultry behavior and production. Domestic Animal Endocrinology, 56, 94–100.

Doyle, A. M., Roberts, D. J., & Goldstein, A. M. (2004). Enteric nervous system patterning in the avian hindgut. Developmental Dynamics, 229, 708–712.

Esmail, S. H. M. (1988). Scanning electron microscopy of intestinal villous structures and their putative relation to digestion and absorption in chickens. Reproduction Nutrition Development, 28(6A), 1479–1487.

Fekete, E., & Csoknya, M. (1987). Fluorescence characterization of the nerve plexuses in the small intestine of the chicken. Acta Biologica Szegediensis, 33, 97–104.

Forder, R. E., Nattrass, G. S., Geier, M. S., Hughes, R. J., & Hynd, P. I. (2012). Quantitative analyses of genes associated with mucin synthesis of broiler chickens with induced necrotic enteritis. Poultry Science, 91, 1335–1341.

Furness, J. B. (2000). Types of neurons in the enteric nervous system. Journal of the Autonomic Nervous System, 81(1–3), 87–96.

Furness, J. B., & Costa, M. (1980). Types of nerves in the enteric nervous system. Commentaries in the Neurosciences, 235–252.

Geyra, A., Uni, Z., & Sklan, D. (2001). Enterocyte dynamics and mucosal development in the posthatch chick. Poultry Science, 80(6), 776–782.

Goldstein, A. M., & Nagy, N. (2008). A bird's eye view of enteric nervous system development: Lessons from the avian embryo. Pediatric Research, 64(4), 326–333.

Hao, M. M., Foong, J. P. P., Bornstein, J. C., Li, Z. L., Vanden Berghe, P., & Boesmans, W. (2016). Enteric nervous system assembly. Functional integration within the developing gut. Developmental Biology, 417, 168–181.

Heak, C., Sukon, P., Kongpechr, S., Tengjaroenkul, B., & Chuachan, K. (2017). Effect of direct-fed microbials on intestinal villus height in broiler chickens: A systematic review and meta-analysis of controlled trials. International Journal of Poultry Science, 16, 403–414.

Heanue, T. A., Shepherd, I. T., & Burns, A. J. (2016). Enteric nervous system development in avian and zebrafish models. Developmental Biology, 417(2), 129–138.

Incharoen, T. (2013). Histological adaptations of the gastrointestinal tract of broilers fed diets containing insoluble fiber from rice hull meal. American Journal of Animal and Veterinary Sciences, 8(2), 79–88.

Incharoen, T., Yamauchi, K., Erikawa, T., & Gotoh, H. (2010). Histology of intestinal villi and epithelial cells in chickens fed low-crude protein or low-crude fat diets. Italian Journal of Animal Science, 9(4), 429–434.

Jeurissen, S. H. M., Lewis, F., Klis, J. D., Mroz, Z., Rebel, J. M. J., & Huurne, A. A. H. M. (2002). Parameters and techniques to determine intestinal health of poultry as constituted by immunity, integrity, and functionality. Current Issues in Intestinal Microbiology, 3, 1–14.

Khalid, K. K., Zuki, A. B., Noordin, M. M., Mohd, A. B., & Mohd, Z. S. (2014). Light and scanning electron microscopy of the small intestine of young Malaysian village chicken and commercial broiler. Pertanika Journal of Tropical Agricultural Science, 37(1), 51–64.

Kjaer, J. B., & Jorgensen, H. (2011). Heart rate variability in domestic chicken lines genetically selected on feather pecking behavior. Genes, Brain nd Behavior, 10, 747–755.

Kogut, M. H., Genovese, K. J., Swaggerty, C. L., He, H., & Broom, L. (2018). Inflammatory phenotypes in the intestine of poultry: Not all inflammation is created equal. Poultry Science, 97(7), 2339–2346.

Kononenko, V. S., & Zaitsev, A. A. (2009). Analіz makromorfometrichnih parametrіv sercja ovec' z rіznim tonusom avtonomnih centrіv [An analysis of macromorphometric parameters of heart of sheep with different tone of autonomous centers]. Naukovij Vіsnik L'vіvs'kogo Nacіonal'nogo Unіversitetu Veterinarnoji medicini ta bіotehnologіj іmenі S. Z. Gzhic'kogo, 11(2), 165–169 (in Ukrainian).

Laudadio, V., Passantino, L., Perillo, A., Lopresti, G., Passantino, A., Khan, R. U., & Tufarelli, V. (2012). Productive performance and histological features of intestinal mucosa of broiler chickens fed different dietary protein levels. Poultry Science, 91, 265–270.

Lavin, S. R., Karasov, W. H., Ives, A. R., Middleton, K. M., & Garland, T. Jr. (2008). Morphometrics of the avian small intestine compared with that of nonflying mammals: A phylogenetic approach. Physiological and Biochemical Zoology, 81(5), 526–550.

Lilburn, M. S., & Loeffler, S. (2015). Early intestinal growth and development in poultry. Poultry Science, 94, 1569–1576.

Mabelebele, M., Alabi, O. J., Ng’ambi, J. W., Norris, D., & Ginindza, M. M. (2014). Comparison of gastrointestinal tracts and pH values of digestive organs of Ross 308 broiler and indigenous venda chickens fed the same diet. Asian Journal of Animal and Veterinary Advances, 9(1), 71–76.

Marchini, C. F. P., Cafe, M. B, Araujo, E. G., & Nascimento, M. R. B. M. (2016). Physiology, cell dynamics of small intestinal mucosa, and performance of broiler chickens under heat stress: A review. Revista Colombiana de Ciencias Pecuarias, 29, 159–168.

Mulisch, M., & Welsch, U. (2010). Mikroskopische technik. Spektrum Akademischer Verlag.

Nasrin, M., Siddiqi, M. N. H., Masum, M. A., & Wares, M. A. (2012). Gross and histological studies of digestive tract of broilers during postnatal growth and development. Journal of the Bangladesh Agricultural University, 10(1), 69–77.

Okpe, C. G., Abiaezute, N. C., & Adigwe, A. (2016). Evaluation of the morphological adaptations of the small intestine of the African pied crow (Corvus albus). The Journal of Basic and Applied Zoology, 75, 54–60.

Palmquist-Gomes, P., Guadix, J. A., & Perez-Pomares, J. M. (2016). A chick embryo cryoinjury model for the study of embryonic organ development and repair. Differentiation, 91(4–5), 72–77.

Pandit, K., Dhote, B. S., Mahanta, D., Sathapathy, S., Tamilselvan, S., Mrigesh, M., & Mishra, S. (2018). Histological, histomorphometrical and histochemical studies on the large intestine of Uttara Fowl. International Journal of Current Microbiology and Applied Sciences, 7(3), 1477–1491.

Revajova, V., Slaminkova, Z., Gresakova, L., & Levkut, M. (2013). Duodenal morphology and immune responses of broiler chickens fed low doses of deoxynivalenol. Acta Veterinaria Brno, 82, 337–342.

Sasselli, V., Pachnis, V., & Burns, A. J. (2012). The enteric nervous system. Developmental Biology, 366, 64–73.

Scanes, C. G. (2017). Grand and less grand challenges in avian physiology. Frontiers in Physiology, 222, 1–5.

Scanesa, C. G., & Pierzchala-Koziec, K. (2014). Biology of the gastro-intestinal tract in poultry. Avian Biology Research, 7(4), 193–222.

Shah, R., Greyner, H., & Dzialowski, E. M. (2010). Autonomic control of heart rate and its variability during normoxia and hypoxia in emu (Dromaius novaehollandiae) hatchlings. Poultry Science, 89(1), 135–144.

Sheng, Y., & Zhu, L. (2018). The crosstalk between autonomic nervous system and blood vessels. International Journal of Physiology, Pathophysiology and Pharmacology, 10(1), 17–28.

Shyer, A. E., Tallinen, T., Nerurkar, N. L., Wei, Z., Gil, E. S., Kaplan, D. L., Tabin, C. J., & Mahadevan, L. (2013). Villification: How the gut gets its villi. Science, 342, 212–218.

Sittiya, J., & Yamauchi, K. (2014). Growth performance and histological intestinal alterations of sanuki cochin chickens fed diets diluted with untreated whole-grain paddy rice. The Journal of Poultry Science, 51(1), 52–57.

Sklan, D. (2001). Development of the digestive tract of poultry. World’s Poultry Science Journal, 57, 415–428.

Sokolov, V. I., & Chukalovskaja, R. N. (1980). Proliferativnye processy i citohimicheskie osobennosti kishechnogo jepitelija cypljat [Proliferative processes and cytochemical features of the intestinal epithelium of chickens]. Morphology of farm animals. Collection of Scientific Papers, 60, 74–78 (in Russian).

Svihus, B. (2014). Function of the digestive system. The Journal of Applied Poultry Research, 23(2), 306–314.

Taylor, E. W., Leite, C. A. C., Sartori, M. R., Wang, T., Abe, A. S., & Crossley, D. A. (2014). The phylogeny and ontogeny of autonomic control of the heart and cardiorespiratory interactions in vertebrates. The Journal of Experimental Biology, 217, 690–703.

Theerawatanasirikul, S., Koomkrong, N., Kayan, A., & Boonkaewwan, C. (2017). Intestinal barrier and mucosal immunity in broilers, Thai Betong, and native Thai Praduhangdum chickens. Turkish Journal of Veterinary and Animal Sciences, 41, 357–364.

Tsirtsikos, P., Fegeros, K., Balaskas, C., Kominakis, A., & Mountzouris, K. C. (2012). Dietary probiotic inclusion level modulates intestinal mucin composition and mucosal morphology in broilers. Poultry Science, 91, 1860–1868.

Tybinka, A., Zaitsev, O., & Blishch, G. (2016). Impact of autonomic tonus typological features on the duodenum structure of chickens. Veterinary Medicine – Open Journal, 1(1), 12–17.

Uesaka, T., Young, H. M., Pachnis, V., & Enomoto, H. (2016). Development of the intrinsic and extrinsic innervation of the gut. Developmental Biology, 417, 158–167.

Uni, Z., Ganot, S., & Sklan, D. (1998). Posthatch development of mucosal function in the broiler small intestine. Poultry Science, 77(1), 75–82.

Uni, Z., Tako, E., Gal-Garber, O., & Sklan, D. (2003). Morphological, molecular, and functional changes in the chicken small intestine of the late-term embryo. Poultry Science, 82, 1747–1754.

Varasteh, S., Braber, S., Akbari, P., Garssen, J., & Fink-Gremmels, J. (2015). Differences in susceptibility to heat stress along the chicken intestine and the protective effects of galacto-oligosaccharides. PLoS One, 10(9), e0172511.

Verdal, H., Mignon-Grasteau, S., Jeulin, C., Le Bihan-Duval, E., Leconte, M., Mallet, S., Martin, C., & Narcy, A. (2010). Digestive tract measurements and histological adaptation in broiler lines divergently selected for digestive efficiency. Poulty Science, 89, 1955–1961.

Wali, O. N., & Kadhim, K. K. (2014). Histomorphological comparison of proventriculus and small intestine of heavy and light line pre- and at hatching. International Journal of Animal and Veterinary Advances, 6(1), 40–47.

Wang, F., Zuo, Z., Chen, K., Gao, C., Yang, Z., Zhao, S., Li, J., Song, H., Peng, X., Fang, J., Cui, H., Ouyang, P., Zhou, Y., Shu, G., & Jing, B. (2018). Histopathological injuries, ultrastructural changes, and depressed TLR expression in the small intestine of broiler chickens with aflatoxin B1. Toxins, 10(4), 131–147.

Wijtten, P. J. A., Langhout, D. J., & Verstegen, M. W. A. (2012). Small intestine development in chicks after hatch and in pigs around the time of weaning and its relation with nutrition: A review. Acta agriculturae Scandinavica, A 62, 1–12.

Yamauchi, K. (2002). Review on chicken intestinal villus histological alterations related with intestinal function. The Journal of Poultry Science, 39(4), 229–242.

Yamauchi, K. (2007). Review of a histological intestinal approach to assessing the intestinal function in chickens and pigs. Animal Science Journal, 78, 356–370.

Yamauchi, K. E., Incharoen, T., & Yamauchi, K. (2010). The relationship between intestinal histology and function as shown by compensatory enlargement of remnant villi after midgut resection in chickens. The anatomical record, 293(12), 2071–2079.

Yang, P., Gandahi, J. A., Zhang, Q., Zhang, L. L., Bian, X. G., Wu, L., Liu, Y., & Chen, Q. S. (2013). Quantitative changes of nitrergic neurons during postnatal development of chicken myenteric plexus. Journal of Zhejiang University-Science B (Biomedicine and Biotechnology), 14(10), 886–895.

Yegani, M., & Korver, D. R. (2008). Factors affecting intestinal health in poultry. Poultry Science, 87(10), 2052–2063.

Zeng, Y.-J., Qiao, A.-K., Yu, J.-D., Zhao, J.-B., Liao, D.-H., Xu, X.-H., & Gregersen, H. (2003). Collagen fiber angle in the submucosa of small intestine and its application in gastroenterology. World Journal of Gastroenterology, 9(4), 804–807.

How to Cite
Tybinka, A., Blishch, H., & Shchebentovska, O. (2018). Influence of the type of autonomic tone on the volume of the mucous membrane of the small intestine of laying hens. Regulatory Mechanisms in Biosystems, 9(3), 453-459.