Abstract
Nutraceuticals have been evaluated for their ability to protect and heal the gastrointestinal mucosa, especially in adverse conditions. Thus, the present study evaluated the effect of a nutraceutical diet composed of bovine first milk secretion in the intestinal health of juvenile Piaractus mesopotamicus subjected to high stocking density. Juveniles (140 ± 10 g) distributed into 16 cages and stocked at 50 kg m−3 were fed twice daily with a pelleted and semi-purified diet containing nutraceutical food (NF) in increasing levels, being 0, 10, 20, and 30% of inclusion (n = 4). Quantification of goblet cells containing neutral, acidic (including sialo and sulfomucins) and acidic-neutral mucins, volume (Vv), and surface density (Sv) of the mucosa and thickness of the internal circular muscle layer was determined after 28 experimental days in the middle gut and rectum (RT). The apoptotic rate was analyzed qualitatively according to the intensity (high, medium, and low) of caspase-3 immunostaining in epithelial cells. Performance parameters were not affected by the inclusion of NF in the diets. Juveniles fed 20% and 30% of NF showed a lower number of goblet cells containing sulfomucins than juveniles fed 0% and 10% of NF (P = 0.01) in the RT. In the last segment of the middle gut (S2) and RT, the intensity of caspase-3 immunostaining in enterocytes was inversely related to the concentration of NF added in the diet. The inclusion of 20% and 30% of nutraceutical food in the diet of P. mesopotamicus reduced the rate of apoptosis and the number of goblet cells containing sulfomucin in the last intestinal segments of juveniles subjected to high stocking density, mitigating the effects caused by the adverse condition and being, therefore, beneficial for intestinal health.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Abdel-Tawwab M, Monier MN, Hoseinifar SH, Faggio C (2019) Fish response to hypoxia stress: growth, physiological, and immunological biomarkers. Fish Physiol Biochem 45:997–1013. https://doi.org/10.1007/s10695-019-00614-9
Appukutty M, Radhakrishnan AK, Ramasamy K, Ramasamy R, Majeed ABA, Noor MI, Safii NS, Koon PB, Chinna K, Haleagrahara N (2012) Colostrum protects against exercise - induced oxidative stress in skeletal muscle in mice. BMC Res Notes 5:649–656. https://doi.org/10.1186/1756-0500-5-649
Baddeley AJ, Gundersen HJ, Cruz-Orive LM (1986) Estimation of surface areas from vertical sections. J Microsc 142:259–276. https://doi.org/10.1111/j.1365-2818.1986.tb04282.x
Baeverfjord G, Krogdahl Å (1996) Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. J Fish Dis 19:375–387. https://doi.org/10.1046/j.1365-2761.1996.d01-92.x
Bagwe S, Tharappel LJP, Kaur G, Buttar HS (2015) Bovine colostrum: an emerging nutraceutical. J Complement Integr Med 12:175–185. https://doi.org/10.1515/jcim-2014-0039
Baldisseroto B, Gomes LC (2005) Espécies nativas para piscicultura no Brasil. UFSM, Santa Maria, p 470
Bojarski C, Bendfeldt K, Gitter AH, Mankertz J, Fromm M, Wagner S, Riecken E-O, Schulzke J-D (2006) Apoptosis and intestinal barrier function. Ann N Y Acad Sci 915:270–274. https://doi.org/10.1111/j.1749-6632.2000.tb05252.x
Castagliuolo I, Wershil BK, Karalis K, Pasha A, Nikulasson ST, Pothoulakis C (1998) Colonic mucin release in response to immobilization stress is mast cell dependent. Am J Physiol Liver Physiol 274:G1094–G1100. https://doi.org/10.1152/ajpgi.1998.274.6.G1094
Catinean A, Neag MA, Muntean DM, Bocsan IC, Buzoianu AD (2018) An overview on the interplay between nutraceuticals and gut microbiota. PeerJ 6:e4465. https://doi.org/10.7717/peerj.4465
Cencik A, Chingwaru W (2010) The role of functional foods, nutraceuticals, and food supplements in intestinal health. Nutrients 2:611–624. https://doi.org/10.3390/nu2060611
Choi HS, Ko YG, Lee JS, Kwon OY, Kim S-K, Cheong C, Jang K-H, Kang SA (2010) Neuroprotective effects of consuming bovine colostrum after focal brain ischemia/reperfusion injury in rat model. Nutr Res Pract 4:196–202. https://doi.org/10.4162/nrp.2010.4.3.196
CONCEA (2013) Diretrizes da Prática de Eutanásia do Concea. MCTI/CONCEA, Brasília/DF, p 54
Curry SM, Schwartz KJ, Yoon KJ, Gabler NK, Burrough ER (2017) Effects of porcine epidemic diarrhea virus infection on nursery pig intestinal function and barrier integrity. VetMicrobiol 211:58–66. https://doi.org/10.1016/j.vetmic.2017.09.021
da Cruz TMP, Moretti DB, Nordi WM, Cyrino JEP, Machado-Neto R (2017) Dietary lyophilized colostrum alters distribution of goblet cells and the intestinal epithelium of Piaractus mesopotamicus. Aquaculture 468:286–292. https://doi.org/10.1016/j.aquaculture.2016.10.032
Deplancke B, Gaskins HR (2001) Microbial modulation of innate defense: goblet cells and the intestinal mucus layer. Am J Clin Nutr 73:1131S–1141S. https://doi.org/10.1093/ajcn/73.6.1131S
Jerez-Cepa I, Marín-Rincón A, Martínez-Rodríguez G, Ruiz-Jarabo I, Mancera JM (2020) A natural additive in the diet to improve growth and reduce energy expenditure of gilthead seabream (Sparus aurata L.): attenuation of high stocking density stress responses. Aquaculture 524:735263. https://doi.org/10.1016/j.aquaculture.2020.735263
Kim J, Park H, Kim K-W, Hwang I-K, Kim D-H, Oh CW, Lee JS, Kang J-C (2017) Growth performance, oxidative stress, and non-specific immune responses in juvenile sablefish, Anoplopoma fimbria, by changes of water temperature and salinity. Fish Physiol Biochem 43:1421–1431. https://doi.org/10.1007/s10695-017-0382-z
Kumar N, Krishnani KK, Singh NP (2020) Effect of zinc on growth performance and cellular metabolic stress of fish exposed to multiple stresses. Fish Physiol Biochem 46:315–329. https://doi.org/10.1007/s10695-019-00719-1
Kwon OY, Lee JS, Choi HS, Hong HP, Jang KH, Paek JH, Ah Kan S, Ko YG (2010) Antioxidant and anticytokine effects of bovine colostrum in intestinal ischemia/reperfusion injured rat model. Food Sci Biotechnol 19:1295–1301. https://doi.org/10.1007/s10068-010-0185-9
Marchbank T, Davison G, Oakes JR, Ghatei MA, Patterson M, Moyer MP, Playford RJ (2011) The nutraceutical bovine colostrum truncates the increase in gut permeability caused by heavy exercise in athletes. Am J Physiol Liver Physiol 300:G477–G484. https://doi.org/10.1152/ajpgi.00281.2010
Mazzon E, Sturniolo GC, Puzzolo D, Frisina N, Fries W (2002) Effect of stress on the paracellular barrier in the rat ileum. Gut 51:507–513. https://doi.org/10.1136/gut.51.4.507
Merola N, De Souza JH (1988) Preliminary studies on the culture of pacu, Colossoma mitrei, in floating cages: effect of stocking density and feeding rate on growth performance. Aquaculture 68:243–248. https://doi.org/10.1016/0044-8486(88)90356-0
Møller HK, Thymann T, Fink LN, Frokiaer H, Kvistgaard AS, Sangild PT (2011) Bovine colostrum is superior to enriched formulas in stimulating intestinal function and necrotising enterocolitis resistance in preterm pigs. Br J Nutr 105(1):44–53. https://doi.org/10.1017/S0007114510003168
Moretti DB, Nordi WM, Machado-Neto R (2019) Redox balance and tissue development of juvenile Piaractus mesopotamicus subjected to high stocking density and fed dry diets containing nutraceutical food. Latin Am J Aq Res 47:423–432. https://doi.org/10.3856/vol47-issue3-fulltext-4
Myers RB, Fredenburgh JL, Grizzle WE (2008) Carbohydrates. In: Bancroft JD, Gamble M (eds) Theory and pratice of histological techniques. Churchill Livingstone, Edinburgh, pp 161–186
Nagata S (2018) Apoptosis and clearance of apoptotic cells. Ann Rev Immunol 36:489–517. https://doi.org/10.1146/annurev-immunol-042617-053010
Oliveira KRB, Segura JG, Oliveira BA, Medeiros ACL, Zimba RD, Viegas EMM (2020) Distillers’ dried grains with soluble in diets for Pacu, Piaractus mesopotamicus juveniles: growth performance, feed utilization, economic viability, and phosphorus release. An Feed Sci Technol 262:114393. https://doi.org/10.1016/j.anifeedsci.2020.114393
Ostaszewska T, Dabrowski K, Palacios ME, Olejniczak M, Wieczorek M (2005) Growth and morphological changes in the digestive tract of rainbow trout (Oncorhynchus mykiss) and pacu (Piaractus mesopotamicus) due to casein replacement with soybean proteins. Aquaculture 245:273–286. https://doi.org/10.1016/j.aquaculture.2004.12.005
Oyarzún R, Paredes R, Saravia J, Morera FJ, Muñoz JLP, Ruiz-Jarabo I, Mancera JM, Vargas-Chacoff L (2020) Stocking density affects the growth performance, intermediary metabolism, osmoregulation, and response to stress in Patagonian blennie Eleginops maclovinus. Aquaculture 515:734565. https://doi.org/10.1016/j.aquaculture.2019.734565
Panettieri V, Chatzifotis S, Messina CM, Olivotto I, Manuguerra S, Randazzo B, Ariano A, Bovera F, Santulli A, Severino L, Piccolo G (2020) Honey bee pollen in meagre (Argyrosomus regius) juvenile diets: effects on growth, diet digestibility, intestinal traits, and biochemical markers related to health and stress. Animals 10:231
Park SYS, Jeong A-J, Kim G-Y, Jo A, Lee JE, Leem S-H, , Yoon J-H, Ye SK, Chung JW (2017) Lactoferrin protects human mesenchymal stem cells from oxidative stress-induced senescence and apoptosis. J Microbiol Biotechnol 27:1877–1884. https://doi.org/10.4014/jmb.1707.07040
Rajamanickam K, Gogoi J, Leela V, Suganya G (2016) Current and future prospects of colostrum—Indian ethnic food supplement. Res Rev J Dairy Sci Technol 5:23–28p
Rathe M, Müller K, Sangild PT, Husby S (2014) Clinical applications of bovine colostrum therapy: a systematic review. Nutr Rev 72:237–254. https://doi.org/10.1111/nure.12089
Refaey MM, Li D, Tian X, Zhang Z, Zhang X, Li L, Tang R (2018) High stocking density alters growth performance, blood biochemistry, intestinal histology, and muscle quality of channel catfish Ictalurus punctatus. Aquaculture 492:73–81. https://doi.org/10.1016/j.aquaculture.2018.04.003
Reyes-Becerril M, Angulo C, Sanchez V, Vázquez-Martínez J, López MG (2019) Antioxidant, intestinal immune status and anti-inflammatory potential of Chenopodium ambrosioides L. in fish: in vitro and in vivo studies. Fish & Shellfish Immunology 86:420–428. https://doi.org/10.1016/j.fsi.2018.11.059
Rodrigues APO, Pauletti P, Kindlein L, Delgado EF, Cyrino JEP, Machado-Neto R (2010a) Intestinal histomorphology in Pseudoplatystoma fasciatum fed bovine colostrum as source of protein and bioactive peptides. Sci Agric 67:524–530. https://doi.org/10.1590/S0103-90162010000500005
Rodrigues LA, Fernandes JBK, Fabregat TEHP, Sakomura NK (2010b) Productive performance, body composition and physiological parameters of pacu fed increasing levels of fiber. Pesq Agrop Bras 45:897–902. https://doi.org/10.1590/S0100-204X2010000800016
Rosengren M, Thörnqvist P-O, Winberg S, Sundell K (2018) The brain-gut axis of fish: rainbow trout with low and high cortisol response show innate differences in intestinal integrity and brain gene expression. Gen Comp Endocrinol 257:235–245. https://doi.org/10.1016/j.ygcen.2017.09.020
Santos J, Saunders PR, Hanssen NPM, Yang PC, Yates D, Groot JA, Perdue MH (1999) Corticotropin-releasing hormone mimics stress-induced colonic epithelial pathophysiology in the rat. Am J Physiol Liver Physiol 277:G391–G399. https://doi.org/10.1152/ajpgi.1999.277.2.G391
Santos J, Benjamin M, Yang P-C, Prior T, Perdue MH (2000) Chronic stress impairs rat growth and jejunal epithelial barrier function: role of mast cells. Am J Physiol Liver Physiol 278:G847–G854. https://doi.org/10.1152/ajpgi.2000.278.6.G847
Seth R, Das A (2011) Colostrum powder and its health benefits. In: Sharma R, Mann B (eds) Chemical analysis of value added dairy products and their quality assurance. Division of Dairy Chemistry, National Dairy Research Institute, Karnal, Haryana, India, pp 59–67
Söderholm JD, Perdue MH (2001) II. Stress and intestinal barrier function. Am J Physiol Liver Physiol 280:G7–G13. https://doi.org/10.1152/ajpgi.2001.280.1.G7
Tan C, Sun D, Tan H, Liu W, Luo G, Wei X (2018) Effects of stocking density on growth, body composition, digestive enzyme levels and blood biochemical parameters of anguilla marmorata in a recirculating aquaculture system. Turkish J Fish Aquat Sci 18:9–16. https://doi.org/10.4194/1303-2712-v18_1_02
Trenzado CE, Carmona R, Merino R, García-Gallego M, Furné M, Domezain A, Sanz A (2018) Effect of dietary lipid content and stocking density on digestive enzymes profile and intestinal histology of rainbow trout (Oncorhynchus mykiss). Aquaculture 497:10–16. https://doi.org/10.1016/j.aquaculture.2018.07.031
Verma N, Kumari U, Mittal S, Mittal AH (2017) Effect of asiaticoside on the healing of skin wounds in the carp Cirrhinus mrigala: an immunohistochemical investigation. Tissue Cell 49:734–745. https://doi.org/10.1016/j.tice.2017.10.005
Williams JM, Duckworth CA, Burkitt MD, Watson AJM, Campbell BJ, Pritchard DM (2015) Epithelial cell shedding and barrier function: a matter of life and death at the small intestinal villus tip. Vet Pathol 52:445–455. https://doi.org/10.1177/0300985814559404
Yang Y, Zhang Y, Wang L, Lee S (2017) Levistolide a induces apoptosis via ROS-mediated ER stress pathway in colon cancer cells. Cell Physiol Biochem 42:929–938. https://doi.org/10.1159/000478647
Zeng LQ, Li FJ, Li XM, Cao ZD, Fu SJ, Zhang YG (2012) The effects of starvation on digestive tract function and structure in juvenile southern catfish (Silurus meridionalis Chen). Comp Biochem Physiol Part A Mol Integr Physiol 162:200–211. https://doi.org/10.1016/j.cbpa.2012.02.022
Funding
Authors are grateful to the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP) for funding the project [grant #2015/16151-3, #2015/06583-3 and #2014/14937-7, São Paulo Research Foundation (FAPESP)].
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
Moretti, D.B. has received research grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (grant #2014/14937-7 and # 2015/06583-3). Pontin, M.C.F. has received research grants from Fundação de Amparo à Pesquisa do Estado de São Paulo (grant #2015/16151-3).
Ethical approval
All applicable international, national, and/or institutional guidelines for the care and use of animals were followed by the authors (approved by the Ethics Committee on Animal Use‑CEUA, at the Luiz de Queiroz Campus, University of São Paulo, Brazil, registered as No. 2015-13).
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Pontin, M.C.F., Nordi, W.M., Pampolini, J. et al. Protective effect of nutraceutical food on the intestinal mucosa of juvenile pacu Piaractus mesopotamicus under high stocking density. Aquacult Int 28, 1981–1995 (2020). https://doi.org/10.1007/s10499-020-00570-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10499-020-00570-9