The aim of this study was to investigate the effect of Lactobacillus reuteri E81 (LRE) probiotic supplementation on heat stress responses in chukar partridges (Alectoris chukar). The birds were divided into two groups, one of which was exposed to heat stress (HS). Within each group, four subgroups, each including 64 birds, were created for the three treatment doses (200, 400 or 600 mg/kg) of LRE and the control. The experiment was started with day-old birds, kept at a temperature of 25 °C or 37 °C. After a 7-day adjustment period, the LRE supplementation lasted for 35 days. The levels of different adipokines, including visfatin (VF), adiponectin (ADP), chemerin (CHEM), as well as the concentration of plasma citrulline (CIT) and the levels of thyroid hormones (T3 and T4) and thyroid-stimulating hormone (TSH) in the blood were measured at 21 and 42 days of age. A significant correlation (P < 0.01) was found between LRE supplementation and the decrease in serum VF, ADP, CIT, T3 and T4 levels in partridges exposed to HS. On the other hand, no significant relationship was found between LRE supplementation and the serum CHEM and TSH levels (P > 0.05). We concluded that the addition of 600 mg/kg LRE is beneficial in preventing intestinal damage and inflammation provoked by HS.
Ahmed, R. G. (2017): Synergistic actions of thyroid–adipokines axis during development. Endocrinol. Metab. Syndr. 6, 2161–1017.
Ait-Belgnaoui, A. , Durand, H. , Cartier, C. , Chaumaz, G. , Eutamene, H. , Ferrier, L. , Houdeau, E. , Fioramonti, J. and Theodorou, V. (2012): Prevention of gut leakiness by a probiotic treatment leads to attenuated HPA response to an acute psychological stress in rats. Psychoneuroendocrinology 37, 1885–1895.
Al-Fataftah, A. R. and Abdelqader, A. (2014): Effects of dietary Bacillus subtilis on heat-stressed broilers performance, intestinal morphology and microflora composition. Anim. Feed Sci. Technol. 198, 279–285.
Alhenaky, A. , Abdelqader, A. , Abuajamieh, M. and Al-Fataftah, A. R. (2017): The effect of heat stress on intestinal integrity and Salmonella invasion in broiler birds. J. Therm. Biol. 70, 9–14.
Al-Sagan, A. A. , Khalil, S. , Hussein, E. O. S. and Attia, Y. A. (2020): Effects of fennel seed powder supplementation on growth performance, carcass characteristics, meat quality, and economic efficiency of broilers under thermoneutral and chronic heat stress conditions. Animals 10, 206–218.
AOAC (2005): Official methods of analysis of AOAC international. 18th ed. Association of Official Analytical Chemists, Rockville, MD, USA.
Awad, W. A. , Ghareeb, K. , Abdel-Raheem, S. and Böhm, J. (2009): Effects of dietary inclusion of probiotic and synbiotic on growth performance, organ weights, and intestinal histomorphology of broiler chickens. Poult. Sci. 88, 49–56.
Baldwin, S. , Hughes, R. J. , Hao Van, T. T. , Moore, R. J. and Stanley, D. (2018): At-hatch administration of probiotic to chickens can introduce beneficial changes in gut microbiota. PloS One 13, 1–14.
Barbe, A. , Bongrani, A. , Mellouk, N. , Estienne, A. , Kurowska, P. , Grandhaye, J. and Dupont, J. (2019): Mechanisms of adiponectin action in fertility: an overview from gametogenesis to gestation in humans and animal models in normal and pathological conditions. Int. J. Mol. Sci. 20, 1526–1563.
Baxter, M. F. , Latorre, J. D. , Dridi, S. , Merino-Guzman, R. , Hernandez-Velasco, X. , Hargis, B. M. and Tellez-Isaias, G. (2019): Identification of serum biomarkers for intestinal integrity in a broiler chicken malabsorption model. Front. Vet. Sci. 6, 1–6.
Bayraktar, B. and Tekce, E. (2020): Effect of probiotic supplementation on adipokine profile (visfatin, adiponectin and chemerin), intestinal (citrulline) and thyroid functions in Japanese quails subjected to heat stress (in German, with English abstract). Eur. Poult. Sci. 84, 2020. ISSN 1612-9199.
Chen, R. , Wang, C. , Meng, X. , Chen, H. , Thach, T. Q. , Wong, C. M. and Kan, H. (2013): Both low and high temperature may increase the risk of stroke mortality. Neurology 81, 1064–1070.
Crenn, P. , Coudray-Lucas, C. , Thuillier, F. , Cynober, L. and Messing, B. (2000): Postabsorptive plasma citrulline concentration is a marker of absorptive enterocyte mass and intestinal failure in humans. Gastroenterology 119, 1496-1505.
Crenn, P. , Messing, B. and Cynober, L. (2008): Citrulline as a biomarker of intestinal failure due to enterocyte mass reduction. Clin. Nutr. 27, 328–339.
Diot, M. , Reverchon, M. , Rame, C. , Froment, P. , Brillard, J. P. , Brière, S. and Dupont, J. (2015): Expression of adiponectin, chemerin and visfatin in plasma and different tissues during a laying season in turkeys. Reprod. Biol. Endocrinol. 13, 1–14.
Douglas-Escobar, M. , Elliott, E. and Neu, J. (2013): Effect of intestinal microbial ecology on the developing brain. JAMA Pediatr. 167, 374–379.
Elabd, E. M. Y. , Morsy, S. M. and Elmalt, H. A. (2018): Investigating of Moringa oleifera role on gut microbiota composition and inflammation associated with obesity following high fat diet feeding. Open Access Maced. J. Med. Sci. 6, 1359–1364.
Ferrante, M. C. , Raso, G. M. , Esposito, E. , Bianco, G. , Iacono, A. , Clausi, M. T. and Meli, R. (2011): Effects of non-dioxin-like polychlorinated biphenyl congeners (PCB 101, PCB 153 and PCB 180) alone or mixed on J774A.1 macrophage cell line: modification of apoptotic pathway. Toxicol. Lett. 202, 61–68.
Geraert, P. A. , Padilha, J. C. F. and Guillaumin, S. (1996): Metabolic and endocrine changes induced by chronic heat exposure in broiler chickens: growth performance, body composition and energy retention. Br. J. Nutr. 75, 195–204.
Gibson, G. R. (1998): Dietary modulation of the human gut microflora using probiotics. Br. J. Nutr. 80, S209–S212.
Goralski, K. B. , Jackson, A. E. , McKeown, B. T. and Sinal, C. J. (2019): More than an adipokine: the complex roles of chemerin signaling in cancer. Int. J. Mol. Sci. 20, 4778.
Gosselin, K. B. , Feldman, H. A. , Sonis, A. L. , Bechard, L. J. , Kellogg, M. D. , Gura, K. and Duggan, C. (2014): Serum citrulline as a biomarker of gastrointestinal function during hematopoietic cell transplantation (HCT) in children. J. Pediatr. Gastroenterol. Nutr. 58, 709–714.
Gradinaru, D. , Margina, D. , Borsa, C. , Ionescu, C. , Ilie, M. , Costache, M. and Prada, G. I. (2017): Adiponectin: possible link between metabolic stress and oxidative stress in the elderly. Aging Clin. Exp. Res. 29, 621–629.
Hendricks III, G. L. , Hadley, J. A. , Krzysik-Walker, S. M. , Prabhu, K. S. , Vasilatos-Younken, R. and Ramachandran, R. (2009): Unique profile of chicken adiponectin, a predominantly heavy molecular weight multimer, and relationship to visceral adiposity. Endocrinology 150, 3092–3100.
Heijtz, R. D. , Wang, S. , Anuar, F. , Qian, Y. , Björkholm, B. , Samuelsson, A. , Hibberd, M. L. , Forssberg, H. and Pettersson, S. (2011): Normal gut microbiota modulates brain development and behavior. Proc. Natl. Acad. Sci. U.S.A. 108, 3047–3052.
Hosseini, E. , Cheraghi, J. , Taheri, S. S. , Taherpour, K. , Kaviani, K. Z. and Rezazadeh, L. (2013): Thyroid hormones investigation under heat stress in broilers administered with probiotic (BIO-SAF) and prebiotic (BIO-MOS). Eur. J. Exp. Biol. 3, 562–567.
Incharoen, T. , Charoensook, R. , Onoda, S. , Tatrakoon, W. , Numthuam, S. and Pechkong, T. (2019): The effects of heat-killed Lactobacillus plantarum L-137 supplementation on growth performance, intestinal morphology, and immune-related gene expression in broiler chickens. Anim. Feed Sci. Tech. 257, 114272, 1–10.
Kőrösi-Molnár, A. , Kőrösi, L. , Balázs, B. and Gáspárdy, A. (2021): Effects of heat stress on the immune responses of chickens subjected to thermal manipulation in the pre-hatch period. Acta Vet. Hung. 69, 67–72.
Lara, L. J. and Rostagno, M. H. (2013): Impact of heat stress on poultry production. Animals 3, 356–369.
Lee, H. , Tu, T. H. , Park, B. S. , Yang, S. and Kim, J. G. (2019): Adiponectin reverses the hypothalamic microglial inflammation during short-term exposure to fat-rich diet. Int. J. Mol. Sci. 20, 1–12.
Lin, P. W. and Stoll, B. J. (2006): Necrotising enterocolitis. The Lancet 368, 1271–1283.
Logan, A. C. and Katzman, M. (2005): Major depressive disorder: probiotics may be an adjuvant therapy. Med. Hypotheses 64, 533–538.
Marchini, C. F. P. , Fernandes, E. A. , Nascimento, M. R. B. M. , Araújo, E. G. , Guimarães, E. C. , Bueno, J. P. R. and Café, M. B. (2018): The effect of cyclic heat stress applied to different broiler chicken brooding stages on animal performance and carcass yield. Braz. J. Poult. Sci. 20, 765–772.
Medina-Gómez, G. (2012): Mitochondria and endocrine function of adipose tissue. Best Pract. Res. Cl. En. 26, 791–804.
Morera, P. , Basiricò, L. , Hosoda, K. and Bernabucci, U. (2012): Chronic heat stress up-regulates leptin and adiponectin secretion and expression and improves leptin, adiponectin and insulin sensitivity in mice. J. Mol. Endocrinol. 48, 129–138.
Mountzouris, K. C. , Tsitrsikos, P. , Palamidi, I. , Arvaniti, A. , Mohnl, M. , Schatzmayr, G. and Fegeros, K. (2010): Effects of probiotic inclusion levels in broiler nutrition on growth performance, nutrient digestibility, plasma immunoglobulins, and cecal microflora composition. Poult. Sci. 89, 58–67.
Mousavi, A. A. M. S. , Hosseini, M. H. and Mirhosseini, S. A. (2018): A review of dietary probiotics in poultry. J. Appl. Biotechnol. Rep. 5, 48–54.
Mullur, R. , Liu, Y-Y. and Brent, G. A. (2014): Thyroid hormone regulation of metabolism. Physiol. Rev. 94, 355–382.
Ng, S. C. , Hart, A. L. , Kamm, M. A. , Stagg, A. J. and Knight, S. C. (2009): Mechanisms of action of probiotics: recent advances. Inflamm. Bowel Dis. 15, 300–310.
Nyoni, N. M. B. , Grab, S. and Archer, E. R. (2019): Heat stress and chickens: climate risk effects on rural poultry farming in low-income countries. Clim. Dev. 11, 83–90.
Ouwehand, A. C. , Kirjavainen, P. V. , Shortt, C. and Salminen, S. (1999): Probiotics: mechanisms and established effects. Int. Dairy J. 9, 43–52.
Pilz, S. , Mangge, H. , Obermayer-Pietsch, B. and März, W. (2007): Visfatin/pre-B-cell colony-enhancing factor: a protein with various suggested functions. J. Endocrinol. Invest. 30, 138–144.
Pourvali-Talatappeh, P. and Alipoor, E. (2019): Visfatin; a potential novel mediator of brown adipose tissue. Obes. Med. 15, 100122.
Pringsulaka, O. , Rueangyotchanthana, K. , Suwannasai, N. , Watanapokasin, R. , Amnueysit, P. , Sunthornthummas, S. and Rangsiruji, A. (2015): In vitro screening of lactic acid bacteria for multi-strain probiotics. Livest. Sci. 174, 66–73.
Rongvaux, A. , Shea, R. J. , Mulks, M. H. , Gigot, D. , Urbain, J. , Leo, O. and Andris, F. (2002): Pre-B-cell colony-enhancing factor, whose expression is up-regulated in activated lymphocytes, is a nicotinamide phosphoribosyltransferase, a cytosolic enzyme involved in NAD biosynthesis. Eur. J. Immunol. 32, 3225–3234.
Saleh, K. M. and Al-Zghoul, M. B. (2019): Effect of acute heat stress on the mRNA levels of cytokines in broiler chickens subjected to embryonic thermal manipulation. Animal 9, 1–13.
Sen, S. , Ingale, S. L. , Kim, Y. W. , Kim, J. S. , Kim, K. H. , Lohakare, J. D. and Chae, B. J. (2012): Effect of supplementation of Bacillus subtilis LS 1-2 to broiler diets on growth performance, nutrient retention, caecal microbiology and small intestinal morphology. Res. Vet. Sci. 93, 264–268.
Sinha, R. A. , Singh, B. K. and Yen, P. M. (2018): Direct effects of thyroid hormones on hepatic lipid metabolism. Nat. Rev. Endocrinol. 14, 259–269.
St-Pierre, N. R. , Cobanov, B. and Schnitkey, G. (2003): Economic losses from heat stress by US livestock industries. J. Dairy Sci. 86, E52–E77.
Sumathi, T. , Asha, D. , Nagarajan, G. , Sreenivas, A. and Nivedha, R. (2016): L-Theanine alleviates the neuropathological changes induced by PCB (Aroclor 1254) via inhibiting upregulation of inflammatory cytokines and oxidative stress in rat brain. Environ. Toxicol. Pharmacol. 42, 99–117.
Tao, X. , Zhang, Z. Y. , Dong, H. , Zhang, H. and Xin, H. (2006): Responses of thyroid hormones of market-size broilers to thermoneutral constant and warm cyclic temperatures. Poult. Sci. 85, 1520–1528.
Tsao, T. S. , Tomas, E. , Murrey, H. E. , Hug, C. , Lee, D. H. , Ruderman, N. B. and Lodish, H. F. (2003): Role of disulfide bonds in Acrp30/Adiponectin structure and signaling specificity: different oligomers activate different signal transduction pathways. J. Biol. Chem. 278, 50810–50817.
Wang, Y. J. , Zhao, J. L. , Lau, W. B. , Liu, J. , Guo, R. and Ma, X. L. (2017): Adipose tissue-derived cytokines, CTRPs as biomarkers and therapeutic targets in metabolism and the cardiovascular system. Vessel Plus 1, 202–212.
Wittamer, V. , Franssen, J. D. , Vulcano, M. , Mirjolet, J. F. , Le Poul, E. , Migeotte, I. and Mantovani, A. (2003): Specific recruitment of antigen-presenting cells by chemerin, a novel processed ligand from human inflammatory fluids. J. Exp. Med. 198, 977–985.
Xu, Y. , Lai, X. , Li, Z. , Zhang, X. and Luo, Q. (2018): Effect of chronic heat stress on some physiological and immunological parameters in different breed of broilers. Poult. Sci. 97, 4073–4082.
Yadav, S. and Jha, R. (2019): Strategies to modulate the intestinal microbiota and their effects on nutrient utilization, performance, and health of poultry. J. Anim. Sci. Biotechnol. 10, 1–11.
Zabel, B. A. , Silverio, A. M. and Butcher, E. C. (2005): Chemokine-like receptor 1 expression and chemerin-directed chemotaxis distinguish plasmacytoid from myeloid dendritic cells in human blood. J. Immunol. Res. 174, 244–251.
Zhang, R. , Zhou, M. , Tu, Y. , Zhang, N. F. , Deng, K. D. , Ma, T. and Diao, Q. Y. (2016): Effect of oral administration of probiotics on growth performance, apparent nutrient digestibility and stress-related indicators in Holstein calves. J. Anim. Physiol. An. N. 100, 33–38.
Zhou, Z. , Chen, H. , Ju, H. and Sun, M. (2018): Circulating chemerin levels and gestational diabetes mellitus: a systematic review and meta-analysis. Lipids Health Dis. 17, 169–180.