Abstract
Ammonia (NH3) is a toxic, environmental pollutant, and irritant gas. Previous studies reported the toxic effects of NH3 which led to inflammation in various organs of chicken. However, the exact mechanism of NH3-induced inflammation in chicken lymphoid organs bursa of fabricius (BF) and thymus is still elusive. Thus, this study was designed to investigate NH3-induced inflammation in chicken BF and thymus. Experimental chickens were divided into low (5.0 mg/m3), middle (10.0–15.0 mg/m3), and high (20.0–45.0 mg/m3) NH3-treated groups. To investigate NH3-induced inflammation in chicken’s BF and thymus, histological observation, NO content and iNOS activity, inflammatory cytokine contents, and mRNA levels were performed by light microscopy, microplate spectrophotometer, ELISA assay, and qRT-PCR. The finding of the present study showed that NH3 exposure reduced BF and thymus index, increased nitric oxide (NO) content and inducible nitric oxide synthase (iNOS) activity, inflammatory cytokine contents and mRNA levels of nuclear factor-kappa B (NF-κB), cyclooxygenase-2 (Cox-2), tumor necrosis factor alpha (TNF-α), interleukin 6 (IL-6), IL-10, IL-1β, IL-18, toll-like receptor 2A (TLR-2A), and iNOS. Histopathological examination revealed signs of inflammation including increased nuclear debris and vacuoles in the cortex and medulla of thymus and bursal follicles. Conclusively, our findings displayed that NH3 exposure affects the normal function of BF and thymus and led inflammation. The data provided a new ground for NH3-induced toxicity and risk assessment in chicken production.
Similar content being viewed by others
References
Aggarwal BB, Shishodia S, Sandur SK, Pandey MK, Sethi G (2006) Inflammation and cancer: how hot is the link? Biochem Pharmacol 72:1605–1621
Al-Sadi RM, Ma TY (2007) IL-1β causes an increase in intestinal epithelial tight junction permeability. J Immunol 178:4641–4649
An Y, Xing H, Zhang Y, Jia P, Gu X, Teng X (2019) The evaluation of potential immunotoxicity induced by environmental pollutant ammonia in broilers. Poult Sci 98(8):3165–3175
Anderson DP, Beard CW, Hanson RP (1966) Influence of poultry house dust, ammonia, and carbon dioxide on the resistance of chickens to Newcastle disease virus. Avian Dis 10:177–188
Ashton KJ, Reichelt ME, Mustafa SJ, Teng B, Ledent C, Delbridge LMD et al (2016) Transcriptomic effects of adenosine 2A receptor deletion in healthy and endotoxemic murine myocardium. Purinergic Signal 13(1):1–23
Atreya I, Atreya R, Neurath MF (2008) NF-κB in inflammatory bowel disease. J Intern Med 263:591–596
Avitsur R, Stark JL, Dhabhar FS, Kramer KA (2003) Social experience alters the response to social stress in mice. Brain Behav Immun 17:426–437
Bartolomucci A, Palanza P, Sacerdote P, Panerai AE, Sgoifo A, Dantzer R, Parmigiani S (2005) Social factors and individual vulnerability to chronic stress exposure. Neurosci Biobehav Rev 29(1):67–81
Bauer SE, Tsigaridis K, Miller R (2016) Significant atmospheric aerosol pollution caused by world food cultivation: agricultural aerosol pollution. Geophys Res Lett 43(10):5394–5400
Beker A, Vanhooser SL, Swartzlander JH, Teeter RG (2004) Atmospheric ammonia concentration effects on broiler growth and performance. J Appl Poult Res 13:5–9
Bellaver B, Souza DG, Souza DO, Quincozessantos A (2017) Hippocampal astrocyte cultures from adult and aged rats reproduce changes in glial functionality observed in the aging brain. Mol Neurobiol 54(4):2969–2985
Beusen AHW, Bouwman AF, Heuberger PSC, Drecht GV, Hoek KWVD (2008) Bottom-up uncertainty estimates of global ammonia emissions from global agricultural production systems. Atmos Environ 42(24):6067–6077
Braissant O, Mclin VA, Cudalbu C (2013) Ammonia toxicity: from head to toe? J Inherit Metab Dis 36(4):595–612
Charles DR, Payne CG (1966) The influence of graded levels of atmospheric ammonia on chickens: 2. Effects on performance of laying hens. Br Poult Sci 7:189–198
Chen D, Miao Z, Peng M, Xing H, Zhang H, Teng X (2019) The co-expression of circRNA and mRNA in the thymuses of chickens exposed to ammonia. Ecotoxicol Environ Saf 176:146–152
Cho R, Lin W, Wang C, Yang C, Hsiao L, Lin C, Yang C (2018) Heme oxygenase-1 induction by rosiglitazone via PKCα/AMPKα/p38 MAPKα/SIRT1/PPARγ pathway suppresses lipopolysaccharide-mediated pulmonary inflammation. Biochem Pharmacol 148:222–237
Dasarathy S, Mookerjee RP, Rackayova V, Thrane VR, Vairappan B, Ott P, Rose CF (2017) Ammonia toxicity: from head to toe? Metab Brain Dis 32(2):529–538
Ghareeb K, Awad WA, Soodoi C, Sasgary S, Strasser A, Böhm J (2013) Effects of feed contaminant deoxynivalenol on plasma cytokines and mRNA expression of immune genes in the intestine of broiler chickens. PLoS One 8(8):e71492
Goodman WA, Omenetti S, Date D, Di ML, De SC, Kim GD et al (2016) KLF6 contributes tomyeloid cell plasticity in the pathogenesis of intestinal inflammation. Mucosal Immunol 9(5):1250–1262
Hseu YC, Wu FY, Wu JJ, Chen JY, Chang WH, Lu FJ, Lai YC, Yang HL (2006) Anti-inflammatory potential of Antrodia Camphorata through inhibition of iNOS, COX-2 and cytokines via the NF-κB pathway. Int Immunopharmacol 5(13–14):1914–1925
Hu Y, Lou J, Mao YY, Lai TW, Liu LY, Zhu C et al (2016) Activation of MTOR in pulmonary epithelium promotes LPS-induced acute lung injury. Autophagy 12(12):2286–2299
Hu X, Chi Q, Wang D, Chi X, Teng X, Li S (2018) Hydrogen sulfide inhalation-induced immune damage is involved in oxidative stress, inflammation, apoptosis and the Th1/Th2 imbalance in broiler bursa of Fabricius. Ecotoxicol Environ Saf 164:201–209
Hu X, Chi Q, Liu Q, Wang D, Zhang Y, Li S (2019) Atmospheric H2S triggers immune damage by activating the TLR-7/MyD88/NF-κB pathway and NLRP3 inflammasome in broiler thymus. Chemosphere 237:124427
Huang H, Liu Y, Daniluk J, Wang H, Ji B, Logsdon CD (2013) Elevated acinar cell NF-κB activity increases pancreatitis severity. Pancreatology 13(2):e9
Ishfaq M, Zhang W, Ali Shah SW, Wu Z, Wang J, Ding L, Li J (2020) The effect of mycoplasma gallisepticum infection on energy metabolism in chicken lungs: through oxidative stress and inflammation. Microb Pathog 138:103848
Kristensen HH, Wathes CM (2000) Ammonia and poultry welfare: a review. Worlds Poult Sci J 56(03):235–245
Lelieveld J, Evans JS, Fnais M, Giannadaki D, Pozzer A (2015) The contribution of outdoor air pollution sources to premature mortality on a global scale. Nature 525(7569):367–371
Li J, Qiao Z, Hu W, Zhang W, Shah SWA, Ishfaq M (2019) Baicalin mitigated mycoplasma gallisepticum-induced structural damage and attenuated oxidative stress and apoptosis in chicken thymus through the Nrf2/HO-1 defence pathway. Vet Res 50(1):83
Mihina Š, Sauter M, Palkovičová Z, Karandušovská I, Brouček J (2012) Concentration of harmful gases in poultry and pig houses. Anim Sci Paper Rep 30:395–406
Miles DM, Branton SL, Lott BD (2004) Atmospheric ammonia is detrimental to the performance of modern commercial broilers. Poult Sci 83:1650–1654
Miles DM, Rowe DE, Cathcart TC (2011) Litter ammonia generation: moisture content and organic versus inorganic bedding materials. Poult Sci 90:1162–1169
Napetschnig J, Wu H (2013) Molecular basis of NF-κB signaling. Annu Rev Biophys 42:443–468
Naseem S, King AJ (2018) Ammonia production in poultry houses can affect health of humans, birds, and the environment—techniques for its reduction during poultry production. Environ Sci Pollut Res 25(16):15269–15293
Nounou HA, Deif MM, Shalaby MA (2012) Effect of flaxseed supplementation and exercise training on lipid profile, oxidative stress and inflammation in rats with myocardial ischemia. Lipids Health Dis 11:129
Osborne LC, Abraham N (2010) Regulation of memory T cells by γc cytokines. Cytokine 50(2):105–113
Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9):e45
Quarles CCL, Kling HF (1974) Evaluation of ammonia and infectious bronchitis vaccination stress on broiler performance and carcass quality. Poult Sci 53:1592–1596
Quinteiro-Filho WM, Ribeiro A, Ferraz-de-Paula V, Pinheiro ML (2010) Heat stress impairs performance parameters, induces intestinal injury, and decreases macrophage activity in broiler chickens. Poult Sci 89:1905–1914
Quinteiro-Filho WM, Rodrigues MV, Ribeiro A, Ferraz-de-Paula V (2012) Acute heat stress impairs performance parameters and induces mild intestinal enteritis in broiler chickens: role of acute hypothalamic-pituitary-adrenal axis activation. J Anim Sci 90:1986–1994
Rao M, Yang W, Seifalian AM, Winslet MC (2004) Role of cyclooxygenase-2 in the angiogenesis of colorectal cancer. Int J Color Dis 19(1):1–11
Salzanoa S, Checconia P, Hanschmannc EM (2014) Linkage of inflammation and oxidative stress via release of glutathionylated peroxiredoxin-2, which acts as a danger signal. Proc Natl Acad Sci U S A 111(33):12157–12162
Santos CL, Bobermin LD, Souza DG, Bellaver B, Bellaver G, Arús BA, Souza DO, Gonçalves CA, Quincozes-Santos A (2015) Lipoic acid and N-acetylcysteine prevent ammonia induced inflammatory response in C6 astroglial cells: the putative role of ERK and HO1 signaling pathways. Toxicol in Vitro 29(7):1350–1357
Seidavi A, Dadashbeiki M, Alimohammadi-Saraei MH, van den Hoven R, Payan-Carreira R, Laudadio V, Tufarelli V (2017) Effects of dietary inclusion level of a mixture of probiotic cultures and enzymes on broiler chickens immunity response. Environ Sci Pollut Res 24(5):4637–4644
Shah SWA, Chen J, Han Q, Xu Y, Ishfaq M, Teng X (2020) Ammonia inhalation impaired immune function and mitochondrial integrity in the broilers bursa of fabricius: implication of oxidative stress and apoptosis. Ecotoxicol Environ Saf 190:110078
Sharma JN, Al-Omran A, Parvathy SS (2007) Role of nitric oxide in inflammatory diseases. Inflammopharmacology 15:252–259
Sutton MA, Stefan R, Riddick SN, Ulrike D, Eiko N, Theobald MR, Dore AJ (2013) Towards a climate-dependent paradigm of ammonia emission and deposition. Philos Trans R Soc Lond 368(1621):20130166
Tanaka T, Kishimoto T (2012) Targeting interleukin 6: all the way to treat autoimmune and inflammatory diseases. Int J Biol Sci 8:1227–1236
Vitkina TI, Yankova VI, Gvozdenko TA, Kuznetsov VL, Krasnikov DV, Nazarenko AV, Golokhvast KS (2016) The impact of multi-walled carbon nanotubes with different amount of metallic impurities on immunometabolic parameters in healthy volunteers. Food Chem Toxicol 87:138–147
Wang YM, Meng QP, Guo YM, Wang YZ, Wang Z, Yao ZL, Shan TZ (2010) Effect of atmospheric ammonia on growth performance and immunological response of broiler chickens. J Anim Vet Adv 9:2802–2806
Wang J, Yi M, Chen X, Muhammad I, Liu F, Li R, Li J, Li J (2016) Effects of colistin on amino acid neurotransmitters and blood-brain barrier in the mouse brain. Neurotoxicol Teratol 55:32–37
Wei FX, Hu XF, Xu B (2015) Ammonia concentration and relative humidity in poultry houses affect the immune response of broilers. Genet Mol Res 14:3160–3169
Weng X, He Y, Visvabharathy L, Liao CM, Tan X, Balakumar A, Wang CR (2017) Crosstalk between type II NKT cells and T cells leads to spontaneous chronic inflammatory liver disease. J Hepatol 67:791–800
Wu YN, Yan FF, Hu JY, Chen H, Tucker CM, Green AR, Cheng HW (2017) The effect of chronic ammonia exposure on acute-phase proteins, immunoglobulin, and cytokines in laying hens. Poult Sci 96(6):1524–1530
Xie W, Lv A, Li R, Tang Z, Ma D, Huang X, Zhang R, Ge M (2018) Agaricus blazei murill polysaccharides protect against cadmium-induced oxidative stress and inflammatory damage in chicken spleens. Biol Trace Elem Res 184:247–258
Xing H, Peng M, Li Z, Chen J, Zhang H, Teng X (2019) Ammonia inhalation-mediated mir-202-5p leads to cardiac autophagy through PTEN/AKT/mTOR pathway. Chemosphere 235:858–866
Xu Y, Li Z, Zhang S, Zhang H, Teng X (2020) miR-187-5p/apaf-1 axis was involved in oxidative stress-mediated apoptosis caused by ammonia via mitochondrial pathway in chicken livers. Toxicol Appl Pharmacol 388:114869
Zhao P, Guo Y, Zhang W, Chai H, Xing H, Xing M (2017) Neurotoxicity induced by arsenic in Gallus gallus: regulation of oxidative stress and heat shock protein response. Chemosphere 166:238–245
Zimmer J, Weitnauer M, Boutin S, Küblbeck G, Thiele S, Walker P et al (2016) Nuclear localization of suppressor of cytokine signaling-1 regulates local immunity in the lung. Front Immunol 7:514
Funding
The present study was supported by National Natural Science Foundation of China (No. 31972612), National Key Research and development Program of China (No. 2016YFD0500501).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
Additional information
Responsible editor: Mohamed Abdel-Daim
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
All authors have read the manuscript and agreed to submit it in its current form for consideration for publication in the journal.
Rights and permissions
About this article
Cite this article
Shah, S.W.A., Ishfaq, M., Nasrullah, M. et al. Ammonia inhalation-induced inflammation and structural impairment in the bursa of fabricius and thymus of broilers through NF-κB signaling pathway. Environ Sci Pollut Res 27, 11596–11607 (2020). https://doi.org/10.1007/s11356-020-07743-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-020-07743-2