Abstract
NaCl is the main component of freshwater salinization. High NaCl concentration in drinking water can cause pulmonary hypertension syndrome (PHS) and kidney damage in broilers. To explore the effect of NaCl in drinking water on broilers’ kidneys, this study divided 80 chickens into four groups. With the control group fed with pure water, broiler chickens were fed with fresh water (FW, NaCl 1 g/L), low salt–contaminated water (L-SCW, NaCl 2.5 g/L), and high salt–contaminated water (H-SCW, NaCl 5 g/L). The results show that ascites heart index (AHI) and hematocrit (HCT) of broilers increase in L-SCW and H-SCW, the serum blood urea nitrogen and creatinine of broilers increase significantly, the kidney index increases, the kidney sections show vacuolar degeneration and fibrotic degeneration, and the TUNEL results show that the kidneys possess obvious apoptosis. In addition, the detection of RAAS-related genes (AGT gene in the liver, REN in the kidney, ACE in the lung) demonstrates that after using salt-contaminated water, the transcription levels of AGT, REN, and ACE rise significantly, and the concentration of angiotensin II (Ang II) also increases significantly. In order to verify the effect of Ang II on broiler kidneys, this research used exogenous Ang II to treat chicken embryonic kidney (CEK) cells. The results show that the cell activity of CEK decreased with the increase of the concentration of exogenous Ang II. Meanwhile, the flow cytometry assay shows that Ang II could promote the apoptosis of CEK cells. These results indicate that the salt-contaminated water can aggravate PHS and cause kidney damage. The mechanism may be related to the increase of Ang II.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Not applicable.
References
Brummermann M, Simon E (1990) Arterial hypotension in ducks adapted to high salt intake. J Comp Physiol B 160:127–136. https://doi.org/10.1007/bf00300944
Chaszczewska-Markowska M, Sagan M, Bogunia-Kubik K (2016) The renin-angiotensin-aldosterone system (RAAS) - physiology and molecular mechanisms of functioning. Postepy Hig Med Dosw (Online) 70:917–927. https://doi.org/10.5604/17322693.1218180
Chatelanat O, Pechère-Bertschi A, Ponte B (2019) Salt sensitivity and hypertension. Rev Med Suisse 15:1625–1628
Chaves Hernández A (2014) Poultry and avian diseases. Encyclopedia of Agriculture and Food Systems.:504–520. https://doi.org/10.1016/B978-0-444-52512-3.00183-2
Chen Y, Lin L, Tao X, Song Y, Cui J, Wan J (2019) The role of podocyte damage in the etiology of ischemia-reperfusion acute kidney injury and post-injury fibrosis. BMC Nephrol 20:106. https://doi.org/10.1186/s12882-019-1298-x
Crossley DA 2nd, Jonker SS, Hicks JW, Thornburg KL (2010) Maturation of the angiotensin II cardiovascular response in the embryonic White Leghorn chicken (Gallus gallus). J Comp Physiol B 180:1057–1065. https://doi.org/10.1007/s00360-010-0473-y
Elijovich F, Weinberger MH, Anderson CA, Appel LJ, Bursztyn M, Cook NR, Dart RA, Newton-Cheh CH, Sacks FM, Laffer CL, American Heart Association Professional and Public Education Committee of the Council on Hypertension; Council on Functional Genomics and Translational Biology; and Stroke Council (2016) Salt sensitivity of blood pressure: a scientific statement from the American Heart Association. Hypertension 68:e7–e46. https://doi.org/10.1161/hyp.0000000000000047
Elsakka EGE, Elsisi AM, Mansour OAA, Elsadek BEM, Abd Elaziz AI, Salama SA, Allam S (2020) Androgen/androgen receptor affects gentamicin-induced nephrotoxicity through regulation of megalin expression. Life Sci 251:117628. https://doi.org/10.1016/j.lfs.2020.117628
Entrekin SA, Clay NA, Mogilevski A, Howard-Parker B, Evans-White MA (2018) Multiple riparian-stream connections are predicted to change in response to salinization. Philos Trans R Soc Lond B Biol Sci 374:20180042. https://doi.org/10.1098/rstb.2018.0042
Grèze C, Guttmann A, Pons-Rejraji H, Vasson MP, Lornage J, Ouchchane L, Brugnon F (2019) Can the SCD test and terminal uridine nick-end labeling by flow cytometry technique (TUNEL/FCM) be used interchangeably to measure sperm DNA damage in routine laboratory practice? Basic Clin Androl 29:17. https://doi.org/10.1186/s12610-019-0098-2
Jiang B, Su Y, Chen Q, Dong L, Zhou W, Li H, Wang Y (2020) Protective effects of ozone oxidative postconditioning on long-term injury after renal ischemia/reperfusion in rat transplant. Proc 52:365–372. https://doi.org/10.1016/j.transproceed.2019.10.004
Kaushal SS, Likens GE, Pace ML, Haq S, Wood KL, Galella JG, Morel C, Doody TR, Wessel B, Kortelainen P, Räike A, Skinner V, Utz R, Jaworski N (2018a) Novel ‘chemical cocktails’ in inland waters are a consequence of the freshwater salinization syndrome. Philos Trans R Soc Lond B Biol Sci 374:20180017. https://doi.org/10.1098/rstb.2018.0017
Kaushal SS, Likens GE, Pace ML, Utz RM, Haq S, Gorman J, Grese M (2018b) Freshwater salinization syndrome on a continental scale. Proc Natl Acad Sci U S A 115:E574–e583. https://doi.org/10.1073/pnas.1711234115
Lee DL, Pollock JS, Brands MW (2005) Chronic AngII infusion causes greater hypertension and increased IL-6 in mice with knockout of peroxisome proliferator activated receptor-alpha: LB19. Hypertension 46
Mezzano SA, Ruiz-Ortega M, Egido J (2001) Angiotensin II and renal fibrosis. Hypertension 38:635–638. https://doi.org/10.1161/hy09t1.094234
Mirsalimi SM, O’Brien PJ, Julian RJ (1993) Blood volume increase in salt-induced pulmonary hypertension, heart failure and ascites in broiler and White Leghorn chickens. Can J Vet Res 57:110–113
Mueller CA, Burggren WW, Crossley DA 2nd (2013) ANG II and baroreflex control of heart rate in embryonic chickens (Gallus gallus domesticus). Am J Physiol Regul Integr Comp Physiol 305:R855–R863. https://doi.org/10.1152/ajpregu.00298.2013
Nowghani F, Chen CC, Jonusaite S, Watson-Leung T, Kelly SP, Donini A (2019) Impact of salt-contaminated freshwater on osmoregulation and tracheal gill function in nymphs of the mayfly Hexagenia rigida. Aquat Toxicol 211:92–104. https://doi.org/10.1016/j.aquatox.2019.03.019
Olkowski AA, Korver D, Rathgeber B, Classen HL (1999) Cardiac index, oxygen delivery, and tissue oxygen extraction in slow and fast growing chickens, and in chickens with heart failure and ascites: a comparative study. Avian Pathol 28:137–146. https://doi.org/10.1080/03079459994867
Pakdel A, Bijma P, Ducro BJ, Bovenhuis H (2005) Selection strategies for body weight and reduced ascites susceptibility in broilers. Poult Sci 84:528–535. https://doi.org/10.1093/ps/84.4.528
Patel S, Rauf A, Khan H, Abu-Izneid T (2017) Renin-angiotensin-aldosterone (RAAS): the ubiquitous system for homeostasis and pathologies. Biomed Pharmacother 94:317–325. https://doi.org/10.1016/j.biopha.2017.07.091
Rocha AR, Silva R, Villegas A, Sánchez-Guzmán JM, Ramos JA, Masero JA (2016) Physiological, morphological and behavioural responses of self-feeding precocial chicks copying with contrasting levels of water salinity during development. PLoS One 11:e0165364. https://doi.org/10.1371/journal.pone.0165364
Sabat P, Bozinovic F, Contreras-Ramos C, Nespolo RF, Newsome SD, Quirici V, Maldonado K, Peña-Villalobos I, Ramirez-Otarola N, Sanchez-Hernandez JC (2019) The interplay between ambient temperature and salt intake affects oxidative status and immune responses in a ubiquitous Neotropical passerine, the rufous-collared sparrow. Comp Biochem Physiol A Mol Integr Physiol 234:50–59. https://doi.org/10.1016/j.cbpa.2019.04.016
Schulz CJ, Cañedo-Argüelles M (2018) Lost in translation: the German literature on freshwater salinization. Philos Trans R Soc Lond B Biol Sci 374:20180007. https://doi.org/10.1098/rstb.2018.0007
Shan H, He Y, Hao S, Wang B, Xu M, Qi H, Liu S, du Y, Yu X (2019) Vps15 is critical to mediate autophagy in AngII treated HUVECs probably by PDK1/PKC signaling pathway. Life Sci 233:116701. https://doi.org/10.1016/j.lfs.2019.116701
Shengyou Y, Li Y (2015) The effects of siRNA-silenced TRPC6 on podocyte autophagy and apoptosis induced by AngII. J Renin Angiotensin Aldosterone Syst 16:1266–1273. https://doi.org/10.1177/1470320314543724
Siller WG (1981) Renal pathology of the fowl — a review. Avian Pathology 10:187–262
Simon-Oppermann C, Gray D, Szczepanska-Sadowska E, Simon E (1984) Arterial hypotension at elevated plasma levels of Na+, ADH and AII in ducks with high chronic salt intake. Clin Exp Hypertens A 6:2117–2121. https://doi.org/10.3109/10641968409046139
Surai PF, Kochish II, Fisinin VI, Kidd MT (2019) Antioxidant defence systems and oxidative stress in poultry biology: an update. Antioxidants (Basel) 8:235. https://doi.org/10.3390/antiox8070235
Takekawa JY, Ackerman JT, Brand LA, Graham TR, Eagles-Smith CA, Herzog MP, Topping BR, Shellenbarger GG, Kuwabara JS, Mruz E, Piotter SL, Athearn ND (2015) Unintended consequences of management actions in salt pond restoration: cascading effects in trophic interactions. PLoS One 10:e0119345. https://doi.org/10.1371/journal.pone.0119345
Wideman RF Jr, Eanes ML, Hamal KR, Anthony NB (2010) Pulmonary vascular pressure profiles in broilers selected for susceptibility to pulmonary hypertension syndrome: age and sex comparisons. Poult Sci 89:1815–1824. https://doi.org/10.3382/ps.2010-00754
Wideman RF, Rhoads DD, Erf GF, Anthony NB (2013) Pulmonary arterial hypertension (ascites syndrome) in broilers: a review. Poult Sci 92:64–83. https://doi.org/10.3382/ps.2012-02745
Yang F, Cao H, Xiao Q, Guo X, Zhuang Y, Zhang C, Wang T, Lin H, Song Y, Hu G, Liu P (2016) Transcriptome analysis and gene identification in the pulmonary artery of broilers with ascites syndrome. PLoS One 11:e0156045. https://doi.org/10.1371/journal.pone.0156045
Zhang J, Feng X, Zhao L, Wang W, Gao M, Wu B, Qiao J (2013) Expression of hypoxia-inducible factor 1α mRNA in hearts and lungs of broiler chickens with ascites syndrome induced by excess salt in drinking water. Poult Sci 92:2044–2052. https://doi.org/10.3382/ps.2013-03097
Zhu WZ, Wen YC, Lin SY, Chen TC, Chen HW (2020) Anti-Influenza protective efficacy of a H6 virus-like particle in chickens. Vaccines (Basel) 8(3):465. https://doi.org/10.3390/vaccines8030465
Funding
This research was funded by the National Natural Science Foundation of China (Grant No. 31972748) and the Fundamental Research Funds for the Central Universities (Grant No. 2662020DKPY013).
Author information
Authors and Affiliations
Contributions
YP, XY, and HL conceived and designed the experiments; XY, HL, JZ, and MZ contributed to the sample collection and preparation of reagents; YP, HL, AL, and MI wrote the manuscript; JL and DZ provided technical guidance; DZ provided the experimental funding. All the authors involved in discussing the contents of the manuscript and agreed for publication.
Corresponding author
Ethics declarations
Ethics approval and consent to participate
The experimental protocol was established, according to the Experimental Animal Center of Huazhong Agricultural University. Consent to participate is not applicable.
Consent for publication
Not applicable.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
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
Peng, Y., Yang, X., Li, H. et al. Salt-contaminated water inducing pulmonary hypertension and kidney damage by increasing Ang II concentration in broilers. Environ Sci Pollut Res 29, 1134–1143 (2022). https://doi.org/10.1007/s11356-021-13358-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-021-13358-y