Structural Changes in the Skeletal Muscle of Pigs after Long-Term Administration of Testosterone, Nandrolone and a Combination of the Two
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články
Grantová podpora
QK1910311
NAZV
AF-IGA2022-IP-020
the Mendel University in Brno Internal grant agency
PubMed
37443939
PubMed Central
PMC10339938
DOI
10.3390/ani13132141
PII: ani13132141
Knihovny.cz E-zdroje
- Klíčová slova
- anabolic steroids, histology, muscle fibers, pigs, satellite cells,
- Publikační typ
- časopisecké články MeSH
Anabolic steroid hormones (AASs) are used in most countries of the world to accelerate the growth of animals, increase the volume of their muscles and thereby increase meat production. However, there is a strict ban on the use of AASs in the fattening of all animals in all countries of the European Union, and there must therefore be effective methods of detection and control of these substances. Methods based on chromatography and mass spectrometry may no longer be completely effective when faced with new synthetic steroids of unknown chemical structures and low concentrations. Therefore, there is an effort to develop new methods of AAS detection, based primarily on the monitoring of biological changes at the level of gene expression or changes in metabolism or structure at the cellular level. More detailed knowledge of the mechanisms of action of AASs on tissues is essential for these methods, and histological changes are one of them. In this study, we report histological changes in muscle structure after AAS application, specifically in the size of muscle fibers, the amount of endomysium and the number of nuclei and satellite cells in muscle fibers. A pig model was also intentionally used for the study, as no such study has been carried out on this species, and at the same time, pork is one of the most consumed meats across Europe. The results of histology and fluorescent antibody labeling showed that AASs increased the diameter and surface area of muscle fibers and also significantly increased the number of satellite cells on the fiber surface. The evident correlations between the number of satellite cells, all nuclei and the diameters of muscle fibers between some experimental groups provide evidence that the selected histological parameters could be additional detection mechanisms for screening a large number of samples and indicate the possibility of the presence of AASs in pork meat in the future.
Zobrazit více v PubMed
Cole T.J., Short K.L., Hooper S.B. The science of steroids. Semin. Fetal Neonatal Med. 2019;24:170–175. doi: 10.1016/j.siny.2019.05.005. PubMed DOI
Kuhn C.M. Anabolic Steroids. Recent. Prog. Horm. Res. 2002;57:411–434. doi: 10.1210/rp.57.1.411. PubMed DOI
Kreutzer K.V., Turk J.R., Casteel S.W. Clinical Biochemistry in Toxicology. In: Kaneko J.J., Harvey J.W., Bruss M.L., editors. Clinical Biochemistry of Domestic Animals. 6th ed. Academic Press; Cambridge, MA, USA: 2008. pp. 821–838.
Reyes-Vallejo L. Current use and abuse of anabolic steroids. Actas Urológicas Españolas (Engl. Ed.) 2020;44:309–313. doi: 10.1016/j.acuroe.2019.10.007. PubMed DOI
Fojtíková L., Göselová S., Holubová B. Anabolické androgenní steroidy—nebezpečí v doplňcích stravy. Chem. Listy. 2015;109:913–917.
Food and Drug Administration: Steroid Hormone Implants Used for Growth in Food-Producing Animals [Online] [(accessed on 13 March 2022)]; Available online: https://www.fda.gov/animal-veterinary/product-safety-information/steroid-hormone-implants-used-growthfood-producing-animals.
Official Journal of the European Union, L12523/05/1996 . Council Directive 96/22/EC of 29 April 1996 Concerning the Prohibition on the Use in Stockfarming of Certain Substances Having a Hormonal or Thyrostatic Action and of Beta-Agonists, and Repealing Directives 81/602/EEC, 88/146/EEC and 88/299/EEC. European Commission; Brussels, Belgium: 1996.
Abrahim O., de Sousa E.C., Santos A. Prevalence of the Use of Anabolic-Androgenic Steroids in Brazil: A Systematic Review. Subst. Use Misuse. 2014;49:1156–1162. doi: 10.3109/10826084.2014.903750. PubMed DOI
Passantino A. Steroid Hormones in Food Producing Animals. In: Perez-Marin C.C., editor. A Bird’s-Eye View of Veterinary Medicine. InTech; Córdoba, Spain: 2012.
Scarth J., Akre C., van Ginkel L., Le Bizec B., De Barbander H., Korth W., Points J., Teale P., Kay J. Presence and metabolism of endogenous androgenic–anabolic steroid hormones in meat-producing animals: A review. Food Addit. Contam. Part A. 2009;26:640–671. doi: 10.1080/02652030802627160. PubMed DOI
Official Medicines Control Laboratories (OMCLs) Market Surveillance of Suspected Illegal Products (MSSIP). MSSIP003: Illegal Anabolic Steroids. Council of Europe; Strasbourg, France: 2022.
Šťastný K., Putecová K., Levá L., Fránek M., Dvořák P., Faldyna M. Profiling of Metabolomic Changes in Plasma and Urine of Pigs Caused by Illegal Administration of Testosterone Esters. Metabolites. 2020;10:307. doi: 10.3390/metabo10080307. PubMed DOI PMC
Official Journal of the European Union, L 248/3 . REGULATIONS COMMISSION DELEGATED REGULATION (EU) 2022/1644 of 7 July 2022 Supplementing Regulation (EU) 2017/625 of the European Parliament and of the Council with Specific Requirements for the Performance of Official Controls on the Use of Pharmacologically Active Substances Authorised as Veterinary Medicinal Products or as Feed Additives and of Prohibited or Unauthorised Pharmacologically Active Substances and Residues Thereof. European Commission; Brussels, Belgium: 2022.
Yin H., Price F., Rudnicki M.A. Satellite Cells and the Muscle Stem Cell Niche. Physiol. Rev. 2013;93:23–67. doi: 10.1152/physrev.00043.2011. PubMed DOI PMC
Wang Y.X., Rudnicki M.A. Satellite cells, the engines of muscle repair. Nat. Rev. Mol. Cell Biol. 2012;13:127–133. doi: 10.1038/nrm3265. PubMed DOI
Relaix F., Zammit P.S. Satellite cells are essential for skeletal muscle regeneration: The cell on the edge returns centre stage. Development. 2012;139:2845–2856. doi: 10.1242/dev.069088. PubMed DOI
Almeida C.F., Fernandes S.A., Ribeiro Junior A.F., Okamoto O.K., Vainzof M. Muscle Satellite Cells: Exploring the Basic Biology to Rule Them. Stem Cells Int. 2016;2016:1078686. doi: 10.1155/2016/1078686. PubMed DOI PMC
Forcina L., Miano C., Pelosi L., Musarò A. An Overview About the Biology of Skeletal Muscle Satellite Cells. Curr. Genom. 2019;20:24–37. doi: 10.2174/1389202920666190116094736. PubMed DOI PMC
Brack A.S., Rando T.A. Tissue-Specific Stem Cells: Lessons from the Skeletal Muscle Satellite Cell. Cell Stem Cell. 2012;10:504–514. doi: 10.1016/j.stem.2012.04.001. PubMed DOI PMC
Wozniak A.C., Kong J., Bock E., Pilipowicz O., Anderson J.E. Signaling satellite-cell activation in skeletal muscle: Markers, models, stretch, and potential alternate pathways. Muscle Nerve Off. J. Am. Assoc. Electrodiagn. Med. 2005;31:283–300. doi: 10.1002/mus.20263. PubMed DOI
Chen W., Datzkiw D., Rudnicki M.A. Satellite cells in ageing: Use it or lose it. Open Biol. 2020;10:200048. doi: 10.1098/rsob.200048. PubMed DOI PMC
Motohashi N., Asakura A. Muscle satellite cell heterogeneity and self-renewal. Front. Cell Dev. Biol. 2014;2:1. doi: 10.3389/fcell.2014.00001. PubMed DOI PMC
Fontana K., Campos G.E.R., Staron R.S., Cruz-Höfling M.A. Effects of Anabolic Steroids and High-Intensity Aerobic Exercise on Skeletal Muscle of Transgenic Mice. PLoS ONE. 2013;8:e80909. doi: 10.1371/journal.pone.0080909. PubMed DOI PMC
Carson J.A., Manolagas S.C. Effects of sex steroids on bones and muscles: Similarities, parallels, and putative interactions in health and disease. Bone. 2015;80:67–78. doi: 10.1016/j.bone.2015.04.015. PubMed DOI PMC
Elgendy H., Alhawary A., El-Shahat M., Ali A. Effect of Anabolic Steroids on the Cardiac and Skeletal Muscles of Adult Male Rats. Int. J. Clin. Dev. Anat. 2018;4:1–14. doi: 10.11648/j.ijcda.20180401.11. DOI
Sretenovic J., Ajdzanovic V., Zivkovic V., Srejovic I., Corbic M., Milosevic V., Jakovljevic V., Milosavljevic Z. Nandrolone decanoate and physical activity affect quadriceps in peripubertal rats. Acta Histochem. 2018;120:429–437. doi: 10.1016/j.acthis.2018.04.004. PubMed DOI
Welder A.A., Robertson J.W., Fugate R.D., Melchert R.B. Anabolic-androgenic steroid-induced toxicity in primary neonatal rat myocardial cell cultures. Toxicol. Appl. Pharmacol. 1995;133:328–342. doi: 10.1006/taap.1995.1158. PubMed DOI
Hassan D.A.E., Ghaleb S.S., Zaki A., Abdelmenem A., Nabil S., Alim M.A.A. The toxic effects of anabolic steroids “nandrolone decanoate” on cardiac and skeletal muscles with the potential ameliorative effects of silymarin and fenugreek seeds extract in adult male albino rats. BMC Pharm. Toxicol. 2023;24:17. doi: 10.1186/s40360-023-00658-x. PubMed DOI PMC
Elmajdoub A., Garbaj A., Abolghait S., El-Mahmoudy A. Evaluation of boldenone as a growth promoter in broilers: Safety and meat quality aspects. J. Food Drug. Anal. 2016;24:284–292. doi: 10.1016/j.jfda.2015.12.001. PubMed DOI PMC
Tousson E. Histopathological alterations after a growth promoter boldenone injection in rabbits. Toxicol. Ind. Health. 2013;32:299–305. doi: 10.1177/0748233713500821. PubMed DOI
Hyyppä S. Effects of Nandrolone Treatment on Recovery in Horses After Strenuous Physical Exercise. J. Vet. Med. Ser. A. 2001;48:343–352. doi: 10.1046/j.1439-0442.2001.00368.x. PubMed DOI
Nimmo M.A., Snow D.H., Munro C.D. Effects of nandrolone phenylpropionate in the horse: (3) Skeletal muscle composition in the exercising animal. Equine Vet. J. 1982;14:229–233. doi: 10.1111/j.2042-3306.1982.tb02402.x. PubMed DOI
Conceição M.S., Vechin F.C., Lixandrão M., Damas F., Libardi C.A., Tricoli V., Roschel H., Camera D., Ugrinowitsch C. Muscle Fiber Hypertrophy and Myonuclei Addition: A Systematic Review and Meta-analysis. Med. Sci. Sport. Exerc. 2018;50:1385–1393. doi: 10.1249/MSS.0000000000001593. PubMed DOI
Eriksson A., Kadi F., Malm C., Thornell L.E. Skeletal muscle morphology in power-lifters with and without anabolic steroids. Histochem. Cell Biol. 2005;124:167–175. doi: 10.1007/s00418-005-0029-5. PubMed DOI
Hartgens F., Van Marken Lichtenbelt W., Ebbing S. Body composition and anthropometry in bodybuilders: Regional changes due to nandrolone decanoate administration. Int. J. Sport. Med. 2001;22:235–241. doi: 10.1055/s-2001-18679-1. PubMed DOI
Hartgens F., Van Marken Lichtenbelt W., Ebbing S., Vollaard N., Rietjens G., Kuipers H. Androgenic-anabolic steroids induced body changes in strength athletes. Phys. Sportsmed. 2001;29:49–66. doi: 10.3810/psm.2001.01.316. PubMed DOI
Johnson B.J., White M.E., Hathaway M.R., Christians C.J., Dayton W.R. Effect of a combined trenbolone acetate and estradiol implant on steady-state IGF-I mRNA con-centrations in the liver of wethers and the longissimus muscle of steers. J. Anim. Sci. 1998;76:491–497. doi: 10.2527/1998.762491x. PubMed DOI
Clancy M.J., Lester J.M., Roche J.F. The Effects of Anabolic Agents and Breed on the Fibers of the Longissimus Muscle of Male Cattle. J. Anim. Sci. 1986;63:83–91. doi: 10.2527/jas1986.63183x. PubMed DOI
Kellermeier J.D., Tittor A.W., Brooks J.C., Galyean M.L., Yates D.A., Hutcheson J.P., Nichols W.T., Streeter M.N., Johnson B.J., Miller M.F. Effects of zilpaterol hydrochloride with or without an estrogen-trenbolone acetate terminal implant on carcass traits, retail cutout, tenderness, and muscle fiber diameter in finishing steers. J. Anim. Sci. 2009;87:3702–3711. doi: 10.2527/jas.2009-1823. PubMed DOI
Gerber C., Meyer D.C., Von Rechenberg B., Hoppeler H., Frigg R., Farshad M., Rotator C. Muscles Lose Responsiveness to Anabolic Steroids After Tendon Tear and Musculotendinous Retraction: An Experimental Study in Sheep. Am. J. Sport. Med. 2012;40:2454–2461. doi: 10.1177/0363546512460646. PubMed DOI
Hala Z.E.M., Heba K.M. Histological and Immunohistochemical Studies of the Effects of Administration of Anabolic Androgenic Steroids Alone and in Concomitant with Training Exercise on the Adult Male Rats Skeletal Muscles. Egypt. J. Histol. 2022;45:36–49.
Yu J.G., Bonnerud P., Eriksson A., Stål P.S., Tegner Y., Malm C. Effects of Long Term Supplementation of Anabolic Androgen Steroids on Human Skeletal Muscle. PLoS ONE. 2014;9:e105330. doi: 10.1371/journal.pone.0105330. PubMed DOI PMC
Asfour H.A., Shaqoura E.I., Said R.S., Mustafa A.G., Emerald B.S., Allouh M.Z. Differential response of oxidative and glycolytic skeletal muscle fibers to mesterolone. Sci. Rep. 2021;11:12301. doi: 10.1038/s41598-021-91854-4. PubMed DOI PMC
Horwath O., Apró W., Moberg M., Godhe M., Helge T., Ekblom M., Hirschberg A.L., Ekblom B. Fiber type-specific hypertrophy and increased capillarization in skeletal muscle following testosterone administration in young women. J. Appl. Physiol. 2020;128:1240–1250. doi: 10.1152/japplphysiol.00893.2019. PubMed DOI
Machek S.B., Lorenz K.A., Kern M., Galpin A.J., Bagley J.R. Skeletal Muscle Fiber Type and Morphology in a Middle-Aged Elite Male Powerlifter Using Anabolic Steroids. J. Sci. Sport. Exerc. 2021;3:404–411. doi: 10.1007/s42978-019-00039-z. DOI