Animal Reproduction (AR)
https://animal-reproduction.org/article/doi/10.1590/1984-3143-AR2023-0072
Animal Reproduction (AR)
ORIGINAL ARTICLE

Fractal analysis is a useful tool for evaluating prostate tissue remodeling caused by ethanol consumption and androgen therapy

Bruna Jardim Pereira Lima; Gabriel Rodrigues Leal de Oliveira; Thainá Cavalleri Sousa; Ariana Musa de Aquino; Karianne Delalibera Hinokuma; Maria Luiza Silva Ricardo; Wellerson Rodrigo Scarano; Anthony César de Souza Castilho; Francis Lopes Pacagnelli; Francisco Eduardo Martinez; Leonardo de Oliveira Mendes

Downloads: 1
Views: 161

Abstract

Abstract: Alcohol has been widely consumed for centuries and is linked to the aggravation of diseases. Several studies have shown that excessive consumption of ethanol results in morphophysiological changes in the male reproductive system. One of the effects of ethanol is the decrease in testosterone concentration and hormonal therapies are an alternative to minimize the changes resulting from chronic alcoholism. Qualitative studies were commonly carried out to evaluate the male histopathological alterations resulting from ethanol consumption, being necessary quantitative and non-subjective techniques. This study analyzes the importance of fractal analysis as a useful tool to identify and quantify tissue remodeling in rats submitted to ethanol consumption and hormone therapy with testosterone. Prostate of animals submitted to chronic ethanol consumption showed tissue disorganization, which was confirmed by an increasing of fractal dimension. Regarding the prostatic stroma, collagen fractal dimension and quantification revealed lower values in animals that were only submitted to androgen therapy. Thus, we can conclude that the fractal analysis was a useful tool to quantify tissue changes caused by ethanol consumption and androgen therapy.

Keywords

chronic alcoholism, fractal dimension, prostate, testosterone

References

Aquino AM, Salata GC, Pinho CF, de Freitas ATAG, Périco LL, de Lion Siervo GEM, Mendes LO, Da Cunha De Medeiros P, Justulin LA, Fernandes GSA, Perobelli JE, Scarano WR. Arsenic exposure during prepuberty alters prostate maturation in pubescent rats. Reprod Toxicol. 2019;89:136-44. http://dx.doi.org/10.1016/j.reprotox.2019.07.010. PMid:31310804.

Arruda PFF, Gatti M, Facio FN Jr, Arruda JGF, Moreira RD, Murta LO Jr, Arruda LF, Godoy MF. Quantification of fractal dimension and Shannon’s entropy in histological diagnosis of prostate cancer. BMC Clin Pathol. 2013;13(1):6. http://dx.doi.org/10.1186/1472-6890-13-6. PMid:23414368.

Bannach SV, Teixeira FB, Fernandes LM, Ferreira RO, Santana LN, Fontes EA Jr,, Oliveira GB, Prediger RD. Alveolar bone loss induced by chronic ethanol consumption from adolescence to adulthood in Wistar rats. Indian J Exp Biol. 2015;53(2):93-7. PMid:25757239.

Cândido EM, Carvalho CAF, Martinez FE, Cagnon VHA. Experimental alcoholism and pathogenesis of prostatic diseases in UChB rats. Cell Biol Int. 2007;31(5):459-72. http://dx.doi.org/10.1016/j.cellbi.2006.11.009. PMid:17188526.

Cicero TJ, Badger TM. Effects of alcohol on the hypothalamic-pituitary-gonadal axis in the male rat. J Pharmacol Exp Ther. 1977;201(2):427-33. PMid:870681.

Cury SS, Freire PP, Martinucci B, Santos VC, Oliveira G, Ferretti R, Dal-Pai-Silva M, Pacagnelli FL, Delella FK, Carvalho RF. Fractal dimension analysis reveals skeletal muscle disorganization in mdx mice. Biochem Biophys Res Commun. 2018;503(1):109-15. http://dx.doi.org/10.1016/j.bbrc.2018.05.189. PMid:29852164.

Dantas AM, Mohn CE, Burdet B, Zubilete MZ, Mandalunis PM, Elverdin JC, Fernández-Solari J. Ethanol consumption enhances periodontal inflammatory markers in rats. Arch Oral Biol. 2012;57(9):1211-7. http://dx.doi.org/10.1016/j.archoralbio.2012.02.008. PMid:22424886.

Deckardt K, Weber I, Kaspers U, Hellwig J, Tennekes H, van Ravenzwaay B. The effects of inhalation anaesthetics on common clinical pathology parameters in laboratory rats. Food Chem Toxicol. 2007;45(9):1709-18. http://dx.doi.org/10.1016/j.fct.2007.03.005. PMid:17459552.

Fávaro WJ, Cagnon VHA. Morphometric and morphological features of the ventral prostate in rats submitted to chronic nicotine and alcohol treatment. Tissue Cell. 2006;38(5):311-23. http://dx.doi.org/10.1016/j.tice.2006.08.002. PMid:17014878.

Fávero PF, Vieira de Lima VA, Helena Dos Santos P, Marques Andrade AP, Mendes LO, Pacagnelli FL, César de Souza Castilho A. Differential fractal dimension is associated with extracellular matrix remodeling in developing bovine corpus luteum. Biochem Biophys Res Commun. 2019;516(3):888-93. http://dx.doi.org/10.1016/j.bbrc.2019.06.002. PMid:31270026.

Felix-Patrício B, Miranda AF, Medeiros JL Jr, Gallo CBM, Gregório BM, Souza DB, Costa WS, Sampaio FJB. The prostate after castration and hormone replacement in a rat model: structural and ultrastructural analysis. International Brazilian Journal of Urology: Official Journal of the Brazilian Society of Urology. 2017;43(5):957-65. http://dx.doi.org/10.1590/s1677-5538.ibju.2016.0484. PMid:28379662.

Fernandes LMP, Teixeira FB, Alves-Junior SM, Pinheiro JJV, Maia CSF, Lima RR. Immunohistochemical changes and atrophy after chronic ethanol intoxication in rat salivary glands. Histol Histopathol. 2015;30(9):1069-78. PMid:25761695.

Fink J, Matsumoto M, Tamura Y. Potential application of testosterone replacement therapy as treatment for obesity and type 2 diabetes in men. Steroids. 2018;138:161-6. http://dx.doi.org/10.1016/j.steroids.2018.08.002. PMid:30118780.

Frisch KE, Duenwald-Kuehl SE, Kobayashi H, Chamberlain CS, Lakes RS, Vanderby R Jr. Quantification of collagen organization using fractal dimensions and Fourier transforms. Acta Histochem. 2012;114(2):140-4. http://dx.doi.org/10.1016/j.acthis.2011.03.010. PMid:21529898.

Galvão-Teles A, Monteiro E, Gavaler JS, Van Thiel DH. Gonadal consequences of alcohol abuse: lessons from the liver. Hepatology. 1986;6(1):135-40. http://dx.doi.org/10.1002/hep.1840060126. PMid:3510948.

Głowińska-Olszewska B, Urban M, Florys B. Ocena stezenia wybranych metaloproteinaz macierzy zewnatrzkomórkowej (MMP-2, MMP-9) u dzieci i młodziezy z otyłościa prosta [Selected matrix metalloproteinases (MMP-2, MMP-9) in obese children and adolescents. Endokrynol Diabetol Chor Przemiany Materii Wieku Rozw. 2006;12(3):179-83. PMid:17020652.

Gomes IC, Cagnon VHA, Carvalho CAF, De Luca IMS. Stereology and ultrastructure of the seminal vesicle of C57/BL/6J mice following chronic alcohol ingestion. Tissue Cell. 2002;34(3):177-86. http://dx.doi.org/10.1016/S0040-8166(02)00029-0. PMid:12182811.

Gordon GG, Altman K, Southren AL, Rubin E, Lieber CS. Effect of alcohol (ethanol) administration on sex-hormone metabolism in normal men. N Engl J Med. 1976;295(15):793-7. http://dx.doi.org/10.1056/NEJM197610072951501. PMid:958274.

Haidar A, Yassin A, Saad F, Shabsigh R. Effects of androgen deprivation on glycaemic control and on cardiovascular biochemical risk factors in men with advanced prostate cancer with diabetes. Aging Male. 2007;10(4):189-96. http://dx.doi.org/10.1080/13685530701653538. PMid:18033628.

Mardones J, Segovia-Riquelme N. Thirty-two years of selection of rats by ethanol preference: UChA and UChB strains. Neurobehav Toxicol Teratol. 1983;5(2):171-8. PMid:6683362.

Martinez FE, Martinez M, Padovani CR, Bustos-Obregón E. Morphology of testis and epididymis in an ethanol-drinking rat strain (UChA and UChB). J Submicrosc Cytol Pathol. 2000;32(2):175-84. PMid:11085206.

Mendes LO, Castilho ACS, Pinho CF, Gonçalvez BF, Razza EM, Chuffa LGA, Anselmo-Franci JA, Scarano WR, Martinez FE. Modulation of inflammatory and hormonal parameters in response to testosterone therapy: effects on the ventral prostate of adult rats. Cell Biol Int. 2018;42(9):1200-11. http://dx.doi.org/10.1002/cbin.10990. PMid:29771451.

Mendes LO, Scarano WR, Rochel-Maia SS, Fioruci-Fontaneli BA, Chuffa LG, Anselmo-Franci JA, Martinez FE. Androgen therapy reverses injuries caused by ethanol consumption in the prostate: testosterone as a possible target to ethanol-related disorders. Life Sci. 2015;120:22-30. http://dx.doi.org/10.1016/j.lfs.2014.11.003. PMid:25447451.

Mendes LO, Scarano WR, Rochel-Maia SS, Fioruci-Fontaneli BA, Chuffa LGA, Martinez FE. Testosterone therapy differently regulates the anti- and pro-inflammatory cytokines in the plasma and prostate of rats submitted to chronic ethanol consumption (UChB). Am J Reprod Immunol. 2014;72(3):317-25. http://dx.doi.org/10.1111/aji.12268. PMid:24828842.

Nazian SJ. Serum concentrations of reproductive hormones after administration of various anesthetics to immature and young adult male rats. Proc Soc Exp Biol Med. 1988;187(4):482-7. http://dx.doi.org/10.3181/00379727-187-42692. PMid:3127834.

PAHO-WHO. Alcohol fact sheet [Internet]. Washington, DC: Pan American Health Organization; 2020 [cited 2021 Jan 17]. Available from: https://www.paho.org/en/node/4825.

Pajevic M, Aleksic M, Golic I, Markelic M, Otasevic V, Jankovic A, Stancic A, Korac B, Korac A. Fractal and stereological analyses of insulin-induced rat exocrine pancreas remodelling. Folia Morphol (Warsz). 2018;77(3):478-84. http://dx.doi.org/10.5603/FM.a2017.0106. PMid:29131278.

Pu Y, Wang W, Al-Rubaiee M, Gayen SK, Xu M. Determination of optical coefficients and fractal dimensional parameters of cancerous and normal prostate tissues. Appl Spectrosc. 2012;66(7):828-34. http://dx.doi.org/10.1366/11-06471. PMid:22710079.

Reyes-Vallejo L, Lazarou S, Morgentaler A. Subjective sexual response to testosterone replacement therapy based on initial serum levels of total testosterone. J Sex Med. 2007;4(6):1757-62. http://dx.doi.org/10.1111/j.1743-6109.2006.00381.x PMid:17087806.

Riley EP, Thomas JD, Goodlett CR, Klintsova AY, Greenough WT, Hungund BL, Zhou F, Sari Y, Powrozek T, Li T. Fetal alcohol effects: mechanisms and treatment. Alcohol Clin Exp Res. 2001;25(5, Suppl):110S-6S. http://dx.doi.org/10.1111/j.1530-0277.2001.tb02384.x PMid:11391059.

Salonen I, Huhtaniemi I. Effects of chronic ethanol diet on pituitary-testicular function of the rat. Biol Reprod. 1990;42(1):55-62. http://dx.doi.org/10.1095/biolreprod42.1.55. PMid:2155675.

Sáttolo S, Carvalho CAF, Cagnon VHA. Influence of hormonal replacement on the ventral lobe of the prostate of rats (Rattus norvegicus albinus) submitted to chronic ethanol treatment. Tissue Cell. 2004;36(6):417-30. http://dx.doi.org/10.1016/j.tice.2004.07.004. PMid:15533457.

Saxena S, Meehan D, Coney P, Wimalasena J. Ethanol has direct inhibitory effects on steroidogenesis in human granulosa cells: specific inhibition of LH action. Alcohol Clin Exp Res. 1990;14(4):522-7. http://dx.doi.org/10.1111/j.1530-0277.1990.tb01192.x PMid:2121059.

Scarano WR, Vilamaior PSL, Taboga SR. Tissue evidence of the testosterone role on the abnormal growth and aging effects reversion in the gerbil (Meriones unguiculatus) prostate. Anat Rec (Hoboken). 2006;288(11):1190-200. http://dx.doi.org/10.1002/ar.a.20391. PMid:17031809.

Shoulders MD, Raines RT. Collagen structure and stability. Annu Rev Biochem. 2009;78(1):929-58. http://dx.doi.org/10.1146/annurev.biochem.77.032207.120833. PMid:19344236.

Silva SA, Gobbo MG, Pinto-Fochi ME, Rafacho A, Taboga SR, Almeida EA, Góes RM, Ribeiro DL. Prostate hyperplasia caused by long-term obesity is characterized by high deposition of extracellular matrix and increased content of MMP-9 and VEGF. Int J Exp Pathol. 2015;96(1):21-30. http://dx.doi.org/10.1111/iep.12107. PMid:25529509.

Tadic SD, Elm MS, Subbotin VM, Eagon PK. Hypogonadism precedes liver feminization in chronic alcohol-fed male rats. Hepatology. 2000;31(5):1135-40. http://dx.doi.org/10.1053/he.2000.6960. PMid:10796890.

Tamarindo GH, Gobbo MG, Taboga SR, Almeida EA, Góes RM. Melatonin ameliorates degenerative alterations caused by age in the rat prostate and mitigates high-fat diet damages. Cell Biol Int. 2021;45(1):92-106. http://dx.doi.org/10.1002/cbin.11472. PMid:32991000.

Tambasco M, Costello BM, Kouznetsov A, Yau A, Magliocco AM. Quantifying the architectural complexity of microscopic images of histology specimens. Micron. 2009;40(4):486-94. http://dx.doi.org/10.1016/j.micron.2008.12.004. PMid:19171487.

Van Thiel DH, Lester R, Sherins RJ. Hypogonadism in alcoholic liver disease: evidence for a double defect. Gastroenterology. 1974;67(6):1188-99. http://dx.doi.org/10.1016/S0016-5085(19)32705-2. PMid:4430432.

Van Thiel DH, Lester R. The effect of chronic alcohol abuse on sexual function. Clin Endocrinol Metab. 1979;8(3):499-510. http://dx.doi.org/10.1016/S0300-595X(79)80028-6 PMid:389488.

Waliszewski P, Wagenlehner F, Gattenlöhner S, Weidner W. On the relationship between tumor structure and complexity of the spatial distribution of cancer cell nuclei: a fractal geometrical model of prostate carcinoma. Prostate. 2015;75(4):399-414. http://dx.doi.org/10.1002/pros.22926. PMid:25545623.

Waliszewski P. The quantitative criteria based on the fractal dimensions, entropy, and lacunarity for the spatial distribution of cancer cell nuclei enable identification of low or high aggressive prostate carcinomas. Front Physiol. 2016;7:34. http://dx.doi.org/10.3389/fphys.2016.00034. PMid:26903883.

Yatkin E, Bernoulli J, Talvitie E, Santti R. Inflammation and epithelial alterations in rat prostate: impact of the androgen to oestrogen ratio. Int J Androl. 2009;32(4):399-410. http://dx.doi.org/10.1111/j.1365-2605.2008.00930.x. PMid:19515173.
 


Submitted date:
05/19/2023

Accepted date:
07/03/2023

650445d3a953957d3d28d014 animreprod Articles
Links & Downloads

Anim Reprod

Share this page
Page Sections