Skip to main content

Advertisement

SpringerLink
Log in

The crucial role of oxidative stress in non-alcoholic fatty liver disease-induced male reproductive toxicity: the ameliorative effects of Iranian indigenous probiotics

  • Original Article
  • Published:
Naunyn-Schmiedeberg's Archives of Pharmacology Aims and scope Submit manuscript

Abstract

Several studies have focused on the high potential effects of probiotics on the reproductive system. However, there is a paucity of information regarding the ameliorative intracellular roles of indigenous Iranian yogurt-extracted/cultured probiotics on animals’ reproductive health suffering from obesity and/or fatty liver disease, such as non-alcoholic fatty liver disease (NAFLD). For this purpose, simultaneously with the consumption of D-fructose (200 g/1000 mL water, induction of NAFLD model), all pubertal animals were also gavaged every day for 63 consecutive days with extracted probiotics, including 1 × 109 CFU/mL of Lactobacillus acidophilus (LA), Bifidobacterium spp. (BIF), Bacillus coagulans (BC), Lactobacillus rhamnosus (LR), and a mixture form (LA + BIF + BC + LR). At the end of the ninth week, the indices of epididymal sperm, and oxidative stress, as well as histopathological changes, were assessed. The results show that NAFLD could induce robust oxidative stress, highlighted as considerable increments in ROS level, TBARS content, total oxidized protein levels, along with severe decrements in reduced glutathione reservoirs, total antioxidant capacity in the hepatic and testicular tissues, as well as testicular and hepatic histopathological alterations. Moreover, a significant decrease in the percentage of sperm progressive motility, sperm count, and membrane integrity along with an increment in the percentage of sperm abnormality was detected in NAFLD animals. The observed adverse effects were significantly reversed upon probiotics treatment, especially in the group challenged with a mixture of all probiotics. Taken together, these findings indicate that the indigenous yogurt-isolated/cultured probiotics had a high potential antioxidant activity and the ameliorative effect against reprotoxicity and blood biochemical alterations induced by the NAFLD model. Highlights: 1. Reproductive indices could be reversely affected by xenobiotics and diseases. 2. NAFLD and cholestasis considerably affect the reproductive system in both genders. 3. NAFLD induced hepatic and testicular oxidative stress (OS). 4. NAFLD induced histopathological alterations and spermatotoxicity through OS. 5. The adverse effects were significantly reversed upon exposure to probiotics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Ackerman Z, Oron-Herman M, Grozovski M, Rosenthal T, Pappo O, Link G, Sela B-A (2005) Fructose-induced fatty liver disease: hepatic effects of blood pressure and plasma triglyceride reduction. Hypertension 45:1012–1018

    Article  CAS  PubMed  Google Scholar 

  • Aggerholm AS, Thulstrup AM, Toft G, Ramlau-Hansen CH, Bonde JP (2008) Is overweight a risk factor for reduced semen quality and altered serum sex hormone profile? Fertil Steril 90:619–626

    Article  CAS  PubMed  Google Scholar 

  • Ahmed E, Nagaoka K, Fayez M, Abdel-Daim MM, Samir H, Watanabe G (2015) Suppressive effects of long-term exposure to P-nitrophenol on gonadal development, hormonal profile with disruption of tissue integrity, and activation of caspase-3 in male Japanese quail (Coturnix japonica). Environ Sci Pollut Res 22:10930–10942

    Article  CAS  Google Scholar 

  • Angelakis E, Merhej V, Raoult D (2013) Related actions of probiotics and antibiotics on gut microbiota and weight modification. Lancet Infect Dis 13:889–899

    Article  CAS  PubMed  Google Scholar 

  • Arora T, Singh S, Sharma RK (2013) Probiotics: interaction with gut microbiome and antiobesity potential. Nutrition 29:591–596

    Article  CAS  PubMed  Google Scholar 

  • Avery SV (2011) Molecular targets of oxidative stress. Biochem J 434:201–210

    Article  CAS  PubMed  Google Scholar 

  • Azarang A, Farshad O, Ommati MM, Jamshidzadeh A, Heidari R, Abootalebi SN, Gholami A (2020) Protective role of probiotic supplements in hepatic steatosis: a rat model study. BioMed Res Int 5487659. https://doi.org/10.1155/2020/5487659

  • Baptissart M, Vega A, Martinot E, Pommier AJ, Houten SM, Marceau G, Haze AD, Baron S, Schoonjans K, Lobaccaro JMA (2014) Bile acids alter male fertility through G-protein-coupled bile acid receptor 1 signaling pathways in mice. Hepatology 60:1054–1065

    Article  CAS  PubMed  Google Scholar 

  • Bashandy AS (2007) Effect of fixed oil of Nigella sativa on male fertility in normal and hyperlipidemic rats. Int J Pharmacol 3:27–33

    Article  CAS  Google Scholar 

  • Bieniek JM, Kashanian JA, Deibert CM, Grober ED, Lo KC, Brannigan RE, Sandlow JI, Jarvi KA (2016) Influence of increasing body mass index on semen and reproductive hormonal parameters in a multi-institutional cohort of subfertile men. Fertil Steril 106:1070–1075

    Article  CAS  PubMed  Google Scholar 

  • Bisanz JE, Enos MK, Mwanga JR, Changalucha J, Burton JP, Gloor GB, Reid G (2014) Randomized open-label pilot study of the influence of probiotics and the gut microbiome on toxic metal levels in Tanzanian pregnant women and school children. MBio 5:e01580-e1614

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analyt Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brooks D (1983) Epididymal functions and their hormonal regulation. Aust J Biol Sci 36:205–222

    Article  CAS  PubMed  Google Scholar 

  • Cai SS, Zhou Y, Ye BC (2021) Reducing the reproductive toxicity activity of Lactiplantibacillus plantarum: a review of mechanisms and prospects. Environ Sci Pollut Res Int 28:36927–36941

    Article  CAS  PubMed  Google Scholar 

  • Caro AA, Adlong LW, Crocker SJ, Gardner MW, Luikart EF, Gron LU (2012) Effect of garlic-derived organosulfur compounds on mitochondrial function and integrity in isolated mouse liver mitochondria. Toxicol Lett 214:166–174

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen X, Gong L, Xu J (2013) Antioxidative activity and protective effect of probiotics against high-fat diet-induced sperm damage in rats. Animal 7:287–292

    Article  CAS  PubMed  Google Scholar 

  • Chitra G, Krishnaveni N (2013) Effect of probiotics on reproductive performance in female livebearing ornamental fish Poecilia sphenops. J Pure Appl Zool 1:249–254

    Google Scholar 

  • Corbett GA, Crosby DA, McAuliffe FM (2020) Probiotic therapy in couples with infertility: a systematic review. Eur J Obstet Gynecol Reprod Biol 256:95–100

    Article  PubMed  Google Scholar 

  • Dale HF, Rasmussen SH, Asiller ÖÖ, Lied GA (2019) Probiotics in irritable bowel syndrome: an up-to-date systematic review. Nutrients 11:2048

    Article  CAS  PubMed Central  Google Scholar 

  • Dallak M (2018) Crataegus aronia enhances sperm parameters and preserves testicular architecture in both control and non-alcoholic fatty liver disease-induced rats. Pharm Biol 56:535–547

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dardmeh F, Alipour H, Gazerani P, van der Horst G, Brandsborg E, Nielsen HI (2017) Lactobacillus rhamnosus PB01 (DSM 14870) supplementation affects markers of sperm kinematic parameters in a diet-induced obesity mice model. PLoS One 12:e0185964

    Article  PubMed  PubMed Central  Google Scholar 

  • Eftekhari A, Dizaj SM, Chodari L, Sunar S, Hasanzadeh A, Ahmadian E, Hasanzadeh M (2018) The promising future of nano-antioxidant therapy against environmental pollutants induced-toxicities. Biomed Pharmacother 103:1018–1027

    Article  CAS  PubMed  Google Scholar 

  • El-Bordeny N, Abdou A, Abo-Eid H, Abdo M, Abdel-Gawad R (2019) Effect of yeast-based probiotics supplementation on the productive and reproductive performance of lactating buffaloes. Egypt J Nutr Feeds 22:33–44

    Article  Google Scholar 

  • Eslamparast T, Eghtesad S, Hekmatdoost A, Poustchi H (2013) Probiotics and nonalcoholic fatty liver disease. Middle East J Dig Dis 5:129–136

    PubMed  PubMed Central  Google Scholar 

  • Ewuola E (2013) Daily sperm production, gonadal and extra-gonadal sperm reserves of rabbits fed prebiotic and probiotic supplemented diets. Int J Appl Agric Apiculture Res 9:48–53

    Google Scholar 

  • Fejes I, Koloszár S, Szöllosi J, Závaczki Z, Pál A (2005) Is semen quality affected by male body fat distribution? Andrologia 37:155–159

    Article  CAS  PubMed  Google Scholar 

  • Fejes I, Koloszár S, Závaczki Z, Daru J, Szöllösi J, Pál A (2006) Effect of body weight on testosterone/estradiol ratio in oligozoospermic patients. Arch Androl 52:97–102

    Article  CAS  PubMed  Google Scholar 

  • Fernández-Sánchez A, Madrigal-Santillán E, Bautista M, Esquivel-Soto J, Morales-González Á, Esquivel-Chirino C, Durante-Montiel I, Sánchez-Rivera G, Valadez-Vega C, Morales-González JA (2011) Inflammation, oxidative stress, and obesity. Int J Mol Sci 12:3117–3132

    Article  PubMed  PubMed Central  Google Scholar 

  • Fernandez CD, Bellentani FF, Fernandes GS, Perobelli JE, Favareto APA, Nascimento AF, Cicogna AC, Kempinas WD (2011) Diet-induced obesity in rats leads to a decrease in sperm motility. Reprod Biol Endocrinol 9:32

    Article  PubMed  PubMed Central  Google Scholar 

  • Figueroa L, Barton S, Schull W, Razmilic B, Zumaeta O, Young A, Kamiya Y, Hoskins J, Ilgren E (2012) Environmental lithium exposure in the north of Chile—I. Natural water sources. Biol Trace Elem Res 149:280–290

    Article  CAS  PubMed  Google Scholar 

  • Fisberg M, Machado R (2015) History of yogurt and current patterns of consumption. Nutr Rev 73:4–7

    Article  PubMed  Google Scholar 

  • Fonseca JF, Torres CAA, Maffili VV, Borges AM, Santos ADF, Rodrigues MT, Oliveira RFM (2005) The hypoosmotic swelling test in fresh goat spermatozoa. Anim Reprod 2:139–144

    Google Scholar 

  • Gates AC, Bernal-Mizrachi C, Chinault SL, Feng C, Schneider JG, Coleman T, Malone JP, Townsend RR, Chakravarthy MV, Semenkovich CF (2007) Respiratory uncoupling in skeletal muscle delays death and diminishes age-related disease. Cell Metab 6:497–505

    Article  CAS  PubMed  Google Scholar 

  • Gatti J-L, Castella S, Dacheux F, Ecroyd H, Metayer S, Thimon V, Dacheux J-L (2004) Post-testicular sperm environment and fertility. Anim Reprod Sci 82:321–339

    Article  PubMed  Google Scholar 

  • Giommi C, Habibi HR, Candelma M, Carnevali O, Maradonna F (2021) Probiotic administration mitigates bisphenol A reproductive toxicity in zebrafish. Int J Mol Sci 22:9314

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guo X-F, Gao J-L, Li J-M, Li D (2017) fat-1 mice prevent high-fat plus high-sugar diet-induced non-alcoholic fatty liver disease. Food Funct 8:4053–4061

    Article  CAS  PubMed  Google Scholar 

  • Hammoud AO, Wilde N, Gibson M, Parks A, Carrell DT, Meikle AW (2008) Male obesity and alteration in sperm parameters. Fertil Steril 90:2222–2225

    Article  PubMed  Google Scholar 

  • Hawksworth DJ, Burnett AL (2020) Nonalcoholic fatty liver disease, male sexual dysfunction, and infertility: common links, common problems. Sex Med Rev 8:274–285

    Article  PubMed  Google Scholar 

  • Heaney RP, Rafferty K, Dowell MS (2002) Effect of yogurt on a urinary marker of bone resorption in postmenopausal women. J Am Diet Assoc 102:1672–1674

    Article  PubMed  Google Scholar 

  • Heidari R, Behnamrad S, Khodami Z, Ommati MM, Azarpira N, Vazin A (2019) The nephroprotective properties of taurine in colistin-treated mice is mediated through the regulation of mitochondrial function and mitigation of oxidative stress. Biomed Pharmacother 109:103–111

    Article  CAS  PubMed  Google Scholar 

  • Heidari R, Jamshidzadeh A, Niknahad H, Safari F, Azizi H, Abdoli N, Ommati MM, Khodaei F, Saeedi A, Najibi A (2016) The hepatoprotection provided by taurine and glycine against antineoplastic drugs induced liver injury in an ex vivo model of normothermic recirculating isolated perfused rat liver. Trends Pharm Sci 2:59–76

    CAS  Google Scholar 

  • Heidari R, Mohammadi H, Ghanbarinejad V, Ahmadi A, Ommati MM, Niknahad H, Jamshidzadeh A, Azarpira N, Abdoli N (2018) Proline supplementation mitigates the early stage of liver injury in bile duct ligated rats. J Basic Clin Physiol Pharmacol 30:91–101

    Article  PubMed  Google Scholar 

  • Heidari R, Niknahad H, Jamshidzadeh A, Azarpira N, Bazyari M, Najibi A (2015) Carbonyl traps as potential protective agents against methimazole-induced liver injury. J Biochem Mol Toxicol 29:173–181

    Article  CAS  PubMed  Google Scholar 

  • Helli B, Kavianpour M, Ghaedi E, Dadfar M, Haghighian HK (2020) Probiotic effects on sperm parameters, oxidative stress index, inflammatory factors and sex hormones in infertile men. Human Fertility 1–9. https://doi.org/10.1080/14647273.2020.1824080

  • Henderson N, Robaire B (2005) Effects of PNU157706, a dual 5 -reductase inhibitor, on rat epididymal sperm maturation and fertility. Biol Reprod 72:436–443

    Article  CAS  PubMed  Google Scholar 

  • Hofny ER, Ali ME, Abdel-Hafez HZ, Kamal EE-D, Mohamed EE, Abd El-Azeem HG, Mostafa T (2010) Semen parameters and hormonal profile in obese fertile and infertile males. Fertil Steril 94:581–584

    Article  CAS  PubMed  Google Scholar 

  • Hooper LV, Wong MH, Thelin A, Hansson L, Falk PG, Gordon JI (2001) Molecular analysis of commensal host-microbial relationships in the intestine. Science 291:881–884

    Article  CAS  PubMed  Google Scholar 

  • Ibrahim HA, Zhu Y, Wu C, Lu C, Ezekwe MO, Liao SF, Huang K (2012) Selenium-enriched probiotics improves murine male fertility compromised by high fat diet. Biol Trace Elem Res 147:251–260

    Article  CAS  PubMed  Google Scholar 

  • Iftikhar M, Noureen A, Uzair M, Jabeen F, Abdel Daim M, Cappello T (2021) Perspectives of nanoparticles in male infertility: evidence for induced abnormalities in sperm production. Int J Environ Res Public Health 18:1758

  • Ilacqua A, Francomano D, Aversa A (2015) Obesity and testicular function. In: Lenzi A, Migliaccio S, Donini LM (eds) Multidisciplinary Approach to Obesity: From Assessment to Treatment. Springer International Publishing, Cham

    Google Scholar 

  • Inatomi T, Otomaru K (2018) Effect of dietary probiotics on the semen traits and antioxidative activity of male broiler breeders. Sci Rep 8:1–6

    Article  CAS  Google Scholar 

  • Jamshidzadeh A, Dabagh F, Farshad O, Ommat MM, Mahdavinia A, Azarpira N, Shahbazi M, Najibi A, Heidari R (2018) Hepatoprotective properties of the glycolipoprotein extract from Eisenia foetida. Trends Pharm Sci 4:149–160

    Google Scholar 

  • Jamshidzadeh A, Niknahad H, Heidari R, Zarei M, Ommati MM, Khodaei F (2017) Carnosine protects brain mitochondria under hyperammonemic conditions: Relevance to hepatic encephalopathy treatment. PharmaNutrition 5:58–63

    Article  Google Scholar 

  • Jungheim ES, Travieso JL, Carson KR, Moley KH (2012) Obesity and reproductive function. Obstet Gynecol Clin North Am 39:479–493

    Article  PubMed  PubMed Central  Google Scholar 

  • Kadooka Y, Sato M, Imaizumi K, Ogawa A, Ikuyama K, Akai Y, Okano M, Kagoshima M, Tsuchida T (2010) Regulation of abdominal adiposity by probiotics (Lactobacillus gasseri SBT2055) in adults with obese tendencies in a randomized controlled trial. Eur J Clin Nutr 64:636–643

    Article  CAS  PubMed  Google Scholar 

  • Kang J-H, Yun S-I, Park M-H, Park J-H, Jeong S-Y, Park H-O (2013) Anti-obesity effect of Lactobacillus gasseri BNR17 in high-sucrose diet-induced obese mice. PloS one 8:e54617

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kasturi SS, Tannir J, Brannigan RE (2008) The Metabolic Syndrome and Male Infertility. J Androl 29:251–259

    Article  CAS  PubMed  Google Scholar 

  • Katalinic V, Modun D, Music I, Boban M (2005) Gender differences in antioxidant capacity of rat tissues determined by 2,2′-azinobis (3-ethylbenzothiazoline 6-sulfonate; ABTS) and ferric reducing antioxidant power (FRAP) assays. Comp Biochem Physiol Toxicol Pharmacol 140:47–52

    Article  CAS  Google Scholar 

  • Khorasgani MR, Shafiei R (2017) Traditional yogurt as a source of lactobacilli and other lactic acid bacteria in Iran.In: SHAH, N. P. (ed.) Yogurt in Health and Disease Prevention. Academic Press 285–294. https://doi.org/10.1016/B978-0-12-805134-4.00016-X

  • Kobyliak N, Abenavoli L, Falalyeyeva T, Mykhalchyshyn G, Boccuto L, Kyriienko D, Kononenko L, Komisarenko I, Dynnyk O (2018a) Beneficial effects of probiotic combination with omega-3 fatty acids in NAFLD: a randomized clinical study. Minerva Medica 109:418–28

    Article  PubMed  Google Scholar 

  • Kobyliak N, Abenavoli L, Mykhalchyshyn G, Kononenko L, Boccuto L, Kyriienko D, Dynnyk O (2018b) A multi-strain probiotic reduces the fatty liver index, cytokines and aminotransferase levels in NAFLD patients: evidence from a randomized clinical trial. J Gastrointest Liver 27:41–49

    Article  Google Scholar 

  • Korada SK, Yarla NS, Mishra V, Daim MA, Sharma B, Gm A, Reggi R, Palmery M, Peluso I, Kamal MA (2018) Single probiotic versus multiple probiotics - a debate on current scenario for alleviating health benefits. Curr Pharm Des 24:4150–4153

    Article  CAS  PubMed  Google Scholar 

  • Kort HI, Massey JB, Elsner CW, Mitchell-Leef D, Shapiro DB, Witt MA, Roudebush WE (2006) Impact of body mass index values on sperm quantity and quality. J Androl 27:450–452

    Article  PubMed  Google Scholar 

  • Král M, Angelovičová M, Mrázová Ľ (2012) Application of probiotics in poultry production. Sci Pap Anim Sci Biotechnologies 45:55–57

    Google Scholar 

  • Kullisaar T, Songisepp E, Zilmer M (2012) Probiotics and oxidative stress. In: Lushchak VI (ed) oxidative stress. IntechOpen, Rijeka

    Google Scholar 

  • Lee H-Y, Park J-H, Seok S-H, Baek M-W, Kim D-J, Lee K-E, Paek K-S, Lee Y, Park J-H (2006) Human originated bacteria, Lactobacillus rhamnosus PL60, produce conjugated linoleic acid and show anti-obesity effects in diet-induced obese mice. Biochim Biophys Acta (BBA)-Mol Cell Biol Lipids 1761:736–744

    CAS  Google Scholar 

  • Lee K, Paek K, Lee HY, Park JH, Lee Y (2007) Antiobesity effect of trans-10, cis-12-conjugated linoleic acid-producing Lactobacillus plantarum PL62 on diet-induced obese mice. J Appl Microbiol 103:1140–1146

    Article  CAS  PubMed  Google Scholar 

  • Lesbros-Pantoflickova D, Corthésy-Theulaz I, Blum AL (2007) Helicobacter pylori and probiotics. J Nutr 137:812s-s818

    Article  CAS  PubMed  Google Scholar 

  • Ley RE, Turnbaugh PJ, Klein S, Gordon JI (2006) Human gut microbes associated with obesity. Nature 444:1022–1023

    Article  CAS  PubMed  Google Scholar 

  • Li RW, Douglas TD, Maiyoh GK, Adeli K, Theriault AG (2006) Green tea leaf extract improves lipid and glucose homeostasis in a fructose-fed insulin-resistant hamster model. J Ethnopharmacol 104:24–31

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Liu L, Wang B, Xiong J, Li Q, Wang J, Chen D (2013) Impairment of reproductive function in a male rat model of non-alcoholic fatty liver disease and beneficial effect of N-3 fatty acid supplementation. Toxicol Lett 222:224–232

    Article  CAS  PubMed  Google Scholar 

  • Ljiljak D, Milaković TT, Severinski NS, Kuna KB, Radojčić A (2012) Sperm cell in art, intech. https://doi.org/10.5772/37498

  • Longato L (2013) Non-alcoholic fatty liver disease (NAFLD): a tale of fat and sugar? Fibrogenesis Tissue Repair 6:14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ma Y-Y, Li L, Yu C-H, Shen Z, Chen L-H, Li Y-M (2013) Effects of probiotics on nonalcoholic fatty liver disease: a meta-analysis. World J Gastroenterol 19:6911–6918

    Article  PubMed  PubMed Central  Google Scholar 

  • Magnusdottir EV, Thorsteinsson T, Thorsteinsdottir S, Heimisdottir M, Olafsdottir K (2005) Persistent organochlorines, sedentary occupation, obesity and human male subfertility. Hum Reprod 20:208–215

    Article  PubMed  Google Scholar 

  • Mandour AS, Samir H, El-Beltagy MA, Abdel-Daim MM, Izumi W, Ma D, Matsuura K, Tanaka R, Watanabe G (2020) Effect of supra-nutritional selenium-enriched probiotics on hematobiochemical, hormonal, and Doppler hemodynamic changes in male goats. Environ Sci Pollut Res 27:19447–19460

    Article  CAS  Google Scholar 

  • Maretti C, Cavallini G (2017) The association of a probiotic with a prebiotic (Flortec, Bracco) to improve the quality/quantity of spermatozoa in infertile patients with idiopathic oligoasthenoteratospermia: a pilot study. Andrology 5:439–444

    Article  CAS  PubMed  Google Scholar 

  • Martı́nez AP (2004) Canine fresh and cryopreserved semen evaluation. Anim Reprod Sci 82:209–224

    Article  PubMed  Google Scholar 

  • Mazanko MS, Gorlov IF, Prazdnova EV, Makarenko MS, Usatov AV, Bren AB, Chistyakov VA, Tutelyan AV, Komarova ZB, Mosolova NI (2018) Bacillus probiotic supplementations improve laying performance, egg quality, hatching of laying hens, and sperm quality of roosters. Probiotics Antimicrob Proteins 10:367–373

    Article  CAS  PubMed  Google Scholar 

  • McFarland LV, Dublin S (2008) Meta-analysis of probiotics for the treatment of irritable bowel syndrome. World J Gastroenterol: WJG 14:2650

    Article  PubMed  PubMed Central  Google Scholar 

  • McGuire T (2020) Advancing your practice: probiotics and DHA: their role in female reproductive health. AJP: Aust J Pharm 101:64

    Google Scholar 

  • Meeks RG, Harrison S (1991) Hepatotoxicology. CRC Press, New York

    Google Scholar 

  • Meroni M, Longo M, Dongiovanni P (2019) The role of probiotics in nonalcoholic fatty liver disease: a new insight into therapeutic strategies. Nutrients 11:2642

    Article  CAS  PubMed Central  Google Scholar 

  • Mosoeunyane NV (2006) Effect of alternatives to antibiotic growth promoters on broiler performance. Thesis: Masters Degrees (Animal and Poultry Science). URL http://hdl.handle.net/10413/4382

  • Nabavi S, Rafraf M, Somi M-H, Homayouni-Rad A, Asghari-Jafarabadi M (2015) Probiotic yogurt improves body mass index and fasting insulin levels without affecting serum leptin and adiponectin levels in non-alcoholic fatty liver disease (NAFLD). J Funct Foods 18:684–691

    Article  CAS  Google Scholar 

  • Nguyen RH, Wilcox AJ, Skjaerven R, Baird DD (2007) Men’s body mass index and infertility. Hum Reprod 22:2488–2493

    Article  PubMed  Google Scholar 

  • Nikkhah A (2014) Yogurt the most natural and healthy probiotic: history reveals. J Prob Health 2:e110

    Article  Google Scholar 

  • Niknahad H, Jamshidzadeh A, Heidari R, Hosseini Z, Mobini K, Khodaei F, Ommati MM, Abdoli N, Keshavarz N, Bazyari M, Najibi A (2016) Paradoxical effect of methimazole on liver mitochondria: In vitro and in vivo. Toxicol Lett 259:108–115

    Article  CAS  PubMed  Google Scholar 

  • Noshahr ZS, Shahraki MR, Ahmadvand H, Nourabadi D, Nakhaei A (2015) Protective effects of Withania somnifera root on inflammatory markers and insulin resistance in fructose-fed rats. Rep Biochem Mol Biol 3:62

    Google Scholar 

  • Ommati M, Heidari R, Manthari R, Chiranjeevi ST, Niu R, Sun Z, Sabouri S, Zamiri M, Zaker L, Yuan J (2019) Paternal exposure to arsenic resulted in oxidative stress, autophagy, and mitochondrial impairments in the HPG axis of pubertal male offspring. Chemosphere 236:124325

    Article  CAS  PubMed  Google Scholar 

  • Ommati M, Zamiri M, Akhlaghi A, Atashi H, Jafarzadeh M, Rezvani M, Saemi F (2013a) Seminal characteristics, sperm fatty acids, and blood biochemical attributes in breeder roosters orally administered with sage (Salvia officinalis) extract. Anim Prod Sci 53:548–554

    Article  CAS  Google Scholar 

  • Ommati MM, Amjadinia A, Mousavi K, Azarpira N, Jamshidzadeh A, Heidari R (2020a) N-acetyl cysteine treatment mitigates biomarkers of oxidative stress in different tissues of bile duct ligated rats. Stress 0:1–16

    Google Scholar 

  • Ommati MM, Arabnezhad MR, Farshad O, Jamshidzadeh A, Niknahad H, Retana-Marquez S, Jia Z, Nateghahmadi MH, Mousavi K, Arazi A, Azmoon MR, Azarpira N, Heidari R (2021) The role of mitochondrial impairment and oxidative stress in the pathogenesis of lithium-induced reproductive toxicity in male mice. Front Vet Sci 8. https://doi.org/10.3389/fvets.2021.603262

  • Ommati MM, Farshad O, Azarpira N, Shafaghat M, Niknahad H, Heidari R (2020b) Betaine alleviates cholestasis-associated renal injury by mitigating oxidative stress and enhancing mitochondrial function. Biologia 76:351–365

    Article  Google Scholar 

  • Ommati MM, Farshad O, Ghanbarinejad V, Mohammadi HR, Khadijeh M, Negar A, Zahra M, Ilkhaninasab F, Moezi L, Heidari R (2020c) The nephroprotective role of carnosine against ifosfamide-induced renal injury and electrolytes imbalance is mediated via the regulation of mitochondrial function and alleviation of oxidative stress. Drug Res 70:49–56

    Article  CAS  Google Scholar 

  • Ommati MM, Farshad O, Jamshidzadeh A, Heidari R (2019) Taurine enhances skeletal muscle mitochondrial function in a rat model of resistance training. PharmaNutrition 9:100161

    Article  Google Scholar 

  • Ommati MM, Farshad O, Mousavi K, Jamshidzadeh A, Azmoon M, Heidari S, Azarpira N, Niknahad H, Heidari R (2020d) Betaine supplementation mitigates intestinal damage and decreases serum bacterial endotoxin in cirrhotic rats. PharmaNutrition 12:100179

    Article  Google Scholar 

  • Ommati MM, Farshad O, Mousavi K, Khalili M, Jamshidzadeh A, Heidari R (2020e) Chlorogenic acid supplementation improves skeletal muscle mitochondrial function in a rat model of resistance training. Biologia 75:1221–1230

    Article  CAS  Google Scholar 

  • Ommati MM, Farshad O, Mousavi K, Taghavi R, Farajvajari S, Azarpira N, Moezi L, Heidari R (2020f) Agmatine alleviates hepatic and renal injury in a rat model of obstructive jaundice. Pharma Nutrition 13:100212. https://doi.org/10.1016/j.phanu.2020.100212

  • Ommati MM, Farshad O, Niknahad H, Arabnezhad MR, Azarpira N, Mohammadi HR, Haghnegahdar M, Mousavi K, Akrami S, Jamshidzadeh A, Heidari R (2019c) Cholestasis-associated reproductive toxicity in male and female rats: The fundamental role of mitochondrial impairment and oxidative stress. Toxicol Lett 316:60–72

    Article  CAS  PubMed  Google Scholar 

  • Ommati MM, Farshad O, Niknahad H, Mousavi K, Moein M, Azarpira N, Mohammadi H, Jamshidzadeh A, Heidari R (2020g) Oral administration of thiol-reducing agents mitigates gut barrier disintegrity and bacterial lipopolysaccharide translocation in a rat model of biliary obstruction. Curr Res Pharmacol Drug Discov 1:10–18

    Article  PubMed  PubMed Central  Google Scholar 

  • Ommati MM, Farshad O, Niknahad H, Mousavi K, Moein M, Azarpira N, Mohammadi H, Jamshidzadeh A, Heidari R (2020h) Oral administration of thiol-reducing agents mitigates gut barrier disintegrity and bacterial lipopolysaccharide translocation in a rat model of biliary obstruction. Curr Res Pharmacol Drug Discov 1:10–18

    Article  PubMed  PubMed Central  Google Scholar 

  • Ommati MM, Heidari R (2021) Amino acids ameliorate heavy metals-induced oxidative stress in male/female reproductive tissue. Toxicology. Elsevier, pp. 371–386. https://doi.org/10.1016/B978-0-12-819092-0.00037-6

  • Ommati MM, Heidari R, Ghanbarinejad V, Abdoli N, Niknahad H (2019d) Taurine treatment provides neuroprotection in a mouse model of manganism. Biol Trace Elem Res 190:384–395

    Article  CAS  PubMed  Google Scholar 

  • Ommati MM, Heidari R, Ghanbarinejad V, Aminian A, Abdoli N, Niknahad H (2020i) The neuroprotective properties of carnosine in a mouse model of manganism is mediated via mitochondria regulating and antioxidative mechanisms. Nutr Neurosci 23:731–743

    Article  PubMed  Google Scholar 

  • Ommati MM, Heidari R, Jamshidzadeh A, Zamiri MJ, Sun Z, Sabouri S, Wang J, Ahmadi F, Javanmard N, Seifi K, Mousapour S, Yeganeh BS (2018a) Dual effects of sulfasalazine on rat sperm characteristics, spermatogenesis, and steroidogenesis in two experimental models. Toxicol Lett 284:46–55

    Article  CAS  PubMed  Google Scholar 

  • Ommati MM, Heidari R, Zamiri MJ, Sabouri S, Zaker L, Farshad O, Jamshidzadeh A, Mousapour S (2019e) The footprints of oxidative stress and mitochondrial impairment in arsenic trioxide-induced testosterone release suppression in pubertal and mature F1-male Balb/c mice via the downregulation of 3β-HSD, 17β-HSD, and CYP11a expression. Biol Trace Elem Res 195:125–134

    Article  PubMed  Google Scholar 

  • Ommati MM, Heidari R, Zamiri MJ, Shojaee S, Akhlaghi A, Sabouri S (2017a) Association of open field behavior with blood and semen characteristics in roosters: as an alternative animal model. Int Andrología 16:50–58

    Google Scholar 

  • Ommati MM, Jamshidzadeh A, Heidari R, Sun Z, Zamiri MJ, Khodaei F, Mousapour S, Ahmadi F, Javanmard N, Shirazi Yeganeh B (2018b) Carnosine and histidine supplementation blunt lead-induced reproductive toxicity through antioxidative and mitochondria-dependent mechanisms. Biol Trace Elem Res 187:151–162

    Article  PubMed  Google Scholar 

  • Ommati MM, Jamshidzadeh A, Niknahad H, Mohammadi H, Sabouri S, Heidari R, Abdoli N (2017b) N-acetylcysteine treatment blunts liver failure-associated impairment of locomotor activity. PharmaNutrition 5:141–147

    Article  Google Scholar 

  • Ommati MM, Manthari RK, Tikka C, Niu R, Sun Z, Sabouri S, Zamiri MJ, Ahmadi HN, Ghaffari H, Heidari R (2020j) Arsenic-induced autophagic alterations and mitochondrial impairments in HPG-S axis of mature male mice offspring (F1-generation): a persistent toxicity study. Toxicol Lett 326:83–98

    Article  CAS  PubMed  Google Scholar 

  • Ommati MM, Manthari RK, Tikka C, Niu R, Sun Z, Sabouri S, Zamiri MJ, Ahmadi HN, Ghaffari H, Heidari R, Wang J (2020k) Arsenic-induced autophagic alterations and mitochondrial impairments in HPG-S axis of mature male mice offspring (F1-generation): a persistent toxicity study. Toxicol Lett 326:83–98

    Article  CAS  PubMed  Google Scholar 

  • Ommati MM, Niknahad H, Farshad O, Azarpira N, Heidari R (2020l) In vitro and in vivo evidence on the role of mitochondrial impairment as a mechanism of lithium-induced nephrotoxicity. Biol Trace Elem Res 199:1908–1918

    Article  PubMed  Google Scholar 

  • Ommati MM, Shi X, Li H, Zamiri MJ, Farshad O, Jamshidzadeh A, Heidari R, Ghaffari H, Zaker L, Sabouri S, Chen Y (2020) The mechanisms of arsenic-induced ovotoxicity, ultrastructural alterations, and autophagic related paths: an enduring developmental study in folliculogenesis of mice. Ecotoxicol Environ Saf 204:110973

    Article  CAS  PubMed  Google Scholar 

  • Ommati MM, Tanideh N, Rezakhaniha B, Wang J, Sabouri S, Vahedi M, Dormanesh B, Koohi Hosseinabadi O, Rahmanifar F, Moosapour S, Akhlaghi A, Heidari R, Zamiri MJ (2018c) Is immunosuppression, induced by neonatal thymectomy, compatible with poor reproductive performance in adult male rats? Andrology 6:199–213

    Article  CAS  PubMed  Google Scholar 

  • Orgebin-Crist M, Tichenor P (1973) Effect of testosterone on sperm maturation in vitro. Nature 245:328–329

    Article  CAS  PubMed  Google Scholar 

  • Oyeyipo I, Maartens P, du Plessis S (2015) Diet-induced obesity alters kinematics of rat spermatozoa. Asian Pac J Reprod 4:235–239

    Article  Google Scholar 

  • Palmer NO, Bakos HW, Fullston T, Lane M (2012a) Impact of obesity on male fertility, sperm function and molecular composition. Spermatogenesis 2:253–263

    Article  PubMed  PubMed Central  Google Scholar 

  • Palmer NO, Bakos HW, Owens JA, Setchell BP, Lane M (2012b) Diet and exercise in an obese mouse fed a high-fat diet improve metabolic health and reverse perturbed sperm function. Am J Physiol Endocrinol Metab 302:768–780

    Article  Google Scholar 

  • Pauli EM, Legro RS, Demers LM, Kunselman AR, Dodson WC, Lee PA (2008) Diminished paternity and gonadal function with increasing obesity in men. Fertil Steril 90:346–351

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Perumpail BJ, Li AA, John N, Sallam S, Shah ND, Kwong W, Cholankeril G, Kim D, Ahmed A (2019) The therapeutic implications of the gut microbiome and probiotics in patients with NAFLD. Diseases 7:27

    Article  CAS  PubMed Central  Google Scholar 

  • Poutahidis T, Springer A, Levkovich T, Qi P, Varian BJ, Lakritz JR, Ibrahim YM, Chatzigiagkos A, Alm EJ, Erdman SE (2014) Probiotic microbes sustain youthful serum testosterone levels and testicular size in aging mice. PLoS One 9:84877

    Article  Google Scholar 

  • Qin DD, Yuan W, Zhou WJ, Cui YQ, Wu JQ, Gao ES (2007) Do reproductive hormones explain the association between body mass index and semen quality? Asian J Androl 9:827–834

    Article  CAS  PubMed  Google Scholar 

  • Quigley EMM (2007) Probiotics in irritable bowel syndrome: an immunomodulatory strategy? J Am Coll Nutr 26:684–690

    Article  Google Scholar 

  • Ramlau-Hansen CH, Thulstrup AM, Nohr EA, Bonde JP, Sørensen TI, Olsen J (2007) Subfecundity in overweight and obese couples. Hum Reprod 22:1634–1637

    Article  CAS  PubMed  Google Scholar 

  • Reid JNS, Bisanz JE, Monachese M, Burton JP, Reid G (2013) The rationale for probiotics improving reproductive health and pregnancy outcome. Am J Reprod Immunol 69:558–566

    CAS  PubMed  Google Scholar 

  • Rosales EB, Ametaj BN (2021) Reproductive tract infections in dairy cows: can probiotics curb down the incidence rate? Dairy 2:40–64

    Article  Google Scholar 

  • Lavekar AS, Raje DV, Manohar T, Lavekar AA (2017) Role of probiotics in the treatment of nonalcoholic fatty liver disease: a meta-analysis. Euroasian J Hepatogastroenterol 7:130–137

    Article  Google Scholar 

  • Saad RA, Mahmoud YI (2014) Ursodeoxycholic acid alleviates cholestasis-induced histophysiological alterations in the male reproductive system of bile duct-ligated rats. Reprod Toxicol 50:87–97

    Article  CAS  PubMed  Google Scholar 

  • Saemi F, Zamiri M, Akhlaghi A, Niakousari M, Dadpasand M, Ommati M (2012) Dietary inclusion of dried tomato pomace improves the seminal characteristics in Iranian native roosters. Poult Sci 91:2310–2315

    Article  CAS  PubMed  Google Scholar 

  • Salarkia N, Ghadamli L, Zaeri F, Rad LS (2013) Effects of probiotic yogurt on performance, respiratory and digestive systems of young adult female endurance swimmers: a randomized controlled trial. Med J Islam Repub Iran 27:141

    PubMed  PubMed Central  Google Scholar 

  • Sallmén M, Sandler DP, Hoppin JA, Blair A, Baird DD (2006) Reduced fertility among overweight and obese men. Epidemiology 17:520–523

    Article  PubMed  Google Scholar 

  • Sayiner S, Gülmez N, Sabit Z, Gülmez M (2019) Effects of deep-frying sunflower oil on sperm parameters in a mouse model: do probiotics have a protective effect? Kafkas Üniversitesi Veteriner Fakültesi Dergisi 25:857–863

    Google Scholar 

  • Sekhavat L, Moein MR (2010) The effect of male body mass index on sperm parameters. Aging Male 13:155–158

    Article  PubMed  Google Scholar 

  • Sharawy SM, Saleh NH, Attallah SA-E, Hashem GA, Khedre DH (2015) Effect of plant extract of Tribulus terrestris and probiotics on the reproductive performance, total cholesterol and testosterone hormone levels of rams. MENA Sci J 1:14–19

    Google Scholar 

  • Singh B, Mal G, Bharti D, Mohania D, Kumar M, Kumar Gautam S, Marotta F, Yadav H, Nagpal R (2013) Probiotics in female reproductive health: paradigms, prospects and challenges. Curr Women’s Health Rev 9:235–244

    Article  Google Scholar 

  • Sousa R, Halper J, Zhang J, Lewis SJ, Li W-IO (2008) Effect of Lactobacillus acidophilus supernatants on body weight and leptin expression in rats. BMC Complement Altern Med 8:1–8

    Article  Google Scholar 

  • Spiller R (2008) Probiotics and prebiotics in irritable bowel syndrome. Aliment Pharmacol Ther 28:385–396

    Article  CAS  PubMed  Google Scholar 

  • Su F-H, Chang S-N, Sung F-C, Su C-T, Shieh Y-H, Lin C-C, Yeh C-C (2014) Hepatitis B virus infection and the risk of male infertility: a population-based analysis. Fertil Steril 102:1677–1684

    Article  PubMed  Google Scholar 

  • Su H-M, Feng L-N, Zheng X-D, Chen W (2016) Myricetin protects against diet-induced obesity and ameliorates oxidative stress in C57BL/6 mice. J Zhejiang Univ Sci B 17:437–446

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Su H, Li R, He X, Chen J, Han Z, Liu Y, Zhang J (2009) Effects of selenium-enriched probiotics on sperm quality of stock boars. Guangdong Agricu Sci 7:156–158

    Google Scholar 

  • Sun Z, Li S, Yu Y, Chen H, Ommati MM, Manthari RK, Niu R, Wang J (2018) Alterations in epididymal proteomics and antioxidant activity of mice exposed to fluoride. Arch Toxicol 92:169–180

    Article  CAS  PubMed  Google Scholar 

  • Takemura N, Okubo T, Sonoyama K (2010) Lactobacillus plantarum strain No. 14 reduces adipocyte size in mice fed high-fat diet. Exp Biol Med 235:849–856

    Article  CAS  Google Scholar 

  • Tappenden KA, Deutsch AS (2007) The physiological relevance of the intestinal microbiota-contributions to human health. J Am Coll Nutr 26:679–683

    Article  Google Scholar 

  • Tomoda T, Nakano Y, Kageyama T (1991) Effect of yogurt and yogurt supplemented with Bifidobacterium and/or lactulose in healthy persons: a comparative study. Bifidobacteria Microflora 10:123–130

    Article  Google Scholar 

  • Toocheck C, Clister T, Shupe J, Crum C, Ravindranathan P, Lee T-K, Ahn J-M, Raj GV, Sukhwani M, Orwig KE (2016) Mouse spermatogenesis requires classical and nonclassical testosterone signaling. Biol Reprod 94:1–14

    Article  Google Scholar 

  • Truong DH, Eghbal MA, Hindmarsh W, Roth SH, O’Brien PJ (2006) Molecular mechanisms of hydrogen sulfide toxicity. Drug Metab Rev 38:733–744

    Article  CAS  PubMed  Google Scholar 

  • Tsuchiya H, Ebata Y, Sakabe T, Hama S, Kogure K, Shiota G (2013) High-fat, high-fructose diet induces hepatic iron overload via a hepcidin-independent mechanism prior to the onset of liver steatosis and insulin resistance in mice. Metabolism 62:62–69

    Article  CAS  PubMed  Google Scholar 

  • Udoh U, Inyang U (2017) Effects of probiotics therapy on semen quality traits of west african dwarf bucks. J Agric Prod Technol ISSN 2360:9364

    Google Scholar 

  • Valcarce DG, Riesco MF, Martínez-Vázquez JM, Robles V (2019a) Diet supplemented with antioxidant and anti-inflammatory probiotics improves sperm quality after only one spermatogenic cycle in zebrafish model. Nutrients 11:843

    Article  CAS  PubMed Central  Google Scholar 

  • Valcarce DG, Riesco MF, Martínez-Vázquez JM, Robles V (2019b) Long exposure to a diet supplemented with antioxidant and anti-inflammatory probiotics improves sperm quality and progeny survival in the Zebrafish model. Biomolecules 9:338

    Article  CAS  PubMed Central  Google Scholar 

  • Vílchez MC, Santangeli S, Maradonna F, Gioacchini G, Verdenelli C, Gallego V, Peñaranda DS, Tveiten H, Pérez L, Carnevali O (2015) Effect of the probiotic Lactobacillus rhamnosus on the expression of genes involved in European eel spermatogenesis. Theriogenology 84:1321–1331

    Article  PubMed  Google Scholar 

  • Vos MB, Lavine JE (2013) Dietary fructose in nonalcoholic fatty liver disease. Hepatology 57:2525–2531

    Article  CAS  PubMed  Google Scholar 

  • Walker WH (2011) Testosterone signaling and the regulation of spermatogenesis. Spermatogenesis 1:116–120

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang J, Chen L (2021) Impact of a novel nano-protectant on the viability of probiotic bacterium lactobacillus casei k17. Foods 10:529

    Article  PubMed  PubMed Central  Google Scholar 

  • Weber D, Davies MJ, Grune T (2015) Determination of protein carbonyls in plasma, cell extracts, tissue homogenates, isolated proteins: focus on sample preparation and derivatization conditions. Redox Biol 5:367–380

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • West CE, Prescott SL (2013) Chapter 16 - probiotics and eczema. In: Watson RR, Preedy VR (eds) Bioactive Food as Dietary Interventions for Arthritis and Related Inflammatory Diseases. Academic Press, San Diego

    Google Scholar 

  • WHO (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. WHO, Geneva

    Google Scholar 

  • Wong VW-S, Wong GL-H, Chim AM-L, Chu WC-W, Yeung DK-W, Li KC-T, Chan HL-Y (2015) Treatment of nonalcoholic steatohepatitis with probiotics. A proof-of-concept study. Annals Hepatol 12:256–262

    Article  Google Scholar 

  • Yang G, Liu Z-Q, Yang P-C (2013) Treatment of allergic rhinitis with probiotics: an alternative approach. N Am J Med Sci 5:465–468

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu Y, Han Y, Niu R, Wang J, Manthari RK, Ommati MM, Sun Z (2017) Ameliorative effect of VE, IGF-I, and hCG on the fluoride-induced testosterone release suppression in mice Leydig cells. Biol Trace Elem Res 181:95–103

    Article  PubMed  Google Scholar 

  • Zeitoun M, Farahna M, Al-Sobayil K, Abdel-Salam A (2014) Impact of the aqueous extract of dandelion, probiotic and their synbiotic on male lamb’s testicular histopathology relative to semen characteristics. Open J Anim Sci 4:23–30

    Article  Google Scholar 

  • Zhu Y, Xiao L, Shen D, Hao Y (2010) Competition between yogurt probiotics and periodontal pathogens in vitro. Acta Odontol Scand 68:261–268

    Article  PubMed  Google Scholar 

  • Zini A, San Gabriel M, Baazeem A (2009) Antioxidants and sperm DNA damage: a clinical perspective. J Assist Reprod Genet 26:427–432

    Article  PubMed  PubMed Central  Google Scholar 

  • Zoghi A, Khosravi-Darani K, Sohrabvandi S (2014) Surface binding of toxins and heavy metals by probiotics. Mini Rev Med Chem 14:84–98

    Article  CAS  PubMed  Google Scholar 

Download references

Funding

Departments of Pharmaceutical Sciences (Shiraz University of Medicine, Shiraz, Iran; Grant No. 1396–01-36–16455) and Life Sciences (Shanxi Agricultural University; Grant No. 2018YJ33 and outstanding doctors volunteering to work in Shanxi Province; Grant No. K271999031 by Dr. M. Mehdi Ommati).

Author information

Author notes

  1. Omid Farshad

    Present address: College of Pharmacy and Nutrition, School of Pharmacy, University of Saskatchewan, Saskatoon, Canada

Authors and Affiliations

  1. College of Life Sciences, Shanxi Agricultural University, Taigu, Shanxi, 030801, People’s Republic of China

    Mohammad Mehdi Ommati, Huifeng Li & Yu Lu

  2. Pharmaceutical Sciences Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

    Akram Jamshidzadeh, Omid Farshad & Reza Heidari

  3. Department of Pharmacology and Toxicology, School of Pharmacy, Shiraz University of Medical Sciences, Shiraz, Iran

    Akram Jamshidzadeh & Fereshteh Khoshghadam

  4. Department of Biology of Reproduction, Autonomous Metropolitan University-Iztapalapa, Mexico City, Mexico

    Socorro Retana-Márquez

  5. Shanxi Key Laboratory of Ecological Animal Science and Environmental Veterinary Medicine, Shanxi Agricultural University, Taigu, Shanxi, 030801, People’s Republic of China

    Mohammad Hasan Nategh Ahmadi

  6. Department of Clinical Studies, School of Veterinary Medicine, Shiraz University, 71345, Shiraz, Iran

    Mohammad Hasan Nategh Ahmadi

  7. Biotechnology Research Center, Shiraz University of Medical Sciences, Shiraz, Iran

    Ahmad Gholami

Authors
  1. Mohammad Mehdi Ommati
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Huifeng Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Akram Jamshidzadeh
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Fereshteh Khoshghadam
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Socorro Retana-Márquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu Lu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Omid Farshad
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Mohammad Hasan Nategh Ahmadi
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Ahmad Gholami
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Reza Heidari
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors declare that all data were generated in-house and that no paper mill was used.

Conceptualization and methodology: M.M.O., R. H., M. H. M., R-M. S., and A. J.

Data curation and investigation: M.M.O., O. F., F. KH., H. L.

Data analysis: M.M.O. and R. H.

Funding acquisition: M. M. O and A. J.

Project administration: M. M. O., R. H., A. J., M. H. N. A., M. S.

Supervision: M. M. O., R. H., A. J.

Writing—original draft: M. M. O.

Writing—review and editing: M. M. O., R. H., R-M. S., A. J.

Corresponding authors

Correspondence to Mohammad Mehdi Ommati or Reza Heidari.

Ethics declarations

Ethics approval

Ethical approval was waived by the local Ethics Committee of Shiraz University of Medical Sciences in view of the retrospective nature of the study and all the procedures being performed were part of the routine care.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Competing interests

The authors declare no competing interests.

Additional information

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ommati, M.M., Li, H., Jamshidzadeh, A. et al. The crucial role of oxidative stress in non-alcoholic fatty liver disease-induced male reproductive toxicity: the ameliorative effects of Iranian indigenous probiotics. Naunyn-Schmiedeberg's Arch Pharmacol 395, 247–265 (2022). https://doi.org/10.1007/s00210-021-02177-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00210-021-02177-0

Keywords

Search

Navigation