By ameliorating redox imbalance, patients of oligoasthenospermia increased sperm acrosin activity after smoking cessation in Chinese

Al mejorar el desequilibrio redox, la actividad de la enzima Acrosin espermatozoidal aumenta en pacientes chinos con oligoastenospermia después de dejar de fumar

Background: The massive harmful effects of cigarette (tobacco) smoking on reproduction and fecundity are apparent. Even smoking cessation is often suggested for infertility patients by clinic doctors, while the impact of smoking cessation on semen quality in patients with oligoasthenospermia is uncovered. Methods: Ninety oligoasthenospermia patients with long tobacco smoking history were directed by andrology doctors to cease smoking, and their cessation was followed up for 3 to 6 months. The changes of semen quality after cessation in patients with at least 70%cessation ratio were evaluated by Paired-t-test for the changes in sperm concentration (SC), sperm progressive motility (PR), sperm volume (SV), sperm acrosin activity (SAA), total sperm count (TSC), normal sperm morphology rate (NSMR) and DNA fragmentation index (DFI). The cessation index was calculated for each patient, and its correlation with changes of semen parameters was analyzed. Results: Among 90 study cases, 81 were followed up successfully. Upon andrology doctors’ routine instructions, only 19 (23.5%, 19/81) achieved a minimum requirement of 70% cessation ratio. In such a cessation level, only SAA has a significant difference after smoking cessation and a significant correlation was observed between the cessation index with the changes in SAA. Inceased glutathione (GSH) level and decreased reactive oxygen species (ROS) level were found in sperm cells and seminal plasma after smoking cessation. Conclusions: Andrology doctors’ routine instructions could not accomplish an ideal level of smoking cessation. The intervene of tobacco smoking cessation for patients of oligoasthenospermia only resulted in a significant improvement of SAA by ameliorating redox imbalance. The goal of improving male reproductive function may be achieved by further improvement of smoking cessation strategies.

Resumen

Antecedentes: Los enormes efectos nocivos del tabaquismo en la reproducción y la reproducción son evidentes. Incluso en pacientes infértiles, los clínicos a menudo recomiendan dejar de fumar, y el efecto de dejar de fumar en la calidad del semen de los pacientes con oligoastenospermia aún no se ha detectado. Métodos: El virólogo guió a 90 pacientes con oligoastenospermia con antecedentes de tabaquismo a largo plazo a dejar de fumar y los siguió de 3 a 6 meses. Los cambios en la calidad del semen después de dejar de fumar en pacientes con una tasa de dejar de fumar de al menos el 70% se evaluaron mediante una prueba t emparejada para detectar cambios en la concentración de espermatozoides (SC), el movimiento progresivo de espermatozoides (PR), el volumen de espermatozoides (SV), la actividad acrosina de espermatozoides (SAA), el número total de espermatozoides (TSC), la tasa morfológica normal de espermatozoides (NSMR) y el índice de fragmentación del ADN (DFI). Se calculó el índice de parada de cada paciente y se analizó su correlación con los cambios en los parámetros del semen. Resultados: De los 90 casos estudiados, 81 fueron seguidos con éxito. Solo 19 personas (23.5%, 19/81) alcanzaron el mínimo del 70% de la tasa de dejar de fumar, según las instrucciones habituales de los virólogos. Bajo este nivel de dejar de fumar, solo la SAA tiene diferencias significativas después de dejar de fumar, y hay una correlación significativa entre el índice de dejar de fumar y los cambios en la SAA. Después de dejar de fumar, los niveles de GSH en los espermatozoides y el plasma seminal aumentaron y los niveles de Especies de oxígeno activo (ROS) disminuyeron. Conclusiones: La orientación rutinaria de los médicos masculinos no puede alcanzar el nivel ideal de dejar de fumar. La intervención para dejar de fumar en pacientes con oligoastenospermia solo mejora significativamente la SAA mejorando el desequilibrio redox. Al mejorar aún más las estrategias para dejar de fumar, se puede lograr el objetivo de mejorar la función reproductiva masculina.

Smoking cessation; Oligoasthenospermia; Sperm acrosin activity; Redox imbalance

Palabras Clave

Dejar de fumar; Oligoastenospermia; Actividad de la enzima Acrosoma espermática; Desequilibrio redox

[1] Chan KH, Xiao D, Zhou M, Peto R, Chen Z. Tobacco control in China. The Lancet Public Health. 2023; 8: e1006–e1015.

[2] Dai X, Gakidou E, Lopez AD. Evolution of the global smoking epidemic over the past half century: strengthening the evidence base for policy action. Tobacco Control. 2022; 31: 129–137.

[3] The national health and family planning commission of the people’s republic of China. The guidelines for clinical smoking cessation in China (2015 edition). People’s Medical Publishing House Co., LTD.: Beijing. 2015.

[4] Wei X, Guo K, Shang X, Wang S, Yang C, Li J, et al. Effects of different interventions on smoking cessation in chronic obstructive pulmonary disease patients: a systematic review and network meta-analysis. International Journal of Nursing Studies. 2022; 136: 104362.

[5] Gepner AD, Piper ME, Johnson HM, Fiore MC, Baker TB, Stein JH. Effects of smoking and smoking cessation on lipids and lipoproteins: outcomes from a randomized clinical trial. American Heart Journal. 2011; 161: 145–151.

[6] Lei S, Li M, Duan W, Peng C, Chen P, Wu S. The long-term outcomes of tobacco control strategies based on the cognitive intervention for smoking cessation in COPD patients. Respiratory Medicine. 2020; 172: 106155.

[7] Levine H, Jørgensen N, Martino-Andrade A, Mendiola J, Weksler-Derri D, Jolles M, et al. Temporal trends in sperm count: a systematic review and meta-regression analysis of samples collected globally in the 20th and 21st centuries. Human Reproduction Update. 2023; 29: 157–176.

[8] Sengupta P, Borges E, Dutta S, Krajewska-Kulak E. Decline in sperm count in European men during the past 50 years. Human & Experimental Toxicology. 2018; 37: 247–255.

[9] Sharma R, Harlev A, Agarwal A, Esteves SC. Cigarette smoking and semen quality: a new meta-analysis examining the effect of the 2010 World Health Organization laboratory methods for the examination of human semen. European Urology. 2016; 70: 635–645.

[10] Engel KM, Baumann S, Blaurock J, Rolle-Kampczyk U, Schiller J, von Bergen M, et al. Differences in the sperm metabolomes of smoking and nonsmoking men†. Biology of Reproduction. 2021; 105: 1484–1493.

[11] Rehman R, Zahid N, Amjad S, Baig M, Gazzaz ZJ. Relationship between smoking habit and sperm parameters among patients attending an infertility clinic. Front Physiol. 2019; 10: 1356–1364.

[12] Christou MA, Christou PA, Markozannes G, Tsatsoulis A, Mastorakos G, Tigas S. Effects of anabolic androgenic steroids on the reproductive system of athletes and recreational users: a systematic review and meta-analysis. Sports Medicine. 2017; 47: 1869–1883.

[13] Ghasemi-Esmailabad S, Talebi AH, Talebi AR, Amiri S, Moshrefi M, Porentezari M. The effects of morphine abuse on sperm parameters, chromatin integrity and apoptosis in men. JBRA Assisted Reproduction. 2022; 26: 444–449.

[14] Bedi YS, Wang H, Thomas KN, Basel A, Prunier J, Robert C, et al. Alcohol induced increases in sperm Histone H3 lysine 4 trimethylation correlate with increased placental CTCF occupancy and altered developmental programming. Scientific Reports. 2022; 12: 8839.

[15] Finelli R, Mottola F, Agarwal A. Impact of alcohol consumption on male fertility potential: a narrative review. International Journal of Environmental Research and Public Health. 2021; 19: 328.

[16] Aprioku JS, Boms R, Ife-tubiyele DO. Effect of simultaneous coffee/caffeine and ethanol administration on sperm quality and reproductive hormones: an experimental study in Sprague Dawley rats. Drug and Chemical Toxicology. 2022; 45: 1012–1020.

[17] Leisegang K, Sengupta P, Agarwal A, Henkel R. Obesity and male infertility: mechanisms and management. Andrologia. 2021; 53: e13617.

[18] Suliga E, Głuszek S. The relationship between diet, energy balance and fertility in men. International Journal for Vitamin and Nutrition Research. 2020; 90: 514–526.

[19] Mai H, Ke J, Zheng Z, Luo J, Li M, Qu Y, et al. Association of diet and lifestyle factors with semen quality in male partners of Chinese couples preparing for pregnancy. Reproductive Health. 2023; 20: 173.

[20] Straub L, Strobl V, Bruckner S, Camenzind DW, Van Oystaeyen A, Wäckers F, et al. Buffered fitness components: antagonism between malnutrition and an insecticide in bumble bees. The Science of the Total Environment. 2022; 833: 155098.

[21] Akhigbe RE, Akhigbe TM, Adegbola CA, Oyedokun PA, Adesoye OB, Adeogun AE. Toxic impacts of arsenic bioaccumulation on urinary arsenic metabolites and semen quality: a systematic and meta-analysis. Ecotoxicology and Environmental Safety. 2024; 281: 116645.

[22] Sun Z, Wen Y, Wang B, Deng S, Zhang F, Fu Z, et al. Toxic effects of per- and polyfluoroalkyl substances on sperm: Epidemiological and experimental evidence. Frontiers in Endocrinology. 2023; 14: 1114463.

[23] Massányi P, Massányi M, Madeddu R, Stawarz R, Lukáč N. Effects of cadmium, lead, and mercury on the structure and function of reproductive organs. Toxics. 2020; 8: 94.

[24] Fasihi-Ramandi M, Bayat G, Kachuei R, Golmohammadi R. Effects of aflatoxin B1 exposure on sperm in rodents: a systematic review and meta-analysis. International Journal of Environmental Health Research. 2023; 33: 1629–1639.

[25] Zhang TY, Wu RY, Zhao Y, Xu CS, Zhang WD, Ge W, et al. Ochratoxin A exposure decreased sperm motility via the AMPK and PTEN signaling pathways. Toxicology and Applied Pharmacology. 2018; 340: 49–57.

[26] Ahmadnia H, Ghanbari M, Moradi MR, Khaje-Dalouee M. Effect of cigarette smoke on spermatogenesis in rats. Urology Journal. 2007; 4: 159–163.

[27] Prentki Santos E, López-Costa S, Chenlo P, Pugliese MN, Curi S, Ariagno J, et al. Impact of spontaneous smoking cessation on sperm quality: case report. Andrologia. 2011; 43: 431–435.

[28] Chinese expert consensus compilation group for asthenozoospermia diagnosis and treatment, reproductive andrology group, reproductive medicine professional committee of Chinese medical doctor association. Chinese experts’ consensus on the diagnosis and treatment of asthenozoospermia. Chinese Journal of Reproduction and Contraception. 2021; 47: 593–599.

[29] World Health Organization. WHO laboratory manual for the examination and processing of human semen. 5th edn. World Health Organization: Geneva. 2010.

[30] Marcy TW, Skelly J, Shiffman RN, Flynn BS. Facilitating adherence to the tobacco use treatment guideline with computer-mediated decision support systems: physician and clinic office manager perspectives. Preventive Medicine. 2005; 41: 479–487.

[31] Lin M, Ling P, He Q, Chen D, Zheng L, Tang L, et al. Low acrosin activity is associated with decreased Spam1/acrosin expression and GSH deficiency-caused premature acrosome release of human sperm cells. Cell and Tissue Research. 2023; 394: 529–545.

[32] Liu Y, Chen S, Pang D, Zhou J, Xu X, Yang S, et al. Effects of paternal exposure to cigarette smoke on sperm DNA methylation and long-term metabolic syndrome in offspring. Epigenetics & Chromatin. 2022; 15: 3.

[33] Naeimi N, Mohseni Kouchesfehani H, Heidari Z, Mahmoudzadeh-Sagheb H. Effect of smoking on methylation and semen parameters. Environmental and Molecular Mutagenesis. 2024; 65: 76-83.

[34] Amor H, Zeyad A, Hammadeh ME. Tobacco smoking and its impact on the expression level of sperm nuclear protein genes: H2BFWT, TNP1, TNP2, PRM1 and PRM2. Andrologia. 2021; 53: e13964.

[35] Wang H, Liu J, Gao J, Yan W, Rehan VK. Perinatal exposure to nicotine alters sperm RNA profiles in rats. Frontiers in Endocrinology. 2022; 13: 893863.

[36] Dai X, Liang R, Dai M, Li X, Zhao W. Smoking impacts alzheimer's disease progression through oral microbiota modulation. To be published in Molecular Neurobiology. 2024. [Preprint].

[37] Fluhr L, Mor U, Kolodziejczyk AA, Dori-Bachash M, Leshem A, Itav S, et al. Gut microbiota modulates weight gain in mice after discontinued smoke exposure. Nature. 2021; 600: 713–719.

[38] Harrell CR, Djonov V, Volarevic V. The effects of cigarette smoking and nicotine on the therapeutic potential of mesenchymal stem cells. Histology and Histopathology. 2022; 37: 93–100.

[39] Evans DE, To CN, Ashare RL. The role of cognitive control in the self-regulation and reinforcement of smoking behavior. Nicotine & Tobacco Research. 2019; 21: 747–754.

[40] Zhao X, Dichtl FF, Foran HM. Predicting smoking behavior: intention and future self-continuity among Austrians. Psychology, Health & Medicine. 2022; 27: 104–1051.

[41] İçmeli ÖS, Türker H, Gündoğuş B, Çiftci M, Aka Aktürk Ü. Behaviours and opinions of adolescent students on smoking. Tuberk Toraks. 2016; 64: 217–222.

[42] Practice committee of the American society for reproductive medicine. Smoking and infertility: a committee opinion. Fertility and Sterility. 2018; 110: 611–618.

[43] Mills SD, Hao Y, Elliott AM, Wiesen CA. State-level patterns and trends in cigarette smoking across racial and ethnic groups in the United States, 2011–2018. Preventing Chronic Disease. 2021; 18: E44.

[44] Mao HT, Yang WX. Modes of acrosin functioning during fertilization. Gene. 2013; 526: 75–79.

[45] Zhao S, Zhang R, Wang L, Zhao D, Tang L, Rao M. Acrosin activity negatively influences the cumulative live birth rate in patients undergoing IVF treatment. Reproductive Biomedicine Online. 2024; 49: 103993.

[46] Hua R, Xue R, Liu Y, Li Y, Sha X, Li K, et al. ACROSIN deficiency causes total fertilization failure in humans by preventing the sperm from penetrating the zona pellucida. Human Reproduction. 2023; 38: 1213–1223.

[47] Hu YN, Hu L, Yin XY, Zhang H, Peng YQ, Liu G, et al. Sperm acrosin activity may be a useful factor in choosing between ICSI and IVF for infertile male patients. Asian Journal of Andrology. 2024; 26: 85–90.

[48] Zhang G, Yang W, Zou P, Jiang F, Zeng Y, Chen Q, et al. Mitochondrial functionality modifies human sperm acrosin activity, acrosome reaction capability and chromatin integrity. Human Reproduction. 2019; 34: 3–11.

[49] Tofighi Niaki M, Hasan Sheikhha M, Ali Khalili M, Fesahat F, Nabi A, Izadi M, et al. Possible harmful effects of smoking hookah on sperm DNA fragmentation index and protamine genes expression in normozoospermic men. Substance Abuse. 2023; 17: 11782218221144547.

[50] Denlinger-Apte RL, Kotlyar M, Koopmeiners JS, Tidey JW, Luo X, Benowitz NL, et al. Effects of very low nicotine content cigarettes on smoking behavior and biomarkers of exposure in menthol and non-menthol smokers. Nicotine & Tobacco Research. 2019; 21: S63–S72.

[51] Hatsukami DK, Luo X, Jensen JA, al’Absi M, Allen SS, Carmella SG, et al. Effect of Immediate vs gradual reduction in nicotine content of cigarettes on biomarkers of smoke exposure: a randomized clinical trial. JAMA. 2018; 320: 880–891.