Journal of Preventive Medicine

Introduction
Male infertility accounts for 40-50% of all infertility cases in the world, which affects approximately 7% of men. Infertility in men is usually caused by defects in the semen; therefore, the quality of the semen is considered as a criterion for determining the fertility of men. Since 40% of male infertility can be diagnosed pathologically, treatment decisions in developing countries have always been more difficult for men than for women. During the past few decades, the quality of semen and fertility in human societies have decreased significantly, which is rooted in toxic environmental factors. Among these toxic factors, the pollutants in cigarette and hookah smoke have received more attention. One of these pollutants is nicotine, which has the ability to react with some intracellular components such as tubulin protein in the cytoplasm of dividing cells (e.g., germ cells) and, thus, cause disruption in cell division. Other adverse effects of heavy metals on fertility include reduction of sperm count, motility and quality, reduction of egg number and quality, menstrual cycle disorders, low gestational weight, premature birth, and abortion. Excessive use of hookah significantly affects hormonal parameters and quality of semen in varicocele patients compared to people with varicocele without hookah use.
Methods
This is a descriptive-analytical study with cross-sectional design that was conducted in 2019. The study population consists of all men aged 20-45 years who, due to their wife’s fertility problems, referred to Imam Reza Hospital in Bandar Abbas, Iran for semen analysis. Of these, 80 were selected, 40 of whom were regular users of hookah and 40 who had no history of hookah use in the past 6 months (controls). Sampling in both groups was done using a simple random method. The data collection tool was a checklist with 38 items including demographic information, pattern of hookah use, type of used tobacco, complete medical history, the results of laboratory tests and sperm analysis.
Data analysis was done in SPSS software v 24. Data related to quantitative variables were described as Mean±SD and data related to qualitative variables were described as percentage. Using the Kolmogorov-Smirnov test, the assumption of normality of quantitative data distribution was investigated. In case of a normal distribution, parametric independent t-test would be used to compare the parameters between two groups of hookah users and non-users; otherwise, nonparametric Mann-Whitney U test was used.
Results
The mean sperm count in hookah users and non-users was 22±12 and 66±22 million per milliliter, respectively. The t-test results showed that a statistically significant difference in terms of sperm count between the two groups (P<0.001). The mean percentage of motile sperms in hookah non-users and users was 51±7% and 35±10%, while for the immotile sperms, it was 49±0.25% and 64±4%, respectively. Mann-Whitney U test results showed a significant difference between the two groups in this regard (P<0.001). The mean percentage of inactive sperms with progressive motility in hookah non-users and users was 35±6% and 21±6%, and the mean percentage of sperms with progressive motility in these two groups was 10±3% and 6±3%, respectively. The difference was statistically significant (P<0.001). The mean percentage of sperms with normal shape in hookah non-users and users was 49±10 and 34±8%, while the mean percentage of sperms with abnormal shape was 50±7 and 65±4%, respectively. The difference was statistically significant (P<0.001). The Mann-Whitney test showed no significant difference between hookah use and the percentage of giant sperm (P=0.446), round-head sperm (P=0.823), pinhead, shapeless and shrinking sperm (P=0.615). long-tail sperm (P=0.178), and two-tailed sperm (P=0.251).
Discussion
The results of this study showed that the mean volume of semen was not significantly different between hookah users and non-users, while there was a significant difference in sperm count and sperm motility between the two groups. 51% of the sperms in hookah non-users were motile, while in hookah users, only 35% were motile. The mean of inactive sperms without progressive motility was not significantly different between the hookah users and non-users, while the difference in inactive sperms with progressive motility was significant. The mean of sperms with normal shape was different between the two study groups, where the percentage of sperms with normal shape were higher in controls. Due to the effect of hookah use on men’s fertility indicators and its adverse effect on the quality of semen, it can put high treatment cost burden on the society and causes problems such as divorce, depression, and mental and psychological problems, etc.

Ethical Considerations
Compliance with ethical guidelines
Ethical approval was received for this study from the Ethics Committee of the Hormozgan University of Medical Sciences (IR.HUMS.REC.1397.168).

Funding
This project was funded by a research grant from the Hormozgan University of Medical Science.

Authors' contributions
Sharareh Gholamrezadeh: collection of samples, analysis and drafting: Sharareh Gholamrezadeh; Analysis of the results: Sakineh Shokohian; Collaboration in sample preparation and preliminary data analysis: Soghari Falahi; Consultant: Hamidreza Ghaffari; Statistical consulting and data analysis: Amin Qanbaranjad; Author of the article: Sakineh Shekohian, Soghari Falahi and Hamidreza Ghafari.

Conflicts of interest
The authors declared no conflict of interest.

Acknowledgements
The authors are grateful for the financial support of Hormozgan University of Medical Sciences, as well as personnel of Imam Reza hospital and all the participants in this research.


References

1. Stojanov M, Baud D, Greub G, Vulliemoz N. Male infertility: The intracellular bacterial hypothesis. New Microbes New Infec. 2018; 26:37-41. [DOI:10.1016/j.nmni.2018.08.012] [PMID] [PMCID]
2. Chiba K, Enatsu N, Fujisawa M. Management of non-obstructive azoospermia. Reprod Med Biol. 2016; 15(3):165-73. [DOI:10.1007/s12522-016-0234-z] [PMID] [PMCID]
3. Alenzi MJ. Synergetic effect of hookah smoking on varicocele-associated male reproductive impairment in the Saudi community in Al Jouf region, Saudi Arabia. Urol Ann. 2021; 13(3):205-9. [DOI:10.4103/UA.UA_68_20] [PMID] [PMCID]
4. Fainberg J, Kashanian JA. Recent advances in understanding and managing male infertility. F1000Res. 2019; 8. [DOI:10.12688/f1000research.17076.1] [PMID] [PMCID]
5. Farshidi H, Zare S, Khajeh ED, Daryanavard A, Zarenejad M, Dehghan-khalili M. [Investigating the pattern of tobacco consumption in different occupations in Bandar Abbas (Persian)]. Med J Hormozgan Uni. 2013; 11(4):273-8. [Link]
6. Liu JC, Peng RD. The impact of wildfire smoke on compositions of fine particulate matter by ecoregion in the Western US. J Expo Sci Environ Epidemiol. 2019; 29(6):765-76. [DOI:10.1038/s41370-018-0064-7] [PMID]
7. Dai J-B, Wang Z-X, Qiao Z-D. The hazardous effects of tobacco smoking on male fertility. Asian J Androl. 2015; 17(6):954-60. [DOI:10.4103/1008-682X.150847] [PMID] [PMCID]
8. Rahimi-Madiseh M, Mohammadi M, Hassanvand A, Ahmadi R, Shahmohammadi M, Rostamzadeh A. Assessment of the toxicity effects of nicotine on sperm and IVF and the potential protective role of silymarin-an experimental study in mice. Middle East Fertil Soc J. 2020; 25(1):14. [DOI:10.1186/s43043-020-00025-4]
9. Jana K, Samanta PK, De DK. Nicotine diminishes testicular gametogenesis, steroidogenesis, and steroidogenic acute regulatory protein expression in adult albino rats: Possible influence on pituitary gonadotropins and alteration of testicular antioxidant status. Toxicol Sci. 2010; 116(2):647-59. [DOI:10.1093/toxsci/kfq149] [PMID]
10. López-Botella A, Velasco I, Acién M, Sáez-Espinosa P, Todolí-Torró J-L, Sánchez-Romero R, et al. Impact of heavy metals on human male fertility-an overview. Antioxidants. 2021; 10(9):1473. [DOI:10.3390/antiox10091473] [PMID] [PMCID]
11. Lee S, Min J-y, Min K-b. Female infertility associated with blood lead and cadmium levels. Int J Environ Res Public Health. 2020; 17(5):1794. [DOI:10.3390/ijerph17051794] [PMID] [PMCID]
12. Kovac JR, Khanna A, Lipshultz LI. The effects of cigarette smoking on male fertility. Postgrad Med. 2015; 127(3):338-41. [DOI:10.1080/00325481.2015.1015928] [PMID] [PMCID]
13. 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. [DOI:10.3389/fphys.2019.01356] [PMID] [PMCID]
14. Bundhun PK, Janoo G, Bhurtu A, Teeluck AR, Soogund MZS, Pursun M, et al. Tobacco smoking and semen quality in infertile males: A systematic review and meta-analysis. BMC Public Health. 2019; 19(1):36. [DOI:10.1186/s12889-018-6319-3] [PMID] [PMCID]
15. Dhair A, Abed Y. Dose-dependent effect of smoking on fertility status among men in Gaza strip, Palestine. Dubai Med J. 2021; 4(3):190-7. [DOI:10.1159/000517354]
16. Inhorn MC, King L, Nriagu JO, Kobeissi L, Hammoud N, Awwad J, et al. Occupational and environmental exposures to heavy metals: Risk factors for male infertility in Lebanon? Reprod Toxicol. 2008; 25(2):203-12. [DOI:10.1016/j.reprotox.2007.10.011] [PMID]
17. Fallahi S, Rajaei M, Hesam MJ, Koolivand M, Malekzadeh K. The effect of phoenix dactylifera pollen on the expression of NRF2, SOD2, CAT, and GPX4 genes, and sperm parameters of fertile and infertile men: A controlled clinical trial. Int J Reprod Biomed. 2021; 19(6):545-8. [DOI:10.18502/ijrm.v19i6.9376] [PMID] [PMCID]
18. Amann RP, Waberski D. Computer-assisted sperm analysis (CASA): Capabilities and potential developments. Theriogenology. 2014; 81(1):5-17.e1-3. [DOI:10.1016/j.theriogenology.2013.09.004] [PMID]
19. Shaarawy M, Mahmoud KZ. Endocrine profile and semen characteristics in male smokers. Fertil Steril. 1982; 38(2):255-7. [DOI:10.1016/S0015-0282(16)46470-8]
20. Asare-Anane H, Bannison SB, Ofori EK, Ateko RO, Bawah AT, Amanquah SD, et al. Tobacco smoking is associated with decreased semen quality. Reprod Health. 2016; 13(1):90. [DOI:10.1186/s12978-016-0207-z] [PMID] [PMCID]
21. Wang W, Yang X, Liang J, Liao M, Zhang H, Qin X, et al. Cigarette smoking has a positive and independent effect on testosterone levels. Hormones. 2013;12(4):567-77. [DOI:10.14310/horm.2002.1445] [PMID]
22. Carvalho CAF, Favaro W, Padovani C, Cagnon V. Morphometric and ultrastructure features of the ventral prostate of rats (rattus norvegicus) submitted to long-term nicotine treatment. Andrologia. 2006; 38(4):142-51. [DOI:10.1111/j.1439-0272.2006.00728.x] [PMID]
23. Londonkar RL, Srinivasreddy P, Somanathreddy P, Patil SB. Nicotine induced inhibition of the activities of accessory reproductive ducts in male rats. J Ethnopharmacol. 1998; 60(3):215-21. [DOI:10.1016/S0378-8741(97)00148-7]
24. Gaur D, Talekar M, Pathak V. Effect of cigarette smoking on semen quality of infertile men. Singapore Med J. 2007; 48(2):119-23. [PMID]
25. Jenardhanan P, Panneerselvam M, Mathur PP, editors. Effect of environmental contaminants on spermatogenesis. Semin Cell Dev Biol. 2016; 59:126-40. [DOI:10.1016/j.semcdb.2016.03.024] [PMID]
26. Chia S, Ong C, Tsakok F. Effects of cigarette smoking on human semen quality. Arch Androl. 1994; 33(3):163-8. [DOI:10.3109/01485019408987820] [PMID]
27. Meri ZB, Irshid IB, Migdadi M, Irshid AB, Mhanna SA. Does cigarette smoking affect seminal fluid parameters? A comparative study. Oman Med J. 2013; 28(1):12-5. [DOI:10.5001/omj.2013.03] [PMID] [PMCID]
28. Oyeyipo I, Maartens P, Du Plessis S. In vitro effects of nicotine on human spermatozoa. Andrologia. 2014; 46(8):887-92. [DOI:10.1111/and.12169] [PMID]