ABSTRACT
Purpose: The aim of our
study is to determine if smoking hookah has an effect on ovarian reserve by
measuring the serum levels of Anti- Mullerian hormone.
Material and methods: A cross-sectional study was performed at the
fertility clinic at Prince Ali Hospital, in the city of Karak, Jordan. Two hundred healthy women within the 20 to
35 years age range, were chosen from those attending the fertility clinic. AMH
serum levels were checked on one occasion on day 2–4 of the menstrual cycle.
Data was collected from November 2020 to July 2021. The serum levels of AMH of
100 smoking hookah women were compared to the other non-smoking hookah women
and results were analysed by Chi-square and independent samples T-result.
Result: A
total of 200 hundred women were enrolled in the study. The mean age of the
participants was 29 ±0.6 years. The mean
AMH level was (2.29 ± 0.106 ng/mL) in hookah non- smokers compared to (1.5 ±
0.126 ng/mL) in hookah smokers. P values ≤ 0.05 were considered statistically
significant. There is a considerable variation in Anti-Mullerian hormone levels
between smokers and non-smokers.
Conclusion:
Hookah smoking has a significant effect on serum Anti-Mullerian hormone levels.
Key words:
Hookah, ovarian reserve, smoking, anti-Mullerian hormone.
Introduction
A hookah is an ancient waterpipe
tobacco-smoking device. Its first use goes back to the Persian empire, and it
was made by Abu’l-Fath Gilani, a Persian physician of Akbar (1,2). It was
thought that inhaling tobacco smoke through a water pipe would filter the
harmful ingredients. This theory, along with the scents and flavours added to
tobacco, led to the misconception that hookah is a safer alternative compared
to regular cigarette smoking (3). This misleading thought has increased hookah
smoking, not just in the Middle East, but also worldwide (4). So, it is
considered a critical issue.
The detrimental effects of hookah
smoking have been consistently shown in many studies. The harmful effect of
hookah on the cardiovascular system, as well as it being a major risk factor
for certain cancers, is now well established. However, there are few
good-quality studies, if any, which show the negative impact of hookah smoking
on ovarian reserve, measured objectively by serum levels of anti-Müllerian
hormone (5,6).
There is also a strong association
between hookah smoking, and adverse fetal and maternal outcome in pregnant
women, such as growth restriction, preterm labour, and pre-eclampsia (7,8).
AMH, secreted by granulosa cells (9), begins to surge in the male fetus at 7
weeks of gestation. It inhibits development of the Müllerian ducts. In the
female fetus, however, granulosa cells start secreting AMH at 36 weeks of
gestation. In women, it has its peak at between 23 and 25 years old (10). AMH
`1has the best predictive value for assessing ovarian reserve in ageing women.
It is secreted by developing antral follicles, thus reflecting the number of
primordial follicles. This mechanism of secretion makes AMH less fluctuating
throughout the menstrual cycle (11,13). The role of AMH in predicting response
in women undergoing fertility treatment is well established (12,14).
Cigarette smoking has a harmful
effect on fertility and AMH levels (16), shown by several studies. However,
there are scarce data in the literature about the effect of hookah. We found
only one study related to the effect of hookah on AMH (15).
Through this study, we aim to
identify the effect of hookah smoking on fertility, by objectively measuring
the AMH levels in participants.
MATERIALS
AND METHODS
This cross-sectional study was performed at
the fertility clinic at Prince Ali Hospital, in the city of Karak, Jordan. Ethical committee approval was
obtained, as well as informed written consent from participants.
Two hundred healthy women, who met the inclusion criteria of the study, were randomly chosen from those attending the fertility clinic. AMH serum levels were checked on one occasion on day 2 or 3 or 4 of the menstrual cycle, as part of our regular investigations at our infertility clinic.
Inclusion criteria were as follows:
Women with no previous medical history, aged
between 20 and 35 years, presenting to the clinic with primary infertility,
defined by the WHO as inability to achieve pregnancy after 12 months of regular
unprotected sexual intercourse. Hookah smoking, at least once daily for at
least one year.
Inclusion criteria were as follows:
Women with no previous medical history, aged between 20 and 35 years, presenting to the clinic with primary infertility, defined by the WHO as inability to achieve pregnancy after 12 months of regular unprotected sexual intercourse. Hookah smoking, at least once daily for at least one year.
And the exclusion criteria include:
•Any woman with chronic medical illness
•Hormonal imbalances like premature ovarian failure
•Irregular cycle and previous ovarian surgery.
•Smoking conventional cigarettes, in addition to hookah use.
AMH serum levels were determined
and compared between 100 women who met the inclusion criteria and 100
non-hookah users. For all women included in the study, demographics have been
recorded and confirmed from medical records. The study was described to the
patients who were enrolled, and the questionnaire was explained. Confirmation
about patients’ understanding of the study and questionnaire was obtained.
Any patient has the right to withdraw at any
time without affecting their treatment plan. Five cc of blood were collected
and allowed to clot for 30 minutes. After that, centrifugation for 10 minutes
at 4500 cycles per minute was performed before analysis using Cobas 6000 (F.
Hoffmann-La Roche Ltd, Basel,
Switzerland). A total volume of
2–3 cc of serum was used for the analysis. Calibration and measurement of AMH.
levels were done using an Elecsys AMH kit (F. Hoffmann-La Roche Ltd, Basel,
Switzerland).
Statistical analysis:
Pearson’s chi-square test was used to evaluate if there were
differences between different parameters and hookah smoking.Data were analysed using SPSS-22 electronic data analysis software
(IBM, Armonk, NY, USA).Statistical
significance was determined at the 95% confidence interval level.Mean AMH was compared between two groups using a two-tailed t-test
of independent samples.
RESULTS
Two hundred women participated in this study; 100 were hookah
smokers and the other 100 were hookah not users.The mean age for the participating women was 29+ 0. 6 years. The
youngest age for smokers was 23 years, while the oldest was 35 years. The
youngest non-smoker woman was 20 years, and the oldest was 35 years old. Table
III
AMH levels were normally distributed for both groups evident by the
normality statistical tests Kolmogorov-smirnov p= 0.2, which consider a
non-significance (0.2> 0.05).
The mean AMH level was (2.29 ± 0.106 ng/mL) in hookah non- smokers compared to (1.5 ± 0.126 ng/mL) in hookah smokers Table
I. Upon comparing the mean in AMH between smokers and non-smokers,
independent t test revealed a statistically significant difference.t (198)
=4.803, p<0.001). The mean difference between both groups in AMH was 0.79
with 95% confidence interval of 0.47 to 1.11, indicating the hookah smokers has
a lower level of AMH as compared to hookah non-smokers.
The normal AMH levels were between 1.2 and 3.2 ng/ml. Referring to Table
II of the total sample, 59 women had
AMH levels less than 1.2 ng/mL, 44 were from the hookah smoking group and the
remaining 15 were from the non-smoking group.
Also 111 women had AMH levels between 1.2 and 3.2 ng/mL, 65 of them were from
the hookah non- smoking group and the remaining 46 were from the smoking group.
This was considered as a subgroup of the normal AMH range.
Of the total sample of participants, 30 women had AMH levels more
than 3.2 ng/mL, 20 of them were from the hookah non- smoking group and the
remaining 10 were from the smoking group. Table II
A chi square of independence revealed a statistical significant
association between hookah smoking and level of AMH, a low level of AMH was
associated with hookah smokers compared to hookah non-smoking X² (2) =126.480. p< 0.001.
Table I: independent t test result
for mean differences
AMH mean
values
|
N
|
Mean
|
Std. deviation
|
t
|
df
|
P value
|
Non-smoking
|
100
|
2.29
|
1.058
|
4.803
|
198
|
0.000
|
Smoking
|
100
|
1.50
|
1.259
|
|
|
|
Table II: Numbers of women smoking and non-smoking with serum level of AM
|
<
1.2 ng/mL
|
1.2–3.2
ng/mL
|
>
3.2 ng/mL
|
X²
|
df
|
P value
|
Non-smoking
|
15 (15%)
|
65 (65%)
|
20 (20%)
|
126.480
|
3
|
0.000
|
Smoking
|
44 (44%)
|
46 (46%)
|
10 (10%)
|
|
|
|
Observed cases
|
59
|
111
|
30
|
|
|
|
Table III: Mean age for smoker and non-smoker women
Mean age and SD
|
Non smoker
|
smokers
|
29+0.6
|
29+0.8
|
DISCUSSION
Tobacco is a major, direct cause of more than 8 million deaths each
year, according to the WHO (18). There is an
alarming increase in hookah use amongst women, and studies show that the number
of women using hookah exceeds that of men (19,20).
This increase has been attributed, at least partly, to the
misconception that hookah is a ‘safer alternative to conventional cigarette
smoking’ and many women acknowledged their psychological dependence on hookahs
as being addictive to smoking hookah. Studies have constantly shown the harmful
effect of hookah on the general health of women, and wellbeing (21). And
increased risk of premature menopause, reduced bone density, infertility,
ectopic pregnancy, increased infant disease and mortality, intrauterine growth
restriction and increased chromosomal disorders (29)(30).
Smoking cigarettes adversely affects the ovarian reserve of women,
leading to poor response during ovarian stimulation (22), and it elevates
atresia of the follicles (23) so it will lead to early menopause in women who
smoke (24). Furthermore, cigarette is associated with a decline in AMH levels
in reproductive age groups (17)
Hookah smoke contains 82 toxic chemicals and carcinogens (24,25)
such as nicotine, carbon monoxide, tar and heavy metals, and 1 hour of hookah
smoking releases 100 to 200 puffs in comparison to 10 puffs from cigarette
smoking (26,27) so they have greater effect on the reproductive system.(31)
Comparing our results between hookah smokers and hookah non- smokers the average AMH in hookah non- smokers was
2.29 ng/mL but for smokers it was 1.5 ng/mL, showing the decline in AMH in
smokers, as the normal result of AMH was 1.2ng/ml to 3.2ng/ml.
Only 15% of non-smokers had a low AMH level beyond 1.5 ng/ml. In
contrast, to 44% of smokers low AMH less than 1.2 ng/mL, showing the effect of
hookah toxins on AMH. We therefore found a significant reduction of AMH in
hookah smokers, which will affect their fertility and may reduce their
fecundity. Moreover, there is an increased prevalence of infertility around the
world and primary infertility have been reported in 3.6% of tobacco smokers.
(Delpishe et al 2014). Also, tobacco use likely increases infertility by
1.6-fold (32).
We found that hookah smoking
has a direct damaging effect on ovarian reserve, expressed here by the serum
levels of AMH.Although no studies till now addressed the mechanism of how these
changes occurred. However, we only found one study evaluating the effect of
hookah on AMH levels, in which the effect was not statistically significant
(28). And that study had a small sample, and patients were randomly selected
from all clinics, and not specifically the infertility setting.
On the other hand, there is a strong association between hookah
smokers and low semen count and volume and motility, so it has a negative
impact on sperm parameters (33) which contribute to the increase in infertility
issues these days among couples smoking hookah by their negative impact on the
AMH in women and sperm parameters in men.
Limitations
The study did not record
the duration nor the number of hookah smoking sessions. It would be advisable
to understand if the duration of hookah smoking has a greater effect, for
example, on AMH levels.
Further studies with a larger number of participants are
recommended. And a long-term follow-up of participants who quit smoking would
show if the detrimental effect is reversible.
CONCLUSION
In a nutshell, our findings shows that hookah has a negative impact
on serum levels of Anti-Mullerian hormone
REFERENCES
1. The Wealth of India. Council of Scientific & Industrial
Research. 1976. Retrieved 1 August 2007. The smoking of hookah and hubble-bubble started in India during
the reign of the great Moghul emperor, Akbar.
2. Encyclopaedia Iranica. ‘Ḡalyān’. www.iranicaonline.org.
Retrieved 29 May 2019. It
seems, therfore, [sic] that Abu’l-Fatḥ Gīlānī should be credited with the
introduction of the ḡalyān, already in use in Persia, to India.
3. Ehteshami Afshar A, Naghshin R, Amidshahi AA, Fereshtehnejad SM,
Naserbakht M. Evaluation of
the effects of hubble-bubble (waterpipe) smoking on pulmonary function in
patients with respiratory symptoms referred to Hazrat Rasoul and Haft-e-Tir
hospitals in Tehran. Razi Journal of Medical Sciences. 2006;13(52):49–57.
(Persian)
4. Maziak W. The
waterpipe: an emerging global risk for cancer. Cancer Epidemiol 2013;37:1–4.Web
of ScienceGoogle Scholar
5. Ezzati M, Lopez AD.
Estimates of global mortality attributable to smoking in 2000. Lancet.
2003;362:847–852. doi: 10.1016/S0140-6736(03)14338-3 [Crossref]
6. Blank MD, Cobb CO, Kilgalen B, Austin J, Weaver MF, Shihadeh A,
Eissenberg T. Acute effects
of waterpipe tobacco smoking: a double-blind, placebo-control study. Drug and
Alcohol Dependence. 2011;116:102–109. doi: 10.1016/j.drugalcdep.2010.11.026
7. Kayemba-Kay’s S, Ribrault A, Burguet A, Gouyon JB, Riethmuller
D, Menget A, et al.
Maternal smoking during pregnancy and fetal growth. Effects in preterm infants
of gestational age less than 33 weeks. Swiss Medical Weekly. 2010;140:w13139.
doi: 10.4414/smw.2010.13139 [PubMed]
8. Robinson JS, Moore VM, Owens JA, McMillen IC. Origins of fetal growth restriction. European Journal of
Obstetrics & Gynecology and Reproductive Biology. 2000;92:13–19. doi:
S0301211500004218 [pii] [PubMed]
9. Vigier B, Picard JY, Tran D, Legeai L, Josso N. Production of anti-Müllerian hormone: another homology between
Sertoli and granulosa cells. Endocrinology. 1984;114:1315–1320.
10. Rajpert-De Meyts E, Jørgensen N, Graem N, Müller J, Cate RL,
Skakkebaek NE. Expression of
anti-Müllerian hormone during normal and pathological gonadal development:
association with differentiation of Sertoli and granulosa cells. Journal of
Clinical Endocrinology and Metabolism. 1999;84(10):3836–3844.
11. Fanchin R, Taieb J, Lozano DH, Ducot B, Frydman R, Bouyer J. Human Reproduction. 2005 Apr;20(4):923–927.
12. Fanchin R, Mendez Lozano DH, Frydman N, Gougeon A, di Clemente
N, Frydman R, Taieb J. Journal
of Clinical Endocrinology and Metabolism. 2007 May;92(5):1796–1802. [PubMed]
[Ref list]
13. . Dewailly, D., Andersen, C.Y., Balen, A., et al. The physiology and clinical utility of anti-Mullerianhormone in
women. Human Reprod Update, 2014. 20:370–85. doi: 10.1093/humupd/dmt062
14. Freour, T., Masson, D., Mirallie, S., et al. Active smoking compromises IVF outcome and affectsovarian reserve.
Reprod Biomed Online, 2008. 16:96-102.
15. Szkup, M., Jurczak, A., Karakiewicz, B., et al. Inuence of cigarette smoking on hormone and lipidmetabolism in
women in late reproductive stage. Clin Interv Aging, 2018. 13:109–15.
doi:10.2147/CIA.S140487.
16. Gulyas BJ, Mattison DR. Degeneration of mouse oocytes in response to polycyclic aromatic
hydrocarbons. The Anatomical Record. 1979;193:863–882. [PubMed] [Google
Scholar]
17.. Plante, B.J., Cooper, G.S., Baird, D.D., et al. The impact of smoking on antimüllerian hormone levels inwomen aged
38 to 50 years. Menopause, 2010. 17:571-5. doi: 10.1097/gme.0b013e3181c7deba.
18. World Health Organization. Tobacco Key Facts. Geneva, Switzerland: World Health Organization.
2019. https://www.who.int/news-room/fact-sheets/detail/tobacco. Accessed 9 June 2019
19. Shearston JA, Park SH, Lee L, Oshinsky C, Sherman S, Weitzman
M. Increasing
hookah use among adolescent females in the US: analyses from the 2011–2014
National Youth Tobacco Survey (NYTS). Tobacco Prevention & Cessation.
2016;2(September).
20. Nakkash RT, Khalil J, Afifi RA. The rise in narghile (shisha, hookah) waterpipe tobacco smoking: a
qualitative study of perceptions of smokers and non-smokers. BMC Public Health.
2011;11(1):315.
21. Tansaz M, Adhami S, Mokaberinejad R, Namavar Jahromi B, Atarzadeh
F, Jaladat AM. An overview of
the causes and symptoms of male infertility from the perspective of traditional
Persian medicine. Iranian Journal of Obstetrics, Gynecology and Infertility.
2016;18(182):11–17.
22. Hershel Jick,JanePortera , AlanS.Morrisonb RELATION BETWEEN
SMOKING AND AGE OF NATURAL MENOPAUSE: Report from the Boston Collaborative Drug Surveillance Program,
Boston University Medical Center et 1977.
23. Soares SR, Simon C, Remohi J,
Pellicer A.
Cigarette smoking affects uterine receptiveness, Hum Reprod, 2007, vol. 22 (pg.
543-547)
24. Ward KD, et al. The
waterpipe: an emerging epidemic in need of action. Tobacco Control.
2015;24(S1):i1–i2.
25. Sepetdjian E, Shihadeh A, Saliba NA. Measurement of 16 polycyclic aromatic hydrocarbons in narghile
waterpipe tobacco smoke. Food and Chemical Toxicology. 2008;46:1582–1590.
26. World Health Organization. WHO Advisory Note: Waterpipe Tobacco Smoking: Health Effects, Research Needs and
Recommended Actions by Regulators. 2005.
27. American Lung Association. Hookah Smoking: A Growing Threat to Public Health. 2011
28. Soha Albeitawi , Lama Almehaisen, Rawan Obeidat ,Qasem Shehab ,Effect of Hookah (water pipe) smoking on AntiMullerian Hormone
levels,
29. Tansaz M, Adhami S, Mokaberinejad R, Namavar Jahromi B,
Atarzadeh F, Jaladat AM. An
overview of the causes and symptoms of male infertility from the perspective of
traditional persian medicine. Iran J Obstet Gynecol Infertility.
2016;18(182):11–17.
30. Sarokhani M, Veisani Y, Mohamadi A, Delpisheh A, Sayehmiri K,
Direkvand-Moghadam A, et al.
Association between cigarette smoking behavior and infertility in women: a
case-control study. Biomed Res Ther. 2017;4(10):1705–1715. doi:
10.15419/bmrat.v4i10.376.
31. A. R. Cooper, K. H. & Moley. Maternal Tobacco Use and Its Preimplantation Effects on Fertility:
More Reasons to Stop Smoking . Seminars in Reproductive Medicine. 2008; 26(02)
: 204-212
32. E. E. Hatch, R. Troisi, L. A. Wise, M. Hyer, J. R. Palmer, L.
Titus-Ernstoff, R. N. Hoover. Age
at Natural Menopause in Women Exposed to Diethylstilbestrol in Utero . American
Journal of Epidemiology. 2006; 164(7) : 682-688 .
33. Zhang JP, Meng QY, Wang Q, Zhang LJ, Mao YL, Sun ZX. Effect of smoking on semen quality of infertile men in Shandong,
China. Asian J Androl. 2000;2(2):143-146