Reproductive Toxicity of Tobacco Shisha Smoking on Semen Parameters and Hormones Levels among Adult Egyptian Men
Irene A. Fawzy,
Nashwa N. Kamal
Ahlam M. Abdulla
There is limited data about the reproductive toxic effects of shisha smoking. The aim of this study was to investigate the toxic effects of this habit on semen parameters and hormones levels by comparing the results with those of cigarette smokers and non-smokers. Forty-two shisha smokers and 81 healthy nonsmokers participated in this study. Additionally, 65 cigarette smokers were recruited for comparison. Tobacco intoxication was evaluated by determination of blood carboxyhaemoglobin. The results showed that shisha intoxication is more than cigarette as evidenced by the significant increase in COHb level and the significant decrease in the percentage of sperm motility in comparison to non smokers. Both shisha and cigarette smoking significantly lowered semen volume, sperm count and the percentage of sperms with normal morphology. Additionally, they significantly delayed the liquefaction time. Present data revealed that shisha smoking affects semen parameters more than cigarette smoking with significant decrease in percentage of sperms with normal morphology among shisha users. Significant higher levels of testosterone, FSH and LH were found among shisha and cigarette smokers. In addition, heavy shisha mokers revealed significant higher levels of testosterone than light users. There was statistically significant negative correlation between the smoking index and semen volume and the sperm count and a significant positive correlation between the smoking index and the testosterone levels. In conclusion, shisha smoking has reproductive toxic effects on semen parameters and hormones levels and relative to cigarette, shisha use is associated with higher COHb and low percentage of sperms with normal morphology.
August 09, 2011; Accepted: November 17, 2011;
Published: December 24, 2011
There is limited data about the reproductive toxic effects of shisha smoking.
However, all stages of reproductive functions may be affected by cigarette smoke
toxicants (Blank et al., 2011). Smoking is a
major public health problem. Globally, more than 5 million deaths each year
are attributed to tobacco use and this may increase to 10 million within the
next 20-30 years (WHO, 2009). Tobacco is commonly consumed
in different ways including cigarette, pipe, cigar and waterpipe smoking. Waterpipe
tobacco smoking usually involves heating flavored tobacco with charcoal and
inhaling the resulting smoke after it has passed through water (Blank
et al., 2011). Research demonstrates that numerous toxic agents,
including carcinogens, heavy metals, other particulate matter and nicotine are
efficiently delivered through waterpipes (Martinasek
et al., 2011). Waterpipes have different names depending on the geographic
region of use. Names include shisha or goza (Egypt and
Saudi Arabia), narghile, nargile or arghile (Jordan,
Lebanon and Syria), hookah (Africa and the Indian subcontinent) and hubble
bubble (in many regions) (Wolfram et al., 2003).
The prevalence of waterpipe (narghile, gosa, shisha, hookah) tobacco smoking
(WTS) in the Middle East region and worldwide is increasing (Maziak,
2008). Youth WTS is on the rise as compared to cigarette smoking. Waterpipe
smoking is also increasing in Egypt with a progressively wider distribution
of cafés attracting new customers (Jha and Chaloupka,
2000). Tobacco used for gosa smoking known as Maassel, as a
proper transliteration, meaning honeyed in Arabic. Maassel contains
about 30% tobacco and up to 70% honey or molasses/sugar cane, in addition to
glycerol and flavoring essences. The uptake of tobacco nicotine in shisha is
equivalent to 2-12 cigarettes per portion of tobacco used (hagar). However,
it is known that waterpipe smoking produces more smoke than cigarette smoking
and it has been estimated that smoke exposure could be as much as 100-200 cigarettes
per session. Therefore, the types and magnitudes of health hazards of waterpipe
smoking are likely to be higher than those of cigarette smoking (WHO,
Shisha smoke has been found to contain high concentrations of carbon monoxide
(CO), nicotine, tar and heavy metals (Knishkowy
and Amitai, 2005; Shafagoj et al., 2002;
Shihadeh, 2003). Also, commonly used heat sources like
charcoal or wood cinders may increase health risks because they produce toxicants
as CO, metals and carcinogens (Shihadeh, 2003; Shihadeh
and Salehm, 2005).
One reason for the global spread of waterpipe tobacco smoking may be due to
the belief that waterpipes are less risky than cigarettes (Aljarrah
et al., 2009). This belief seemingly is contradicted by demonstrations
that various constituents of waterpipe smoke are known to cause cancer (e.g.,
Polycyclic Aromatic Hydrocarbons [PAH]; Sepetdjian et
al., 2008) lung disease (e.g., volatile aldehydes; Al
Rashidi et al., 2008) cardiovascular disease (e.g., carbon monoxide
[CO] Shihadeh and Salehm, 2005) and also dependence
(i.e., nicotine; Shihadeh, 2003). At least some of these
smoke toxicants have been found in waterpipe tobacco smokers during smoking,
including nicotine and CO (El-Nachef and Hammond, 2008).
Among different air pollutants, cigarette smoke contains toxic chemicals, mutagenic
and carcinogenic compounds, which can adversely affect male fertility (Zenzes,
2000; Martinet and Bohadana, 2004). Cigarette smoke
is made up of gas and organic compounds. One of the most abundant organic particles
in cigarette smoke is nicotine, which is responsible for some positive or negative
effects on the various organs. Also, cigarette smoke contains a mixture of harmful
components such as carbon monoxide (CO), hydrogen cyanide (HCN), ammonia, volatile
hydro carbons, Alcohol, aldehydes and ketones (Jorsaraei
et al., 2008).
The effect of smoking on male reproduction has been studied where semen quality
was investigated in many cross-sectional studies including infertile patients
with conflicting results (Mostafa, 2010). Although,
the reproductive toxicity associated with cigarette smoking has been extensively
investigated, studies evaluating such toxicity in shisha users are still lacking.
So, this study was carried out to investigate the toxic effects of waterpipe
(gosa) tobacco smoking on semen parameters and hormones levels and correlate
the results with those of cigarette smokers and non-smokers.
MATERIALS AND METHODS
A cross sectional study was performed on 42 shisha smoker and 65 cigarette
smoker subjects. As a control, 81 nonsmoking subjects were selected to match
cigarette and shisha smokers for age and geographical area. All subjects were
recruited from adult males undergoing screening for marriage at the Andrology
Clinic, El Raey El saleh samalout Hospital at the period from 15th of January
2011 to 15th of June 2011. All the subjects gave informed consent to participate
in the study in accordance with the ethical standards approved by the committee
of Minia University.
Selection criteria: All subjects were healthy adult males, shisha smokers
were those who use only shisha to smoke tobacco and cigarette smokers were those
who use only cigarettes to smoke tobacco for at least 3 years. Shisha smokers
(42 subjects) were into three groups (a) heavy group (Who use shisha daily),
(b) medium group (Who use shisha in 4-5 days/week) and (c) light group (Who
use shisha in <3 days/week). Shisha smokers included in this study were habitual
shisha smokers for at least 3 years and they smoked an average of 20 g Maassel
which is generally used in the shisha bowl per session for a period of 45 min
(Bacha et al., 2007; Shafagoj
et al., 2002).
Exclusion criteria: Those who smoke other type of tobacco products,
for example, cigar, pipe or those who smoked both cigarettes and shisha at same
time. Also, those who were using other habitual substances or those with history
of orchitis, testicular trauma, sexually transmitted disease, varicocele, inguinal
hernia operation and cryptorchism.
Smoking index: Number of cigarettes per day X period of smoking of cigarette smokers was calculated.
Semen analysis: A total of 188 semen specimens from 42 gosa smokers,
65 cigarette smokers and 81 nonsmokers fulfilled the selection criteria were
obtained via masturbation. The semen samples were collected in sterile plastic
containers and allowed to liquefy for 30 min. Thereafter, samples were analysed
within 2 h after collection (Kunzle et al., 2003)
according to WHO (1992) criteria. Semen volume, pH and the
time to liquefaction were measured. The percentage of morphologically normal
sperm, Sperm concentration (count) and sperm motility were determined.
Hormone analysis: Blood samples (5 mL) were obtained at 8:00-10:00 a.m. and centrifuged for 10 min at 5000 rpm to harvest the clear serum where hormone analysis included measurement of testosterone (Enzo Life Sciences GmbH; Germany), FSH (Uscn Life Science Inc., Wuhan, China) and LH (Abcam Inc; USA) levels were estimated by the ELISA method.
Determination of blood carboxyhaemoglobin (COHb): Blood COHb level was
determined using Blood Gas Analyzer; Bayer 855.
Statistical analysis: The Statistical Program SPSS for Windows version 11 was used for data entry and analysis (SPSS Inc., Chicago, IL, USA). Men were grouped into cigarette smokers, shisha smokers and non-smokers. A descriptive analysis of the data was performed and the variables were further analyzed with at-test and analysis of variance (ANOVA) multiple comparisons of shisha smokers with light, medium and heavy groups were done using ANOVA. Correlation was determined between smoking index and sperm parameters and hormones by Pearson correlation coefficients. Statistical significance was determined at the 95% confidence interval level.
A total of 42 shisha smokers (mean age 25.9±5.4 years) 65 cigarette
smokers (mean age 26.5±64 years) and 81 strict non-smokers (mean age
26.4±5.84 years) who fullfiled the selection criteria were included in
this study. The age of patients was not significantly different in all groups
Based on their detailed shisa smoking history, the shisha smokers (n = 42) were
divided into 3 groups as shown in Table 2 according to the
number of sessions per week.
Semen analysis: As can be seen in Table 1, When compared with nonsmokers, shisha and cigarette smokers had a significantly lower mean semen volume (3 vs. 3.8 mL, 3.05 vs. 3.8 mL, respectively F = 29.2, p = 0.001) a significantly lower mean sperm count (34 vs. 59 M mL-1 for shisha smokers and 43 vs. 59 M mL-1 for cigarette smokers, F = 5.7, p = 0.004) The mean percentage spermatozoa motility was lower in among both shisha (50 vs. 57%) and cigarette (54 vs. 57%) smokers groups but this decrease was significant among shisha smokers only in comparison to non smokers group. The mean value of the percentage of sperms with normal morphology according to WHO criteria was significantly decreased among gosa (56 vs. 70%) and cigarette(61 vs. 70% ) smokers compared to the non smokers group (F = 15.6, p = 0.001). The mean pH of ejaculate from shisha and cigarette smokers were significantly higher than that of ejaculate from nonsmokers(7.9 vs. 7.6, 7.8 vs. 7.6, respectively F = 27.8, p = 0.001). Gosa and cigarette smokers had a significantly delayed mean liquefaction time (24 min and 23 min, respectively) vs. 21 min in non smokers (F = 15.04, p = 0.001). There were no statistically significant differences in semen parameters between men smoking cigarettes or shisha except in the percentage of sperms with normal morphology (p<0.05).
|| Semen and hormone analysis results among the studied groups
(values are Mean±SD)
|ap<0.05 vs. the corresponding values of the
cigarette smokers and Non-smokers (control), bp<0.05 vs. the
corresponding values of the Shisha smokers and non-smokers controls and
cp<0.05 vs. the corresponding values of the cigarette smokers
and Shisha smokers
|| Semen and hormone analysis results among the Shisha smoker
groups (values are Mean±SD)
|Group 1: Light shisha users, group 2: Medium shisha users,
group 3: Heavy shisha users, ap<0.05 vs. the corresponding
values of the group 1 and group 2, bp<0.05 vs. the corresponding
values of the group 1 and group 3 and cp<0.05 vs. the corresponding
values of the group 1 and non-smoker group, dp<0.05 vs. the
corresponding values of the group 2 and group 3, ep<0.05 vs.
the corresponding values of the group 2 and non-smoker group and fp<0.05
vs. the corresponding values of the group 3 and non-smoker group
As shown in Table 2, there were significant differences in
semen volume, PH, liquefaction time and the percentage of sperms with normal
morphology between the non smokers group and each of the 3 shisha groups (p
= 0.001). In addition there were significant differences in semen volume and
sperm count between the light and heavy shisha groups (p<0.05) and between
the medium shisha smokers group and the non smokers group in the percentage
of the sperm motility (p<0.05). The mean of smoking index of cigarette smokers'
group was 70.46±32.7. There was negative correlation between the smoking
index and all semen parameters except the liquefaction time which showed positive
correlation with it. The negative correlation was statistically significant
between the smoking index and semen volume (r = -0. 24; p<0.05) and the sperm
count (r = -0.41; p<0.01). Correlations with other semen parameters were
not significant (Table 3).
Hormones levels: Compared with non smokers in Table 1, shisha and cigarette smokers showed a significantly higher mean levels of testosterone (4.7 vs. 4.45 ng mL-1, 4.6 vs. 4.45 ng mL-1, respectively F = 28.2, p = 0.001), LH (3.5 vs. 3.3 mIU mL-1, 3.47 vs. 3.3 mIU mL-1, F = 5.1, p = 0.007) and FSH hormones (3.7 vs. 3.3 mIU mL-1, 3.6 vs. 3.6 mIU mL-1, F = 17.05, p = 0.001).
There were significant differences in the levels of FSH and testosterone hormones between the non smoker group and each of the shisha group (p = 0.001). Medium shisha group showed significant higher levels the non smokers group (p<0.05). Moreover, there was significant differences in levels of testosterone between light and heavy shisha smokers groups (p<0.05) (Table 2).
Table 3 showed positive correlation between the smoking index
and all hormones levels and this correlation was statistically significant with
the testosterone levels (r = 0.27, p<0.05).
Blood COHb level: The mean COHb as shown in Table 4 was 0.93% for non smokers, 1.06 and 1.7% for cigarette and shisha smokers, respectively. It was shown a significant higher level of COHb among both cigarette and shisha smokers compared to non smokers (p<0.001). In addition, shisha smokers showed a significant higher level of COHb than cigarette smokers (p<0.05).
|| Pearson's correlation coefficients between smoking index
and semen parameters and hormones levels in smokers
|*Significant correlation (p <0.05), **Significant correlation
|| Carboxyl Hb levels among the studied groups (values are Mean±SD)
|ap<0.05 vs. the corresponding values of the
cigarette smokers and Non-smokers (control), bp<0.05 vs. the
corresponding values of the Gosa smokers and non-smokers controls and cp<0.05
vs. the corresponding values of the cigarette smokers and Gosa smokers
Shisha smokes likely contains an abundance of several of the toxicants that
are thought to render shisha users more prone to health risks and addiction
(Shihadeh and Salehm, 2005).
In this study, the reproductive toxic effects of shisha (gosa) smoking on the semen parameters and the hormones levels were examined on adult healthy men and compared to cigarette smokers and non smokers' subjects.
In the current study, relative to cigarette users, waterpipe users showed significant
greater COHb level. This is in accordance with (Eissenberg
and Shihadeh, 2009) who revealed that peak waterpipe COHb levels were three
times higher than those for the cigarette. In the same line, Theron
et al. (2010) observed that water-pipesmoker shad significantly higher
increases in blood COHb levels than cigarette smokers.
The present study found that in comparison to non smokers, shisha smokers caused
a significant lowering in the percentage of sperm motility and both shisha and
cigarette smokers showed a significant decrease in semen volume, sperm count,
percentage of sperms with normal morphology, a significant delaying of time
of liquefaction and a significant increase in semen pH. Studies evaluating such
toxicity in shisha users are still lacking. However, there are many debates
regarding the toxic effects of cigarette smoke on human reproduction (Vine
et al., 1996). In agreement to our results, different articles have
demonstrated a negative impact of smoking on human semen parameters (Evans
et al., 1981; EL Mulla et al., 1995)
such as concentration (Handelsman et al., 1984;
Lewin et al., 1991), motility (Handelsman
et al., 1984; Shaarawy and Mahmoud, 1982)
and normal morphology (Shaarawy and Mahmoud, 1982; Evans
et al., 1981). Also, Zhang et al. (2000)
showed that the semen volume was much lower in heavy and long-term smokers than
in nonsmokers and there were modifications in semen pH, sperm concentration,
motility and morphology. Present data revealed that shisha smoking affects the
semen parameters more than cigarette smoking although the difference was not
statistically significant except in lowering the percentage of sperms with normal
morphology. On the other hand, the semen volume and the sperm count was significantly
lower in the heavy shisha smokers group than mild users which indicates that
toxic effects of tobacco in shisha increases with increasing the number of smoking
The mechanism for the potentiated toxicity of shisha smoking on semen parameters
compared with that of regular cigarettes is unknown. In general, tobacco and
charcoal might contribute to the toxicity observed in semen quality of shisha
users, since the toxicity of shisha smoking on semen parameters may be attributed
to the high levels of nicotine which are efficiently delivered through shisha.
Nicotine is a very toxic alkaloid (Branian and Hansen, 2002)
and it has a significant influence on sperm count and sperm morphology (Gornig
and Schirren, 1996). Nicotine and its major metabolites, cotinine and trans-3-hydroxycotinine
have been implicated to mediate the effects of smoking on sperm parameters as
these toxic substances cross the blood-testis barrier (Pacifici
et al., 1993; Vine et al., 1996).
So, the seminal plasma of smokers can be considered as a toxic environment for
spermatozoa (Sepaniaka et al., 2006). Also, toxins
in cigarette smoke reach the male reproductive system and their effects are
mainly due to their direct interaction with seminal fluid components and the
accessory glands, which contribute their secretions to the seminal fluid, leading
to reduce its seminal volume and delayed in the liquefaction time (Gaur
et al., 2007).
Shisha smoke has been shown to contain more concentrated and diverse toxic
compounds compared with cigarette smoke (Shihadeh and Salehm,
2005). Studies on the mainstream smoke aerosol of the shisha showed that
the tar (volatile aldehydes) of a single smoking session is startlingly
high, two order of magnitude greater than that produced from smoking a single
cigarette (Al Rashidi et al., 2008). In addition,
CO exposure is greater in shisha smoking compared with cigarette smoking (Bacha
et al., 2007; Eissenberg and Shihadeh, 2009;
Maziak et al., 2009). Furthermore, the quantities
of 3- or 4-ring compounds of Polycyclic Aromatic Hydrocarbon (PAH) in shisha
smoke are many times more than that of cigarette smoke (Shihadeh
et al., 2004; Shihadeh and Salehm, 2005;
Monzer et al., 2008; Sepetdjian
et al., 2008). Recently, it has been found that the levels of carboxyhemoglobin
after shisha smoking are approximately triple when compared with those obtained
after cigarette smoking (Eissenberg and Shihadeh, 2009).
Also, the style of shisha smoking results in a dramatically higher exposure
volume to smoke, more tobacco consumption per smoking event and a longer smoke
inhalation period (Bacha et al., 2007; Eissenberg
and Shihadeh, 2009; Cobb et al., 2010). Shisha
smoke has been reported to increase the amount of free radicals in the bodies
of smokers (Sharma et al., 1997). Free radicals
can cause oxidative DNA damage and chromosomal damage (Salmon
et al., 2004).
One of the constituents of massel used in shisha is heavy metals where Al-Attar
(2011) mentioned that the toxicity of heavy metals caused alteration in
sperm morphology, count, motility as well as hormones (Chowdhury,
1992). Also, Salem et al. (1990) revealed higher
levels of lead in the water (in water pipes) after smoking which causes a decrease
of sperm motility in men most likely due to increased lipid peroxidation (Kasperczyk
et al., 2008).
The lower values for sperm motility in smokers may be also caused by disturbances
in spermatogenesis or epididymal sperm maturation process secondary to secretory
dysfunction at the level of the Leydig and Sertoli cells. Epididymal dysfunction
in smokers will likely have detrimental effects on the various cytb structural
modifications and biochemical change that spermatozoa normally undergo during
epididymal maturation and may lead to decrease in sperm motility and sperm fertilizing
capacity (Sofikitis et al., 1995).
Contradict to our study, Some researches could not find a relationship between
cigarette smoking and seminal quality (Dikshit et al.,
1987; Trummer et al., 2002; Baldelli
et al., 2002) found no deleterious effect of cigarette smoking on
semen quality except for a non-significant trend toward decreased ejaculate
volume. This could be explained as their studies were performed on a different
number of samples than our study.
The current study revealed a significant higher levels of testosterone, FSH
and LH hormones among both shisha and cigarette smokers than in non smokers.
This is in agreement with Trummer et al. (2002),
Vogt et al. (1986), Field
et al. (1994). These results could be explained as smoking has an
effect on the various metabolic and biological processes in the body including
secretion of hormones. These are mediated chiefly through behavioral and pharmacological
actions of nicotine but also occur as a result of increases in the physical
effects of stress on the body caused by smoking. Also, the significantly elevated
LH in smokers suggests a central activation of Leydig cells, which explains
elevated testosterone (Rahman et al., 2011).
Our data is against Sofikitis et al. (1995)
and Pasqualotto et al. (2006) who reported that,
there were no significant differences in the serum levels of follicle-stimulating
hormone, luteinizing hormone and testosterone between smokers and nonsmokers
and Ochedalski et al. (1994) who reported that
the mean levels of LH and FSH were lower among smokers compared with non-smokers,
while the mean levels of testosterone did not differ. A possible explanation
is that smoking may, over time lead to a degeneration of Leydig cells (Rahman
et al., 2011).
In conclusion, Shisha intoxication is more than cigarette as evidenced by the
significant increase in COHb level among shisha smokers than cigarette smoking.
Also, shisha tobacco smoking has deleterious effects on male fertility as it
has significant toxic effects on semen parameters and levels of testosterone,
FSH and LH hormones and this toxicity is higher than that induced by cigarette
smoking with significant decrease in the percentage of sperms with normal morphology
among shisha smokers than cigarette smokers. Therefore, shisha smoking seems
to induce more toxic effects and the results of the current study highlight
the fact that smoking via shisha is not a safer alternative to smoking cigarettes.
Also, heavy shisha smokers showed a significant decrease in semen volume and
sperm count than the light group. In addition our study concluded statistically
significant negative correlations between smoking index and the semen volume
and sperm count as well as a significant positive correlation between it and
the testosterone level. So, this correlation placed special emphasis on the
negative impact of smoking on semen quality and level of testosterone. Thus,
it is recommended that men who have a habit of shisha smoking as an alternative
to cigarette smoking tobacco should be informed about the potential adverse
effects of their habit on sperm quality and hormones levels to stop it.
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