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R E S E A R C H A R T I C L E Open Access
Tobacco smoking and semen quality in
infertile males: a systematic review and
meta-analysis
Pravesh Kumar Bundhun
1
, Girish Janoo
2
, Akash Bhurtu
2
, Abhishek Rishikesh Teeluck
2
,
Mohammad Zafooruddin Sani Soogund
2
, Manish Pursun
2
and Feng Huang
3*
Abstract
Background: Nowadays, the total number of couples visiting an infertility clinic is on the rise. Tobacco smoking is
considered one of the major factors leading to male infertility. In this study, we aimed to systematically investigate
the impact of tobacco smoking on semen quality in infertile male participants.
Methods: Online databases (Cochrane Central database of Randomized Controlled Trials and the databases of
MEDLINE and EMBASE respectively) were searched for relevant English publications that satisfied the inclusion and
exclusion criteria of this analysis. The clinical endpoints which were assessed included semen parameters (oligozoospermia,
asthenozoospermia, teratozoospermia, and azoospermia), morphological defects of spermatozoa and the hormones
involved in reproduction. RevMan 5.3 software was used to analyze the data whereby mean difference (MD) and risk ratios
(RR) with 95% confidence intervals (CI) were generated to represent the results.
Results: Sixteen studies with a total number of 10,823 infertile male participants (5257 smokers and 5566 non-smokers)
were included. Results of this analysis showed oligozoospermia to be significantly higher in smokers (RR: 1.29, 95% CI: 1.05–
1.59; P= 0.02). Morphological defect of spermatozoa (MD: 2.44, 95% CI: 0.99–3.89; P= 0.001) was also significantly higher in
smokers whereby significant head (MD: 1.76, 95% CI: 0.32–3.20; P = 0.02), neck (MD: 1.97, 95% CI: 0.75–3.18; P=0.002)and
tail (MD: 1.29, 95% CI: 0.35–2.22; P= 0.007) defects were observed. However, smoking did not affected the pH (MD: 0.04,
95% CI: [−0.03–0.11]; P= 0.30) and motility (RR: 1.42, 95% CI: 0.97–2.09; P= 0.07) of spermatozoa. Additionally, tobacco
smoking did not cause any dis-balance in hormones which were involved in reproduction.
Conclusions: In conclusion, with reference to the clinical endpoints which were studied in this analysis, tobacco smoking
was associated with a lower sperm count and an increase in the number of morphological defects of spermatozoa.
However, the pH and motility of spermatozoa as well as the production of hormones which were involved in reproduction
were not affected in this population of infertile males.
Keywords: Smoking, Infertile men, Semen, Oligozoospermia, Asthenozoospermia, Teratozoospermia, Azoospermia
Background
Tobacco smoking among the young generation is becom-
ing worse day by day [1]. The effect of tobacco smoking
on lung cancer is already well-known [2]. However, other
serious health hazards of smoking have not often well
been investigated [3]. Not lately, there has been evidence
showing tobacco smoking to have shocking impact on
reproductive health irrespective of gender status.
Nowadays, the total number of couples visiting an infer-
tility clinic is on the rise [4]. According to the American
Society for Reproductive Medicine, infertility is defined as
the inability to achieve pregnancy after a duration period
of one year of regular, unprotected sexual intercourse [5].
Tobacco smoking is considered one of the major fac-
tors leading to male infertility [6] and recent surveys
have demonstrated approximately 120, 000 young men
* Correspondence: huangfeng7925@163.com
3
Institute of Cardiovascular Diseases and Guangxi Key Laboratory Base of
Precision Medicine in Cardio-cerebrovascular Disease Control and Prevention
and Guangxi Clinical Research Center for Cardio-cerebrovascular Diseases,
the First Affiliated Hospital of Guangxi Medical University, Nanning 530021,
Guangxi, China
Full list of author information is available at the end of the article
© The Author(s). 2019 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0
International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and
reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to
the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver
(http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Bundhun et al. BMC Public Health (2019) 19:36
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(30 to 50 years old) in the United Kingdom to be impo-
tent due to this bad habit. Male infertility (approximately
50% of the cases of infertility among couples [7]) is grad-
ually leading to depression and other psychological out-
comes, and this might be potential signs of serious
future consequences.
The impact of tobacco smoking on semen quality has sel-
dom been systematically studied. Therefore, by comparing
semen parameters between smokers and non-smokers, we
aimed to systematically investigate the impact of tobacco
smoking on semen quality in infertile male participants.
Methods
Electronic databases and searched strategies
An electronic search was carried out for English language
publications through the Cochrane Central database of
Randomized Controlled Trials, the databases of MED-
LINE (Medical-related publications) and EMBASE re-
spectively. The terms ‘smoking and infertility’,‘smoking
and male infertility’,‘smoking and semen’,‘smoking and
sperm’,‘smoking and young males’,‘infertility and tobacco
smoking’,‘smoking and male health’,‘smoking, males and
impotence’,‘smoking and infertile men’,‘smoking and
sperm morphology’,‘smoking and sex’,‘smoking and sperm
count’,‘smoking and testosterone’,‘smoking and LH’,‘smok-
ing and FSH’,‘smoking and prolactin’and ‘smoking and
sperm motility’were used to find relevant publications.
To improve this search process, the terms ‘males,
men, cigarettes, nicotine, tobacco and non-fertile’were
also included one at a time during the search process. In
addition, reference lists of suitable articles were also
reviewed for relevant publications.
Inclusion criteria
Inclusion criteria were based on the following features:
(a) Studies based strictly on infertile male participants;
(b) Studies that compared respective semen parameters
in smokers versus non-smokers;
(c) Studies that reported the following endpoints:
semen parameters, pH of semen, morphological
defects of spermatozoa, types of abnormal
structural defects, and hormones which were
involved in the functioning of the male
reproductive system.
Exclusion criteria
Exclusion criteria were based on the following features:
(a) Studies that consisted of fertile/normal male
participants;
(b) Studies that did not compare respective semen
parameters in smokers versus non-smokers;
(c) Studies that did not report the above-mentioned
endpoints;
(d) Duplicated studies.
Endpoints
Selective endpoints included:
–Oligozoospermia;
–Asthenozoospermia;
–Teratozoospermia;
–Azoospermia;
–Morphological defects of spermatozoa: head, neck or
tail defects;
–pH of semen;
–Testosterone level;
–Follicle stimulating hormone (FSH) level;
–Luteinizing hormone (LH) level;
–Prolactin level.
The endpoints have been listed in Table 1.
Table 1 Reported endpoints
Study Selective endpoints reported
Al-Turki2014
10
pH of semen, testosterone level, FSH level, LH level,
prolactin level
Al-Turki2016
11
Serum testosterone, semen pH
Anifandis2014
12
Sperm immotility
Caserta2012
13
Oligozoospermia, asthenozoospermia, teratozoospermia,
FSH level, LH level
Cui2016
14
Abnormal sperm head, abnormal sperm body,
abnormal sperm tail
Gaur2007
15
Oligozoospermia, asthenozoospermia, teratozoospermia
Meri2013
16
Serum pH
Mitra2012
17
Asthenozoospermia (reduced motility), oligozoospermia
(low sperm count), teratozoospermia (sperm with
abnormal morphology), azoospermia (no sperm count),
immotility, sperm head defect, sperm tail defect
Trummer2002
18
Asthenozoospermia, oligozoospermia, teratozoospermia,
azoospermia, testosterone, FSH level, LH level, prolactin
level
Mostafa2006
19
Amorphous sperm head, pathological sperm midpiece,
pathological sperm tails
Osser1992
20
Amorphous sperm head, pathological sperm midpiece,
pathological sperm tails
Yu2013
21
Sperm immotility
Zhang2013
22
Semen pH, sperm head defects, sperm neck defect,
sperm tail defect
Zhang2015
23
FSH level, LH level, testosterone level
Dikshit1987
24
Immotility of sperms and abnormal morphology
Kunzle2003
25
pH, immotility of sperms and abnormal morphology
Abbreviations: FSH follicle stimulating hormones, LH luteinizing hormone
Bundhun et al. BMC Public Health (2019) 19:36 Page 2 of 11
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Data extraction and review
The search of studies was carried out with reference to
the PRISMA guideline [8]. Six authors (PKB, GJ, AB,
ART, MZSS and MP) independently reviewed the arti-
cles which were considered relevant to this analysis and
data were extracted appropriately. The authors’names,
year of publication, the study design, the endpoints
which were reported, the total number of smokers and
non-smokers respectively, age of patients, and the total
number of events which were reported in each study
were carefully extracted.
Any disagreement which was raised was spontaneously
resolved by the seventh author (FH).
With the exception of the mean age of the partici-
pants, other data at baseline were not included in this
analysis for two main reasons:
–Many original studies did not include risk factors
and co-morbidities at baseline;
–Baseline features which were reported in certain
studies were different from those reported in other
studies and a comparison would not have been
possible.
Statistical analysis
The latest version of RevMan software (5.3) was used to
analyze the data. This analysis involved both continuous
and dichotomous data. Mean and standard deviation
(SD) were used during subgroup analysis whereby
pooled mean difference (MD) was calculated for the
continuous data. For dichotomous data, risk ratios (RR)
and 95% confidence intervals (CI) were generated to
represent the results.
The statistic Q test and statistic I
2
test were used to
evaluate heterogeneity [9]. During the subgroup analysis,
statistical significance was set at a Pvalue ≤0.05. A fixed
effects model (I
2
< 50%) or a random effects model (I
2
>
50%) was used based upon the I
2
value which was ob-
tained during each subgroup analysis.
Each study was excluded one by one and a new ana-
lysis was carried out each time to observe any significant
difference compared to the main results which were ob-
tained (sensitivity analysis).
Ethical approval or board review approval was not re-
quired for this type of research articles.
Results
Search outcomes
Electronic search resulted in a total number of 342 arti-
cles. After a proper assessment of the titles and ab-
stracts, we excluded 285 studies. Fifty-seven (57)
full-text articles were assessed for eligibility. Among the
full-text articles, further studies were eliminated
because:
–They included fertile/normal male participants (8);
–They involved infertile couples without specifying
the gender (3);
–They reported endpoints which were not considered
relevant specifically for this analysis (9);
–They were duplicated studies (21).
Finally, 16 studies [10–25] which satisfied all the inclu-
sion and exclusion criteria of this research were included
in this analysis (Fig. 1).
Basic features of the studies which were included in this
analysis
A total number of 10,823 infertile male participants
(5257 smokers and 5566 non-smokers) were included in
this analysis.
The main features of the original studies have been
summarized in Table 2.
The study design, the participants’enrollment time pe-
riods (1985–2015), the mean age (26.5–40.5 years old),
and the total number of smokers (5257 participants) and
non-smokers (5566 participants) have been listed in
Table 2.
Other characteristics of the participants and the rea-
sons for exclusion have been summarized in Table 3.
Majority of the patients did not consume alcohol and
the minority who consumed alcohol were only moderate
consumers. Participants with varicocele, cryptorchidism,
aspermia, chronic diseases, genital infections, genital
trauma, chromosomal abnormalities were excluded from
this analysis (Table 3).
Oligozoospermia and teratozoospermia
Results of this analysis showed oligozoospermia to be
significantly higher in smokers (RR: 1.29, 95% CI: 1.05–
1.59; P= 0.02) whereas teratozoospermia was not signifi-
cantly different (RR: 1.22, 95% CI: 0.96–1.56; P= 0.10)
between the smokers and the non-smokers as illustrated
in Fig. 2.
Asthenozoospermia and azoospermia
Asthenozoospermia (RR: 1.42, 95% CI: 0.97–2.09; P=
0.07) and azoospermia (RR: 3.02, 95% CI: 0.23–40.01; P
= 0.40) were not significantly different between the
smokers and non-smokers (Fig. 3).
Impaired motility of spermatozoa and pH of semen
(continuous data)
The motility of sperms was not impaired between the
smokers and non-smokers (MD: 1.26, 95% CI: [−0.64–
3.17]; P= 0.19). In addition, pH of semen was also simi-
larly observed (MD: 0.04, 95% CI: [−0.03–0.11]; P=
0.30) [Fig. 4].
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Table 2 General features of the studies
Studies Study design Year of patients’enrollment No of infertile smokers (n) No of infertile non-smokers (n) Age (years) S/NS
Al-Turki2014 Retrospective 2010–2012 90 168 34.2/34.1
Al-Turki2016 Retrospective 2008–2013 194 322 34.6/34.3
Anifandis2014 Prospective –33 98 37.9/37.1
Caserta2012 Cross sectional 2006–2011 200 448 38.3/38.5
Cui2016 Prospective 2013–2015 920 298 –
Gaur2007 Retrospective 2001–2004 100 100 –
Meri2013 Retrospective 2010–2011 396 564 –
Mitra2012 Cross sectional –178 126 40.5/35.0
Trummer2002 Prospective 1993–2000 478 517 31.5/33.4
Mostafa2006 Prospective –20 20 –
Osser1992 Retrospective –186 164 –
Yu2013 Cross sectional 2011–2012 147 175 35.6/33.6
Zhang2013 Retrospective 2007–2010 737 775 29.6/29.9
Zhang2015 Retrospective 2013–2014 704 372 29.9/30.4
Dikshit1987 Prospective 1985–1986 219 288 26.7/26.5
Kunzle2003 Retrospective 1991–1997 655 1131 32.3/33.2
Total no of patients (n) 5257 5566
Abbreviations: Ssmokers, NS non-smokers
Fig. 1 Flow diagram representing the study selection
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Morphological defects of spermatozoa
There was a significant increase in the morphological
defects of spermatozoa (MD: 2.44, 95% CI: [0.99–3.89];
P= 0.001) including head (MD: 1.76, 95% CI: 0.32–3.20;
P= 0.02), neck (MD: 1.97, 95% CI: 0.75–3.18; P= 0.002)
and tail (MD: 1.29, 95% CI: 0.35–2.22; P= 0.007) defects
as shown in. Figure 5.
Hormones which were involved in reproduction
This analysis did not show any significant difference
in testosterone level (MD: 0.18, 95% CI: -1.26 –1.63;
P= 0.80), LH level (MD: 0.18, 95% CI: -0.47 –0.83;
P= 0.58) and prolactin level (MD: 1.79, 95% CI: -5.78
–9.36; P= 0.64) between smokers and non-smokers
asshowninFig.6. FSH level was also not signifi-
cantly decreased (MD: 0.12, 95% CI: -0.41 –0.64; P=
0.66) [Fig. 7].
Table 4has summarized the results of this analysis.
Sensitivity analysis showed that in the subgroup
analyzing for teratozoospermia, excluding study Mos-
tafa2002 showed a statistically significant result (RR:
1.32, 95% CI: 1.03–1.70; P= 0.03). Otherwise, consist-
ent results were obtained throughout all the other
subgroups.
Table 3 Other characteristics and reasons for exclusion of participants
Studies Type of participants Alcohol consumption Reasons for exclusion Patients
identification
Al-Turki2014 Primary and secondary
infertility
Alcohol consumption was
controlled
Patients with azoospermia Infertility clinic
Al-Turki2016 Primary and secondary
infertility
More than 87% of
participants do not
consume alcohol
Patients with azoospermia Infertility clinic
Anifandis2014 Not specified 59.9% participants do not
consume alcohol, and 28%
were moderate consumers
Infertility clinic
Caserta2012 Primary infertility Not specified Patients with azoospermia, orchitis or prostatitis,
grade 2 or 3 varicocele, undescended testes or its
surgery, altered karyotype
Infertility clinic
Cui2016 Primary infertility Not specified Cryptorchidism, varicocele, infections, anti-sperm
antibodies, chromosomal abnormalities
Infertility clinic
Gaur2007 Primary infertility Not specified Using contraceptive measures, secondary infertility,
occupational exposure to chemicals, cryptorchidism,
varicocele, chronic illness, leucocytospermia,
azoospermia, age > 45 years
Infertility clinic
Meri2013 Not specified Not specified Varicocele, undescended testes, small testes,
azoospermia, mumps, history of inguinal hernia
or scrotal surgery, chronic medical illness
Infertility clinic
Mitra2012 Not specified Not specified Pathology of chronic diseases Infertility clinic
Trummer2002 Not specified Not specified Not specified Infertility clinic
Mostafa2006 Not specified Not specified Not specified Infertility clinic
Osser1992 Not specified Not specified Not specified Infertility clinic
Yu2013 Not specified Not specified Unhealthy, varicocele, infection, obstruction of
the vas deferens, chromosomal abnormality,
azoospermia, severe oligozoospermia, hemospermia,
leukospermia, necrozoospermia
Infertility clinic
Zhang2013 Not specified Not specified Azoospermia, excessive alcohol intake, hallucinatory
drugs, serious systemic disease, abnormality of the
external genitalia, known family genital disorders,
infection or trauma to genitals
Infertility clinic
Zhang2015 Not specified Not specified Not specified Infertility clinic
Dikshit1987 Screening for idiopathic
infertility
No Past or present systemic disease, alcohol consumption,
genital tract disorder, varicocele, genital infection,
hormonal abnormalities or treatment, exposure to
radiation, drug abuse
Infertility clinic
Kunzle2003 Men attending the andrology
laboratory in the context of
infertility investigation
Yes History of orchitis, testicular trauma, sexually
transmitted
disease, varicocele, inguinal hernia operation and
cryptorchism.
Infertility clinic
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Discussion
As expected, this analysis showed smoking to have a sig-
nificant impact on the quantity and quality of sperms in
the infertile male participants. Tobacco smoking was as-
sociated with a lower sperm count and an increase in
the number of morphological defects including head,
neck and tail defects of spermatozoa. However, the pH
and motility of spermatozoa as well as the hormones
which were involved in reproduction were not affected
in this population of infertile males.
A recent meta-analysis which assessed human semen
showed tobacco smoking to have a negative impact on
semen parameters [26]. The analysis which consisted of
a total number of 5865 fertile and infertile men showed
a reduced sperm count and impaired motility in semen
samples of these young men. Even though the results
Fig. 2 Oligozoospermia and teratozoospermia observed in smoking and non-smoking infertile male participants
Fig. 3 Asthenozoospermia and azoospermia observed in smoking and non-smoking infertile male participants
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Fig. 4 Impaired motility of spermatozoa and pH of semen observed in smoking and non-smoking infertile male participants
Fig. 5 Morphological defects of spermatozoa observed in smoking and non-smoking infertile male participants
Bundhun et al. BMC Public Health (2019) 19:36 Page 7 of 11
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which were obtained were almost similar with respect to
this current analysis, the other analysis included only
studies which were published between the years 2010 to
2015, whereas our current analysis included studies
which were published even before the year 2010. An-
other difference with respect to the current analysis was
the fact that there was no language barrier in the other
analysis. Moreover, the other analysis also assessed re-
sults with reference to the total number of cigarettes
which were consumed daily. In contrast to the other
analysis, this current meta-analysis assessed specific
morphological defects, as well as any dis-balance of the
hormones which were involved in reproduction.
Another study evaluating the effect of cigarette smok-
ing on vital seminal parameters which influence fertility
showed smoking to cause impaired motility to a higher
extent in comparison to the impairment in sperm count
[27]. Men with primary infertility aged between 25 to 40
years were included and a follow-up period of less and
above 5 years were considered.
A case control study also showed smoking to be asso-
ciated with a lower semen concentration, impaired mo-
tility of spermatozoa and an increased morphology
defect [28] in part reflecting the results of this current
analysis. Additionally, an article published by the Canad-
ian Society of Clinical Chemists showed that abnormal
structural defects of spermatozoa, especially round head
defects, were associated with tobacco smoking which
might be attributed to increased oxidative stress and in-
sufficient scavenging antioxidant enzymes in the seminal
fluids of infertile men [29]. Other studies have shown
zinc to contribute to this unwanted mechanism in
Fig. 6 Hormones involved with reproduction observed in smoking and non-smoking infertile male participants (part 1)
Fig. 7 Hormones involved with reproduction observed in smoking and non-smoking infertile male participants (part 2)
Bundhun et al. BMC Public Health (2019) 19:36 Page 8 of 11
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infertile smokers [30]. Other mechanisms have well been
explained in previously published reviews [31,32].
Briefly, the possible mechanisms which might be in-
volved with the effect of cigarette smoking on semen pa-
rameters are: toxic contents found in cigarette smoking
might have harmful effects on male germ cells and their
developmental processes [33]. Negative effects of nico-
tine on semen parameters have also previously been re-
ported [34]. Other possible mechanisms might be
related to the negative impact of smoking on the 8
nAChR subunits found in human spermatozoa, resulting
in smoking-related sperm damage [35]. In addition, dif-
ferent proteins (Aldoa, ATP5a1, Gpx4, Cs) expressed in
sperms were significantly altered in smokers [36].
Cigarette smoking was found to also affect Ca
2+
- ATPase
activity of the spermatozoa as well [37].
However, even though clinical research has shown
smoking to have an adverse effect on the progressive
sperm motility irrespective of the total number of ciga-
rettes smoked daily [38,39], other studies showed no re-
lationship between smoking and male infertility [40].
This current analysis showed no significant influence
of smoking on testosterone, prolactin, FSH and LH
levels. To support this point, Wang et al. showed smok-
ing not to be an independent predictor of sex-hormone
binding globulin even though a relation or linked was
observed between increasing packets of cigarette and
sex-hormone binding globulin [41]. Similarly, another
study conducted in Taiwan showed no significant differ-
ence in LH and FSH levels between smokers and
non-smokers [42] showing smoking to have a much
higher impact on semen compared to the production of
hormones which were involved in the functioning of the
male reproductive system.
Several alternative methods to stop smoking have been
suggested [43–46]. However, apart from smoking, other
factors such as regular heavy alcohol consumption [47],
certain medications, co-morbidities, autoimmune diseases
and other environmental factors might also contribute to
abnormalities in semen parameters, morphology and
impaired motility and should further be investigated [48].
This interesting research should inspire other scientists
to investigate more about the mechanisms, the factors
associated with a poor semen quality in smokers; in order
for proper actions to be taken in a timely manner to
reduce this serious dilemma faced by several young men
and couples in our society.
This meta-analysis should be considered new for the fol-
lowing reasons: it is among the only few meta-analyses to
systematically show the impact of smoking on the quality
of semen in infertile males. This article might be consid-
ered new on the basis of the total number of participants
and the number of different endpoints which were
analyzed in one particular study.
Limitations
Limitations might be the fact that a high level of
heterogeneity was observed among several of the
subgroups analyzing the different endpoints. This
could be due to the inclusion of observational data.
In addition, several endpoints were analyzed only
using a small number of studies. Factors such as alco-
hol consumption could have had an influence on the
main results. Moreover, the infertility duration, and
other associated factors such as genital infections,
varicocele, environmental factors were not clearly re-
ported in several studies.
Table 4 Results of this analysis
Endpoints No of studies involved (n) RR or MD with 95% CI P value I
2
(%)
Oligozoospermia 4 1.29 [1.05–1.59] 0.02 0
Teratozoospermia 3 1.22 [0.96–1.56] 0.10 0
Asthenozoospermia 4 1.42 [0.97–2.09] 0.07 85
Azoospermia 2 3.02 [0.23–40.01] 0.40 92
pH of semen 4 0.04 [−0.03–0.11] 0.30 92
Impaired motility of sperm (continuous data) 4 1.26 [−0.64–3.17] 0.19 87
Abnormal form of sperm 6 2.44 [0.99–3.89] 0.001 98
Head defects 3 1.76 [0.32–3.20] 0.02 96
Neck defects 3 1.97 [0.75–3.18] 0.002 99
Tail defects 3 1.29 [0.35–2.22] 0.007 98
Testosterone level 4 0.18 [−1.26–1.63] 0.80 94
LH level 3 0.18 [−0.47–0.83] 0.58 66
Prolactin level 2 1.79 [−5.78–9.36] 0.64 95
FSH level 3 0.12 [−0.41–0.64] 0.66 0
Abbreviations: MD mean difference, RR risk ratio, CI confidence intervals, LH luteinizing hormone, FSH follicle stimulating hormone
Bundhun et al. BMC Public Health (2019) 19:36 Page 9 of 11
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Conclusions
In conclusion, with reference to the clinical endpoints
which were studied in this analysis, tobacco smoking
was associated with a lower sperm count and an increase
in the number of morphological defects of spermatozoa.
However, the pH and motility of spermatozoa as well as
the production of hormones which were involved in
reproduction were not affected in this population of in-
fertile males.
Abbreviations
CI: confidence intervals; FSH: follicle stimulating hormones; LH: luteinizing
hormone; RR: risk ratios
Acknowledgements
Not applicable.
Funding
No external funding was used in the preparation of this manuscript. This
research was supported by National Natural Science Foundation of China
(No. 81560046, 81760057) and Guangxi Natural Science Foundation (No.
2016GXNSFAA380002).
Availability of data and materials
All data and materials used in this research are freely available. References
have been provided.
Authors’contributions
PKB, GJ, MZSS, AB, ART, MP and FH were responsible for the conception and
design, acquisition of data, analysis and interpretation of data, drafting the
initial manuscript and revising it critically for important intellectual content.
PKB wrote this manuscript. All authors read and approved the final
manuscript as presented.
Authors’information
Dr. Pravesh Kumar Bundhun (M.D) is the first author. From the Department
of Internal Medicine, the First Affiliated Hospital of Guangxi Medical
University, Nanning, Guangxi, China.
Ethics approval and consent to participate
Ethical approval was not applicable for this systematic review and meta-
analysis.
Consent for publication
Not applicable.
Competing interests
The authors declare that they have no competing interests.
Publisher’sNote
Springer Nature remains neutral with regard to jurisdictional claims in
published maps and institutional affiliations.
Author details
1
Department of Internal Medicine, the First Affiliated Hospital of Guangxi
Medical University, Nanning, Guangxi 530021, People’s Republic of China.
2
Guangxi Medical University, Nanning, Guangxi 530027, People’s Republic of
China.
3
Institute of Cardiovascular Diseases and Guangxi Key Laboratory Base
of Precision Medicine in Cardio-cerebrovascular Disease Control and
Prevention and Guangxi Clinical Research Center for Cardio-cerebrovascular
Diseases, the First Affiliated Hospital of Guangxi Medical University, Nanning
530021, Guangxi, China.
Received: 31 March 2018 Accepted: 12 December 2018
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