Smoking and infertility: a committee opinion
Smoking and infertility:a committee opinion
The Practice Committee of the American Society for Reproductive Medicine
American Society for Reproductive Medicine, Birmingham, Alabama
Approximately 30% of women of reproductive age and 35% of men of reproductive age in theUnited States smoke cigarettes. Substantial harmful effects of cigarette smoke on fecundity andreproduction have become apparent but are not generally appreciated. This document replaces
the 2008 ASRM Practice Committee document of the same name. (Fertil SterilÒ 2012;-:-–-.
Ó2012 by American Society for Reproductive Medicine.)
Discuss: You can discuss this article with its authors and with other ASRM members at
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ent but are not generally appreciated.
medical subject headings ‘‘smoking,’’
tobacco,’’ ‘‘oocyte,’’ ‘‘sperm,’’ ‘‘fertil-
ity,’’ ‘‘pregnancy,’’ ‘‘complications,’’
and ‘‘conception.’’ The reference lists
was restricted to published articles. Re-
tive hazards for both females and males.
jority of the studies were case series and
increase the likelihood that their patients
discussion of additions and deletions.
Overall, the literature strongly supports
Received July 30, 2012; accepted July 31, 2012.
Correspondence: Practice Committee, American Society for Reproductive Medicine, 1209 Montgom-
ery, Hwy., Birmingham, AL 35216 (E-mail:
and also provides an importanteducational and motivational
Fertility and Sterility® Vol. -, No. -, - 2012 0015-0282/$36.00
Copyright 2012 American Society for Reproductive Medicine, Published by Elsevier Inc.
study yielded an overall OR and 95% conﬁdence interval
(CI) for infertility in smoking compared with nonsmokingwomen across all studies designs of 1.60 (CI 1.34–1.91). In co-
Public knowledge of the risks of smoking.
hort studies, the OR for conception delay over one year in
smoking versus nonsmoking women was 1.42 (CI 1.27–
1.58), and in case-control studies, the OR for infertility versus
fertility in smokers compared with nonsmokers was 2.27 (CI
1.28–4.02). The narrow CI suggests that the summary OR is
a reasonably accurate estimate of the effect and that the
results are unlikely to have arisen by chance. Most of the stud-
ies excluded from the meta-analysis also support the ﬁndings
that the prevalence of infertility is higher, fecundity is lower,
Practice Committee. Smoking and infertility. Fertil Steril 2012.
and the time to conception is increased in smokers comparedwith nonsmokers. In some studies, the effects on fertility wereseen only in women smoking more than 20 cigarettes per day,
Speciﬁcity: The speciﬁcity of the association between
but a trend for all levels of smoking was identiﬁed.
smoking and infertility is not strong. The possibility
Furthermore, a large scale population-based study dem-
remains that other confounding variables are in-
onstrated that smoking negatively affects fecundity, indepen-
volved, as suggested by the relationship between
dent of other factors The investigators studied data from
cigarette smoking and tubal factor infertility.
nearly 15,000 pregnancies to determine time to conception. In
Temporal Sequence: Most studies that have examined the
addition to smoking, factors such as parental age, ethnicity,
relationship between smoking and infertility have
education, employment, housing, pre-pregnancy body mass
been retrospective and therefore unable to assess any
index, and alcohol consumption were assessed for their pos-
sible confounding inﬂuences. Active smoking was associated
with increased failure to conceive within both 6- and 12-
month durations of study. Increasing delay to conception cor-
biological plausibility for an adverse effect of smoking
related with increasing daily numbers of cigarettes smoked.
on the ovary, oocytes, and the reproductive tract .
The percentage of women experiencing conception delay
Various known toxins have been identiﬁed in the
for over 12 months was 54% higher for smokers than for non-
ovary and/or follicular ﬂuid of smokers .
smokers. Active smoking by either partner had adverse ef-
Smoking has been associated with short menstrual
fects, and the impact of passive cigarette smoke exposure
cycle length (%24 days), which could result in
alone was only slightly smaller than for active smoking by
reduced fecundity The evidence cited earlier
suggesting accelerated follicular depletion and anearlier age of menopause further supports thebiological plausibility of an adverse impact of
Menopause occurs one to four years earlier in smoking
If a causal relationship between cigarette smoking and fe-
women than in nonsmokers The dose-dependent
male infertility is accepted, up to 13% of female infertil-
nature of the effect supports the contention that smoking
ity may be caused by smoking, based on the 1.6 odds
may accelerate ovarian follicular depletion. Chemicals in cig-
ratio (OR) from meta-analysis and assuming a 25%
arette smoke appear to accelerate follicular depletion and the
prevalence of smoking in women of reproductive age .
loss of reproductive function Mean basal follicle-stimu-lating hormone (FSH) levels are signiﬁcantly higher in young
smokers than in nonsmokers In one study, basal FSHlevels were 66% higher in active smokers than in nonsmokers
and 39% higher in passive smokers than in nonsmokers .
Urinary estrogen excretion during the luteal phase in smokers
Several comprehensive reviews have summarized the cumu-
is only about one-third that observed in nonsmokers ,
lative data on cigarette smoking and female fecundity and
possibly because constituents of tobacco smoke inhibit
all support the conclusion that smoking has an adverse
granulosa cell aromatase Current smoking is also
studies are largely observational and include diverse
in late reproductive age and perimenopausal women
populations, there is considerable potential for bias from
Mean gonadotropin dose requirements for smokers
receiving stimulation for in vitro fertilization (IVF) are higher
A meta-analysis identiﬁed the pertinent literature avail-
when compared with those of nonsmoking women The
able from Medline and Embase databases from 1966 through
higher prevalence of abnormal clomiphene citrate challenge
late 1997 and included 12 studies meeting strict inclusion
test (CCCT) results in smokers than in age-matched non-
criteria . Data from 10,928 exposed women and 19,179
smokers further provides evidence that smoking has adverse
unexposed women were entered into these analyses. The
Five of seven heterogeneous studies (includingthe only prospective study) of natural conception in female
The effect of smoking on male fertility is more difﬁcult to dis-
smokers have found an increased miscarriage risk . In
cern. The effects of smoking and passive smoke on various
one study of inner-city women 14–39 years of age, smoking
semen parameters have been evaluated .
accounted for 16% of miscarriages . Mechanisms have
Reductions in sperm density, motility, antioxidant activity,
not been completely elucidated. There are few data investigat-
and a possible adverse effect on morphology have been
ing chromosomal effects of smoking within abortus tissue,
demonstrated The decrease in sperm concentration
but the vasoconstrictive and antimetabolic properties of
averaged 22% and was dose-dependent. Use of smokeless
some components of cigarette smoke such as nicotine, carbon
tobacco also has a dose-dependent negative effect on multiple
monoxide, and cyanide may lead to placental insufﬁciency
semen parameters . Although sperm concentrations, motil-
and embryonic and fetal growth restriction and demise. How-
ity, and/or morphology often are reduced compared with results
ever, smokeless tobacco also is associated with increased risk
observed in nonsmokers, they often remain within the normal
of pregnancy loss , suggesting that nicotine alone is
range. However, the available evidence suggests that smoking
may have adverse effects on sperm function based on a study
Smoking also has been associated with bacterial vagino-
involving the zona-free hamster egg penetration test The
sis (which in turn is associated with second-trimester miscar-
available data do not demonstrate conclusively that smoking
riage) and with preterm labor . The risk of multiple
decreases male fertility . Few studies have or
gestations also may be increased in smokers .
can address the question, because of the confounding effects
Although it is difﬁcult to control for involvement of other
of partner smoking habits and fecundity.
lifestyle factors, an association between ectopic pregnancy
and smoking also has been reported A case-controlstudy identiﬁed a dose-related risk for ectopic pregnancy
Gametogenesis appears to be vulnerable to damage from
among smokers Women who smoked more than 20 cig-
tobacco smoke . Both chromosomal and DNA damage to
arettes daily had an OR for ectopic pregnancy of 3.5 (95% CI
human germ cells may result from tobacco smoke exposure
1.4–8.6) compared with nonsmokers.
The proportion of diploid oocytes in the ovary increases
Pickup of the oocyte cumulus complex and ciliary beat
with the number of cigarettes smoked per day (P<0.001), an
frequency were found to be inhibited in hamster oviduct sub-
observation suggesting that smoking may disrupt function
jected to cigarette smoke in a perfusion chamber . These
of the meiotic spindle in humans . Moreover, smoking
abnormalities may contribute to increased incidences of
in pregnant women is associated with an increased risk of tri-
ectopic pregnancy and tubal infertility in smoking women.
somy 21 offspring resulting from maternal meiotic nondis-junction . The prevalence of Y chromosome disomy (twohomologous Y chromosomes) in sperm correlates with uri-
Effects of Maternal Smoking on Male Progeny
nary cotinine concentrations, a marker of recent exposure
An epidemiologic study to identify the cause of decreasing
sperm counts in Danish versus Finnish men has suggested
Evidence suggests that gene damage in sperm may relate
an effect of maternal smoking After adjusting for con-
to direct binding of tobacco smoke constituents or their inter-
founding factors, men whose mothers had smoked more
mediates to DNA When bound to DNA, some of these
than 10 cigarettes per day had lower sperm densities than
‘‘adducts’’ represent premutational lesions.
men with nonsmoking mothers. Paternal smoking was unre-
Cigarette smoke contains toxic oxygen reactive species that
lated to semen parameters of the offspring. It is possible that
help produce adducts and are mutagenic in their own right.
these effects on male offspring could be mediated by cad-
Nuclear DNA damage and mitochondrial and cytoskeletal
mium or other contaminants of cigarette smoke. Together
aberrations have been shown to result directly from
with a reduction in fecundity and early pregnancy effects,
oxidative stress in gametes, likely in part via adduct
these effects on progeny may add substantially to the overall
formation. These mechanisms are supported by the ﬁnding
adverse reproductive burden from smoking.
of increased chemical adducts in embryos from smokerscompared with nonsmokers, indicating transmission ofmodiﬁed DNA originating from parental smoking .
Inﬂuence on Assisted Reproduction Outcomes
Gamete DNA damage may cause many of the recognized
Ten retrospective and four prospective studies have been
adverse reproductive effects of smoking such as increased
included in one or more of three meta-analyses that have ex-
miscarriages, accelerated onset of menopause, and reduced fe-
amined the effects of smoking on the outcome of pregnancies
cundity. Increases in birth defects veriably have been reported
achieved via in vitro fertilization (IVF) or gamete intrafallo-
among the offspring of smoking parents, but the teratogenic
pian transfer (GIFT) . Most of these studies of
effects of cigarette smoke during pregnancy confound
assisted reproduction have low power and failed to adjust
whether DNA damage in gametes may play a role .
for confounders. Meta-analysis of nine of the studies identi-ﬁed an OR of 0.66 (95% CI 0.49–0.88) for conception among
smokers undergoing IVF . Another meta-analysis of seven
Smoking is associated with an increase in spontaneous
relevant studies in addition to the authors' own prospective
miscarriage in both natural and assisted-conception cycles
data yielded an OR of 1.79 (95% CI 1.24–2.59) for the quotient
of successful ﬁrst IVF cycles for nonsmokers over smokers
smoking cessation in infertile women found that a relatively
the result suggested that smokers require nearly twice
simple and inexpensive approach based on individualized
the number of IVF cycles to conceive as nonsmokers.
counseling regarding the risks of smoking was reasonably ef-
The speciﬁc adverse effects of smoking on reproductive
fective, increasing the proportion of women who quit smok-
processes cannot be deﬁned precisely because reported out-
ing from 4% at baseline to 24% after 12 months of
comes have been heterogeneous. Yet studies of IVF and
intervention This study method involved several minutes
GIFT have variously reported an increased gonadotropin
of counseling, education, and encouragement during each
requirement for ovarian stimulation, lower peak E2 levels, el-
clinic visit, according to the patient's individual stage of read-
evated testosterone, fewer oocytes retrieved, higher numbers
iness to quit. This method was more successful than just pro-
of canceled cycles, thicker zona pellucida, lower implantation
viding educational materials and website addresses alone .
rates, and more cycles with failed fertilization in smokers
In general populations, various interventions including
behavior modiﬁcation, group counseling, feedback, advice,
examined speciﬁcally the effects of cigarette smoking on
and nicotine weaning with patches and gum have proven ef-
ovulation induction outcomes. The detrimental effect of
fective. However, only 5% of women referred to a specialty
smoking cessation clinic actually attended. Regularly sched-
undergoing treatment . The effects of smoking
uled ofﬁce visits and use of multiple interventions are more ef-
and advancing age may therefore synergize to accelerate
fective, albeit resource-intensive. In infertile women, carbon
monoxide (CO) monitoring using an inexpensive hand-held
Possible mechanisms of compromised oocyte quality
spirometer also may be of beneﬁt. Results correlate well
include the presence of toxins derived from tobacco smoke
with the self-reported number of cigarettes smoked and offer
in follicular ﬂuid. The follicular ﬂuid concentrations of the
feedback to patients. Serum and urine cotinine concentrations
heavy metal cadmium a known ovarian toxin, are higher
also have been used effectively for the same purpose .
in smokers than in nonsmokers. Likewise, the concentrations
The Public Health Service and National Cancer Institute
of cotinine (a major metabolite of nicotine) in the follicular
offer validated ofﬁce-based intervention guidelines for smok-
ﬂuid aspirated from women at time of egg retrieval in IVF cy-
ing cessation that incorporate and extend the above-
cles relate directly to the number of cigarettes smoked . All
described recommendations . A ﬁve-step approach is
women known to be exposed to passive smoke in the home
suggested: 1) Ask about smoking at every opportunity; 2)
also had detectable follicular ﬂuid cotinine levels, albeit at
Advise all smokers to stop; 3) Assess willingness to stop; 4)
lower concentrations. Also concerning was the ﬁnding that
Assist patients in stopping (including the use of pharmaceu-
84% of women who reported themselves as nonsmokers
ticals and CO monitoring); and 5) Arrange followup visits
with nonsmoking partners had detectable levels of cotinine
Speciﬁc smoking-cessation protocols for pregnant
in their follicular ﬂuids These women were exposed en-
women have been outlined in several recent reviews
vironmentally, with all but one working outside the home.
Other helpful resources for smoking cessation for
These data emphasize the potential hazards from passive
health-care providers and patients are available from
A more recent study not included in the meta-analyses
American Cancer Association) via their websites.
also concluded that smoking has adverse effects on concep-
Although medical adjunctive therapy for smoking cessa-
tion rates in assisted reproduction treatment (ART) cycles
tion has not been studied in infertile women, it may be justi-
Uniquely, this was a ﬁve-year prospective study that
ﬁed for some. When behavioral approaches fail, the use of
controlled for potential confounders to the effects of smoking
nicotine replacement therapy (NRT) and/or bupropion has
and analyzed the quantity, frequency, and duration of smok-
resulted in a two-fold increase in the proportion of non-
ing exposure among 221 couples. A dose-response effect for
pregnant women able to quit smoking .
number of cigarettes smoked could not be demonstrated but
Available medical therapies include NRT in the form of
was apparent for the duration of smoking. If a woman ever
gum and patches (both available over the counter) as well
smoked during her lifetime, her risk of failing to conceive
as nasal sprays and inhalers. Because the latter two have
via ART more than doubled (relative risk ¼ 2.5, 95% CI
not been studied in pregnancy and are classiﬁed as category
1.38–4.55, P<0.01). Each year that a woman smoked was as-
D agents (there is positive evidence of human fetal risk based
sociated with a 9% increase in the risk of unsuccessful ART
on adverse reaction data from investigational or marketing
cycles (95% CI 1.02–1.15, P<0.01).
experience or studies in humans), NRT via nasal inhalers
Overall, it appears that ART may not necessarily be able to
and sprays are best avoided in pregnant women and women
overcome the reduction in natural fecundity associated with
attempting to conceive. Nicotine gum carries a category C
classiﬁcation and the nicotine patch is a category D agent,despite its reported safety in the limited clinical studies
involving pregnant women that have been conducted to date.
Unfortunately, even among pregnant women who may
The only non-nicotine Food and Drug Administration
understand the risks of smoking, concerted efforts to help
(FDA)-approved smoking cessation agent is the aminoketone
them quit smoking have been only modestly effective .
bupropion (Zybanª, GlaxoSmithKline) Bupropion is also
Smoking cessation rates generally are better for infertile
available for use as an antidepressant (Wellbutrinª, Glaxo-
women than for pregnant women. The only study to examine
SmithKline) but is marketed differently (Zybanª) for smoking
cessation with a category B classiﬁcation. The efﬁcacy of bu-
have reproductive consequences as great as those observed
propion appears similar to that of NRT strategies. Although
studies of both bupropion and NRT in pregnant women
Clinicians can facilitate smoking cessation by providing
have been limited, no adverse effects for pregnant women
education, monitoring, and consistent individualized
or their fetuses have been reported thus far. Ideally, however,
pharmacological smoking cessation therapies are best usedprior to conception.
When the likelihood of achieving smoking cessation is
The accumulated evidence supports the value of taking a pre-
high and its beneﬁts appear to outweigh the combined risks
ventive approach to infertility by discouraging smoking and
of smoking and NRT in pregnant or potentially pregnant
helping to eliminate exposure to tobacco smoke in both
women, NRT may be reasonable. The nicotine levels that
result from daily inhalation of 10 or more cigarettes are higherthan those associated with recommended doses of nicotine
gum and patches Eliminating the exposure to the
direction of the Practice Committee of the American Society
many other chemicals contained in cigarette smoke is one
for Reproductive Medicine as a service to its members and
clear advantage of NRT No studies have directly compared
other practicing clinicians. Although this document reﬂects
bupropion and NRT in infertile or pregnant women. However,
appropriate management of a problem encountered in the
given the relative safety and generally good compliance with
practice of reproductive medicine, it is not intended to be
prescribed bupropion treatment, it would appear to be an
the only approved standard of practice or to dictate an exclu-
acceptable initial medical intervention, when needed.
sive course of treatment. Other plans of management may be
On average, female smokers referred for evaluation and
appropriate, taking into account the needs of the individual
treatment of infertility have tried to quit smoking three times
patient, available resources, and institutional or clinical prac-
previously. Sadly, only 18% of such women have received ad-
tice limitations. The Practice Committee and the Board of
vice on smoking cessation from their referring physicians .
Directors of the American Society for Reproductive Medicine
The likelihood of achieving smoking cessation appears to in-
crease with each attempt and physicians who care for
The following members of the ASRM Practice Committee
infertile women have another opportunity to help them quit
participated in the development of this document. All Com-
smoking, beginning with their initial visit.
mittee members disclosed commercial and ﬁnancial relation-
The substantial reproductive risks associated with smok-
ships with manufacturers or distributors of goods or services
ing and the revelation that much of the reduced fecundity
used to treat patients. Members of the Committee who were
associated with smoking may be reversed within a year of ces-
found to have conﬂicts of interest based on the relationships
sation can be powerful incentives when included
disclosed did not participate in the discussion or development
in physician counseling. When successful, smoking cessation
of this document. Samantha Pfeifer, M.D.; Marc Fritz, M.D.;
represents an important part of effective treatment for
Jeffrey Goldberg, M.D.; R. Dale McClure, M.D.; Michael
Thomas, M.D.; Eric Widra, M.D.; Glenn Schattman, M.D.;Mark Licht, M.D.; John Collins, M.D.; Marcelle Cedars,
M.D.; Catherine Racowsky, Ph.D.; Owen Davis, M.D.; KurtBarnhart, M.D., M.S.C.E.; Clarisa Gracia, M.D., M.S.C.E.;
Available biologic, experimental, and epidemiological data
William Catherino, M.D., Ph.D.; Robert Rebar, M.D.; Andrew
indicate that up to 13% of infertility may be attributable to
Smoking appears to accelerate the loss of reproductive
function and may advance the time of menopause by 1 to
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I st INDO-FRENCH LEGAL FORUM MEET Intellectual property rights-such as copyrights, patents, trademarks, and so on-offer the legal protection upon which authors, inventors, firms, researchers, and others rely to protect their creations. Intellectual property rights dictate what use can legally be made of the creative work, and are thus essential to ensuring that authors are rewarded for
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